Download The evolution of water transport in plants: an integrated

DOI: 10.1111/j.1472-4669.2010.00232.x
Geobiology (2010), 8, 112–139
The evolution of water transport in plants: an integrated
approach
J. PITTERMANN
Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA, USA
ABSTRACT
This review examines the evolution of the plant vascular system from its beginnings in the green algae to modern
arborescent plants, highlighting the recent advances in developmental, organismal, geochemical and climatological research that have contributed to our understanding of the evolution of xylem. Hydraulic trade-offs in vascular structure–function are discussed in the context of canopy support and drought and freeze–thaw stress
resistance. This qualitative and quantitative neontological approach to palaeobotany may be useful for interpreting the water-transport efficiencies and hydraulic limits in fossil plants. Large variations in atmospheric carbon
dioxide levels are recorded in leaf stomatal densities, and may have had profound impacts on the water conservation strategies of ancient plants. A hypothesis that links vascular function with stomatal density is presented
and examined in the context of the evolution of wood and ⁄ or vessels. A discussion of the broader impacts of
plant transport on hydrology and climate concludes this review.
Received 14 September 2009; accepted 26 December 2009
Corresponding author: J. Pittermann. Tel.: +1 831 459 1782; fax: +1 831 459 5353; e-mail: pittermann@
biology.ucsc.edu
INTRODUCTION
Plants can control climate as well as respond to it. Recent
models supported by independent isotopic evidence suggest
that it was the evolution of large, Devonian land plants that
may have contributed to the dramatic reductions in atmospheric CO2 in the Late Devonian (Beerling & Berner, 2002;
Berner, 2005, 2006) while progressively deeper and more
complex root systems accelerated pedogenesis and carbon
sequestration (Retallack, 1997; Algeo & Scheckler, 1998;
Raven & Edwards, 2001; Berner, 2005). Although the contribution of plants to atmospheric and biogeochemical processes
continues to be well explored (Pataki et al., 2003; Bonan,
2008; Malhi et al., 2008), the role of plant water transport in
responding to or acting on both of these components has
been somewhat overlooked.
There is a direct link, however, between plant water
transport and climate. Indeed, important inferences about the
levels of palaeoatmospheric CO2 have been based on measurements of stomatal distributions in fossil plants. Stomata are
microscopic pores on surfaces of green leaves and stems that
allow CO2 to diffuse into photosynthetic tissue, while letting
water escape. Analysis of fossil plant material across the Phanerozoic suggests that low stomatal densities reflect elevated
palaeoatmospheric CO2 levels, whereas the opposite is true
for high stomatal densities (McElwain & Chaloner, 1996;
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Chaloner & McElwain, 1997; McElwain et al., 1999; Retallack, 2001; Beerling, 2002; Roth-Nebelsick, 2005; Kurschner
et al., 2008). Apparently, a greater number of smaller stomata
are needed to counter CO2 deficits at low ambient CO2,
rather than fewer, but larger stomata (Franks & Beerling,
2009a). However, stomata must also regulate water loss from
the leaf because, for each CO2 molecule fixed by the plant,
200–400 molecules of water may escape through the stomatal
pore. At any point in time, the stomata must optimize plant
water use efficiency, which is the carbon gain for a given
amount of water lost. This trade-off and its implications on
plant water balance, hydraulics and structure–function may
have been apparent early in the evolution of vascular land
plants.
What are the climatic consequences of transpiration for
atmosphere–biosphere interactions and does the answer lie
once again in the stomatal impressions of ancient leaves? How
has the evolution of water transport impacted the overall
design of both ancient and modern flora? The goal of this
review is to address these issues in an interdisciplinary and
accessible manner that draws not only on the fossil record, but
also on the recent advances in molecular, physiological and
evolutionary plant biology. Parts I and II introduce the basics
of the cohesion–tension (C–T) theory of water transport and
examine the evolutionary and developmental transitions that
selected for this ubiquitous and broadly accepted mechanism
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The evolution of water transport in plants
from the earliest vascular land plants to trees. Part III highlights recent advances in our understanding of the structure
and function of plant vascular tissue (xylem), and its potential
utility for the reconstruction of water transport in extinct taxa
from climates that were radically different from today. The
review concludes with a discussion of the significance of plant
water transport on ecosystem and global hydrology.
PART I: THE EVOLUTION OF WATER
TRANSPORT IN TERRESTRIAL PLANTS
Much of the information in Part I draws from the fossil
record, which is both rich with information yet fundamentally
incomplete. Indeed, the fossil record has limited resolution
with respect to the physiological, biochemical and life-history
traits that are integral to understanding the transition of
photosynthesis from an aquatic to a terrestrial setting. Computer models, systematics and developmental approaches can
fill some of these gaps, but the veracity of these hypotheses is
ultimately tested against fossils.
Thus, fossil specimens are scrutinized with much caution.
The majority of fossils are preserved in riverine depositional
environments, meaning that they may have travelled great
distances from potentially very different habitats before
settling permanently (Stewart & Rothwell, 1993; Taylor
et al., 2009). Furthermore, fragmentation can disassociate
fragile structures such as leaves from the rest of the plant body,
thereby obscuring relationships between various tissue samples and potentially inflating species numbers. For instance, it
was not until the discovery of an intact specimen bearing both
wood and foliage that Archaeopteris was treated as a single
species rather than two separate genera (Beck, 1960; MeyerBerthaud et al., 1999). Lastly, diagenesis, that is the chemical
and physical alteration of fossil and sediment during the
conversion to rock, can also cause substantial changes to the
structure and character of a specimen (Taylor et al., 2009).
Sampling biases may affect approximations of species
diversity in the fossil record leading to errors in estimates of
the rates of evolution, particularly if workers focus on particular localities or intervals. In general, if diversity is constant,
sampling intensity will not affect results (Raymond & Metz,
1995; Tarver et al., 2007). However, evidence suggests that
earlier estimates of diversity of Mid-Silurian through Late
Devonian land plants may be higher than expected due to sampling bias, usually attributed to workers’ preferential interest
in one era or locality over another (Raymond & Metz, 1995).
Fortunately, plant vasculature is often the most abundant
and best preserved plant tissue. Indeed, some xylem samples
from the earliest land plants appear as though they were
frozen in time, with little distortion to the cell structure.
Remarkably, even the chemical composition of early vascular
tissue can be discerned to the point where we can reasonably
speculate about the biomechanical properties of the stem, as
well physiological ecology of the plant (Kenrick & Crane,
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1991; Bateman et al., 1998; Boyce et al., 2003; Wilson et al.,
2008). For this reason, macroevolutionary and neontological
approaches can be fruitfully applied to research addressing
evolution of plant water transport, or the relationships of fossil
plants to their climates.
The mechanism of water transport in plants
Water transport in plants is not difficult to understand, but neither is it inherently intuitive. In his book ‘Vegetable Staticks’
(1727), the English physiologist Stephen Hales first remarked
that water is released from a plant by ‘perspiration’. He thus
captured an important element of the C–T theory, which
requires that water is lost from the plant by evaporation in
order for bulk flow to occur. The C–T theory was fully developed by Dixon and Joly (1894), and remains to this day the
most parsimonious and experimentally supported explanation
of plant hydration. The fundamental tenet of the C–T mechanism is that the water column can sustain a very high degree of
tension without ‘breaking’. This phenomenon is entirely consistent with the properties of water, yet so unusual that a few
workers find the C–T mechanism disturbing. Despite recent
controversy, the C–T mechanism has withstood vigorous
experimental scrutiny and remains the most widely accepted
explanation of water movement in land plants (Pockman et al.,
1995; Cochard et al., 2001; Angeles et al., 2004).
Water may be transpired at a high rate from the stomatal
pores, so effective hydraulic transport must efficiently replace
this lost water. Failure to supply water to the shoot as quickly
as it is lost results in the familiar phenomenon of wilting followed by damage to cell membranes and ending with death
(McDowell et al., 2008). Roots are a crucial component for
water entry into the plant yet for the most part, it is the aerial
tissues that drive water movement, much like cut flowers in a
vase.
The process of water transport begins when water is lost
from the mesophyll cell walls located in the interior of the leaf.
Plant cell walls are a tight but porous weave of cellulose and
pectin that act much like a wick. This evaporation creates
capillary suction on the menisci within the cell wall pores,
causing tension to be transmitted down the water column in
the xylem (Pickard, 1981). The xylem tension exists because
the water column is engaged in a ‘tug-of-war’ between
adhesion to soil particles and evaporation from the leaf surface. This tension can also be described as a ‘negative pressure’
that is quantitatively referred to as the water potential (W) and
typically measured in Pascals (Pa) such that increasingly negative water potentials indicate greater tension imposed on the
water column. Because water moves down a water potential
gradient and the water potential of the roots is more negative
than that of the surrounding soil, water enters the roots.
Water movement in plants is referred to as the C–T mechanism because hydrogen bonding holds the water molecules
together and their movement is the result of the pulling action
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(i.e. tension) created by evaporation from the cell wall pores
(Sperry, 2000; Tyree & Zimmermann, 2002; Taiz & Zeiger,
2006).
Because transpiration is chiefly driven by sunlight, water
movement through plants is a passive and therefore cheap
process that selected for low resistance, efficient transport
conduits (Sperry, 2003). These are dead, empty, require little
to no metabolic input and can provide a network that allows
water to reach tree canopies over 100 m in height (Koch
et al., 2004; Burgess et al., 2006; Domec et al., 2008).
Underlying this transport capacity is a fundamentally simple
mechanism whose origins required little more than a hydrophilic cell wall to move water by capillarity. Green algae
possess such a cell wall for the purpose of osmoregulation, so
the framework for the evolutionary transition from wicking
water over the surface of a cell to bulk flow within the specialized conduits of vascular plants was realized well before the
colonization of land (Sperry, 2003; Franks & Brodribb,
2005). In addition to the cell wall, the key innovations that
allowed plants to maintain hydration and adequate rates of gas
exchange on land were the cuticle, the stomata and the evolution of vascular tissue. The functional significance, evolutionary history and developmental elements of these traits will be
addressed below.
The green algae: earth’s first land plants
The connection between land plants and green algae (Chlorophyta) has been apparent since centuries before Darwin’s
time, and there is no doubt that embryophytic land plants are
descendants of freshwater green algae (Graham, 1993;
Graham et al., 2000; Lewis & McCourt, 2004; McCourt
et al., 2004). Specifically, it is believed that for the Charophytic green algae lacking bicarbonate pumps, competition for
CO2 may have been the driving force behind their venture
onto land (Graham, 1993). Clearly, the photosynthetic
benefits of fourfold increased CO2 diffusivity and higher light
levels outweighed the costs of exposure to UV radiation and
dessication (Denny, 1993; Graham, 1993). A complete discussion of the morphological, biochemical and reproductive
adaptations predisposing Charophytic algae to life on land is
beyond the scope of this review, but excellent treatments can
be found in Graham (1993), Graham et al. (2009), Gensel
(2008) and Gensel & Edwards (2001). Because the fossil
record of the green algae is fragmentary and incomplete
(Graham, 1993), the discussion will be limited to recent progress regarding the algal ancestry of land plants.
The green algae display a surprising array of cellular and
colonial morphologies, and some species such as Chara
braunii, may superficially resemble plants (McCourt et al.,
2004). Although green algae are typically associated with
aquatic ecosystems, they can also be indigenous and highly
speciose elements of desert soil microbiotic communities
(Evans & Johansen, 1999). Although the most widely recog-
nized transition of green algae to land has been the one leading
to land plants, recent evidence indicates that the green algae
have colonized terrestrial surfaces on at least a dozen separate
occasions (Lewis & Lewis, 2005). Molecular clock hypotheses
suggest that the first green algae may have appeared in the
Mid-to-Late Mesoproterozoic (1.4–1.0 billion years ago;
Yoon et al., 2004) but the date of their venture onto land is
unclear due to poor preservation (Taylor et al., 2009). The
oldest observed silicaceous or calcium carbonate remains of
green algae are from the Upper Silurian (Feist et al., 2005).
Molecular phylogenies show high support for the two
Chlorophytic and Charophytic lineages of the green algae
(Lewis & McCourt, 2004; Fig. 1), and there is a general
consensus for the placement of the Charophytic lineage as
ancestral to land plants because of the high number of shared
derived molecular, biochemical, reproductive, developmental
and morphological traits between these groups (Graham,
1996; Raven & Edwards, 2004). Nonetheless, the issue of
which Charophytic group is most closely related to terrestrial
plants remains somewhat controversial primarily because of
different approaches to gene and taxon sampling (Qiu et al.,
2006, Qiu, 2008; McCourt et al., 2004; Gensel, 2008; see
also Turmel et al., 2007).
Despite the progress in elucidating the phylogenetic relationships of the green algae and their affinities to land plants,
the shared physiological and biochemical elements of dessication tolerance have attracted less attention (Graham & Gray,
2001). This comes despite Raven’s early efforts to provide
such a context for the evolution of Charophytes and his misgivings about the suitability of Charales to life on land based
on latter group’s physiology and morphology (Raven, 1977).
Perhaps, the plasticity of algal forms (Bhattacharya & Medlin,
1998), combined with the antiquity of the Charophyte
to embryophyte divergence, hopelessly complicates such a
mapping exercise (Graham & Gray, 2001) but it could
nonetheless inform the plausibility of current evolutionary
scenarios because environmental water stress exerts some of
the strongest selective pressures on terrestrial (and marine)
biota (Yancey et al., 1982).
Graham & Gray (2001) argue that the closest Charophytic
ancestors of land plants would have been dessication-tolerant
and occupied ephemeral, ‘variably unfavourable’ aquatic habitats.
These habitats acted as sites of strong evolutionary pressures
related to the effects of water deficit, and thus provided
the Charophytes with an impetus towards terrestrialization
(Graham & Gray, 2001). Consequently, the water status of
terrestrial Charophyceans would have fluctuated in response
to water availability (so-called poikilohydry), and the evolution
of desiccation tolerance would have been essential in allowing
them to recover from otherwise fatal (80–90%) protoplasmic
water loss. Dessication tolerance is a common phenomenon
in basal plant lineages characterized by small-statured phenotypes such as the algae, bryophytes and some ferns (Proctor &
Tuba, 2002). This trait has been lost, however, in more
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The evolution of water transport in plants
115
Fig. 1 The phylogeny of land plants in the context
of palaeoclimate and clade radiations over Phanerozoic time, updated from Sperry (2003). The graph
indicates modelled atmospheric CO2 concentrations
according to Berner (2006), as well as corresponding large-scale climatic patterns (Zachos et al.,
2001; Willis & McElwain, 2002; Berner, 2005; Huey
& Ward, 2005; Brezinski et al., 2008; Trotter et al.,
2008). The phylogeny is from Sperry (2003) with
updates from Burleigh & Mathews (2004) and Qiu
(2008). Important morphological features relevant
to the evolution of plant water relations are indicated on the phylogeny according to Sperry (2003)
with several updates (Proctor, 1981; Franks &
Farquhar, 2007; VanAller Hernick et al., 2008).
Presence in the fossil record is denoted by thick
black line. Relative tracheophyte abundances were
estimated or re-drawn from Niklas (1992, 1997),
Willis & McElwain (2002), Singh (2004) and
Montanez et al. (2007). There is good fossil
evidence to suggest that liverworts may have been
present as early as the Late Ordovician (dotted line;
Wellman et al., 2003).
derived plants due to structural constraints that prevent the
collapse and refilling of cells, as well as the high cost of solute
production required to minimize drought injury to cell
membranes and metabolic components (Beck et al., 2007).
The significance of the plant cuticle
Although multicellularity reduces water loss by reducing total
surface to volume ratios, it is unlikely that an algal colony
larger than few hundred cells could have maintained adequate
hydration for long periods of time without a means of restricting water loss, or efficiently replacing lost water. Additionally,
because a water film represents a significant barrier to CO2
diffusion, such a simple multicellular arrangement may have
significantly constrained photosynthesis (Franks & Brodribb,
2005). All land plants must then reconcile two opposing biophysical constraints. On the one hand, photosynthesis
requires large surface areas to facilitate light capture and CO2
diffusion, whereas on the other, water conservation favours
low surface:volume ratios. Three critical innovations – the
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cuticle, the stomata and water-conducting tissues – allowed
plants to resolve these conflicting requirements. Of these
three traits, the cuticle is the oldest. We currently know nothing about the evolution of the cuticle, except that it is a synapomorphy of land plants, the earliest fragments of which were
found in the Ordovician (Wellman et al., 2003). Nevertheless, one can neither discuss the evolution of plant homoihydry
(that is the ability to maintain hydration over a range of external conditions of water availability; Raven & Edwards, 2004;
Raven, 1984) nor the plant fossil record (Willis & McElwain,
2002; Wellman et al., 2003; Taylor et al., 2009) without
mentioning this feature.
The 1 to 15 lm thick cuticle covers most of the aerial
elements of land plants where it protects the shoot from
herbivory, UV-induced damage and water loss (Edwards
et al., 1996; McElwain & Chaloner, 1996; Raven & Edwards,
2004). The cuticle is essentially a waxy layer on the external
cell walls of the epidermis (Bargel et al., 2004, 2006), in
which cutin forms the highest fraction and acts as a matrix for
the deposition of fatty acids, alkanes and waxes. Because the
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cuticle can significantly restrict water loss, it is unlikely that
the colonization of land by plants would have occurred without the evolution of this layer (Niklas, 1992; Raven &
Edwards, 2004). Waxes are the key constituents of the cuticle
barrier but it is the cutin fraction that is most resilient to
degradation and thus best conserved in the fossil record
(Schreiber & Riederer, 1996). It is noteworthy that some
Charophytic algae can synthesize a wax-free extracellular layer
that may allow a limited amount of water and CO2 diffusion
(Graham, 1993; Edwards et al., 1996).
Historically, the usefulness of fossilized cuticle lay primarily
in the patterns of preserved stomatal impressions whose size,
distribution and abundance are used to infer palaeo-atmospheric CO2 concentrations (McElwain & Chaloner, 1996;
McElwain et al., 1999; Royer et al., 2001; Retallack, 2001;
Kouwenberg et al., 2003). Unfortunately, cuticle thickness
alone is a poor predictor of species’ drought tolerance because
cuticle permeability and thickness may not be related
(Edwards et al., 1996; McElwain & Chaloner, 1996). However, emerging work has shown that cuticle alkanes record the
deuterium isotope signatures (¶D) of meteoric water and can
serve as a accurate biomarkers for palaeoclimatic reconstruction, particularly if isotopic models take into account the
relationships between leaf wax ¶D patterns and latitude, plant
form and photosynthetic pathway (Sachse et al., 2004; Liu &
Yang, 2008). Because deuterium enrichment is also partially
controlled by transpiration and soil evaporation, n-alkanes
may also be useful in constraining estimates of transpiration or
evapotranspiration from well-preserved fossil material (Smith
& Freeman, 2006).
The evolution of stomata
The cuticle imposes a high degree of resistance on gaseous diffusion, so it must be perforated in order for CO2 to enter.
These perforations take the form of stomata, the 30- to 80-lm
long epidermal pores that are formed by the aperture of two
adjacent elongated guard cells and found on surfaces of most
photosynthetic tissue (Hetherington & Woodward, 2003;
Taylor et al., 2009). It is the turgor-mediated opening and
closing of the guard cells in response to leaf hydration, light
levels, atmospheric CO2, abscissic acid and soil water availability that controls the diffusion of CO2 and water vapour
between the leaf and the atmosphere (Davies & Zhang, 1991;
Assmann & Wang, 2001; Buckley, 2005; Messinger et al.,
2006; Ainsworth & Rogers, 2007). Stomatal conductance is
tightly coupled to hydraulic transport in land plants (Jones &
Sutherland, 1991; Brodribb & Holbrook, 2004), so stomatal
evolution may have occurred closely in time with the vascular
system (Kenrick & Crane, 1997; Sperry, 2003).
The position of stomata on the land plant phylogeny is
decided by the placement of ancestral taxa such as liverworts
and bryophytes, the standing of which has been called into
question (Raven, 2002). Some species of liverworts and
mosses exhibit what appear to be proto- or pseudo-stomata
but as the function of these pores in gas exchange is unclear
(see below; Duckett et al., 2009; Proctor, 1981), they may be
unsuitable candidates for stomatal precursors. Hence, true
stomata are currently accepted to be monophyletic, with their
origins in the hornworts (Raven, 2002).
Unfortunately, the fossil record is silent with regard to
changes in epidermal cells that may have led to the formation
of stomata, but simple perforations are apparent in the cuticles
of taxonomically mysterious taxa such as Spongiophyton
(Gensel et al., 1991) and Nematothallus from the Lower
Devonian (Edwards et al., 1998; Taylor et al., 2009). These
organisms had thick cuticles, so epidermal pores would have
significantly reduced resistance for gaseous diffusion. Similar
perforations found on the thalli of the extant liverwort,
Conocephalum conicum probably function in gas exchange
(Proctor, 1981; Raven & Edwards, 2004), but it is unlikely
that they exert dynamic control over water loss. Without
active regulation courtesy of the guard cells, these plants
passively and continually lose water in response to the atmospheric vapour pressure deficit.
The oldest unequivocal stomatal specimens have been
described from unidentified cuticle and tissue fragments from
the Pridoli epoch (Upper Silurian, 416–418.7 Mya, Upper
Silurian, Edwards et al., 1996, 1998). In these samples, the
stomatal apparatus appears nearly circular, consisting of two
thick guard cells that create a lenticular pore. Perhaps due to
poor preservation and small fragment size, there is no
evidence for a substomatal chamber and in several of these
Silurian samples, epidermal cells appear to underlie the guard
cells. Small substomatal cavities are found, however, in samples of pro-tracheophytes such as Rhynia gwynne-vaughanii,
Aglaophyton major, Horneophyton lignieri and the lycophyte
Asteroxylon mackiei from the Lower Devonian (397.5–
416 Mya; Edwards et al., 1998). These taxa generally have
low stomatal frequencies, and some such as Asteroxylon have
sunken stomata –features that are consistent with the idea that
water stress was the key abiotic variable acting on early terrestrial vegetation (Gray et al., 1985).
Based on our understanding of stomatal behaviour in
modern taxa, it has long been accepted that the evolutionary
pressures that drove water conservation strategies favoured
the coupling of the cuticle with stomata (Raven, 2002; Franks
& Brodribb, 2005). However, the underlying assumption
that the regulation of water loss was the impetus for the evolution of stomata (especially in early land plants) has recently
been challenged by Duckett et al. (2009) who argue that the
‘pseudostomata’ of the Sphagnum moss evolved to facilitate
dehydration in sporophytic capsules, rather than conserve
water. In this plant, it is dehiscence and collapse of guard cells
that opens the stomatal aperture, rather than an increase in
guard cell pressure, as typically observed in higher land plants.
Duckett et al.’s results leave the evolution of stomata open to
interpretation. One could argue that stomata initially
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The evolution of water transport in plants
appeared in mosses for the purpose of dehydration and were
subsequently adapted for gas exchange in higher plants, but
alternatively stomata could have evolved to facilitate gas
exchange on land, but were co-opted by the mosses for the
purpose of dehydration. A final option is that, in Sphagnum, the
stomata fulfil both functions over time (Duckett et al., 2009).
Duckett et al.’s study changes our perspective on the evolution of stomata and will undoubtedly motivate future work
on stomatal structure and function in modern taxa. Despite
the fact that stomatal design has remained fundamentally
unchanged, notable differences in size, density, shape and
ornamentation are apparent across the major plant groups
(Ziegler, 1987; Franks & Beerling, 2009a,b). The functional
significance of some of this variation apparently lies in the
tempo of stomatal movements whereby the derived, dumbellshaped stomata of grasses open and close much faster than
the classical kidney-shaped stomata of older lineages (Franks
& Farquhar, 2007). The authors argue that faster response
times of graminoid stomata may have increased water-use
efficiency during the global aridification that peaked 45 to
30 Mya, and thus conferred the grasses with a competitive
advantage.
Others have applied finite element analysis to explore the
relationships between stomatal structure and function to show
that sunken stomata, a cuticular lining, small substomatal
chamber size and reduced stomatal aperture, each have the
potential to greatly decrease stomatal conductance (Roth-Nebelsick, 2007). How variation in the size of the substomatal
chamber relates to stomatal size is empirically unknown, as are
the consequences of this allometry for photosynthesis, but
Roth-Nebelsick’s model suggests that transpiration estimates
based solely on fossil stomatal density and aperture size may
overestimate stomatal conductance.
Along these lines, the gas-exchange response of Rhyniophytic plants has received considerable attention because the
morphological detail of their tissues is well preserved, and
their terrestial habit represents the beginning of the evolution
of modern plant physiology. It appears that Rhyniophytes colonized diverse habitats with variations in temperature
(Edwards et al., 2001) and water availability due to periodic
flooding (Rice et al., 2002; Trewin et al., 2003), thereby providing the context in which the ecophysiology of these taxa
can be examined. The cuticle of Rhyniophytic taxa is characterized by low stomatal densities suggesting that in the CO2rich climate of the Lower Devonian, these plants would have
exhibited high water-use efficiencies (Edwards et al., 1998).
Computer simulations suggest that transpiration and photosynthesis were greatest in Nothia aphylla, a ‘leafy’ Rhyniophyte with relatively high stomatal densities (El-Saadawy &
Lacey, 1979), when compared with the more conservative
Rhynia and Aglaophyton (Konrad et al., 2000; Roth-Nebelsick & Konrad, 2003). The stricter water-use strategies of the
latter two taxa probably reflect the absence of a well-developed root system (Roth-Nebelsick & Konrad, 2003).
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Lastly, increased water use efficiency may have been the
driving force behind selection for presumably ‘optimized’,
i.e. rapid, stomatal responses of angiosperms to short-term
changes in CO2, relative to conifers and ferns (Brodribb
et al., 2009). Considering that water use efficiency positively
affects species’ reproductive output (Farris & Lechowicz,
1990; Dudley, 1996; Ackerly et al., 2000), one could argue
that the evolution of stomata single-handedly provided
ancestral land plants with a competitive advantage, and thus
helped transform the terrestrial landscape into a threedimensional mosaic of vegetation, rather than a dense film of
liverworts.
The transition to plant vascular tissue
With the cuticle and the stomata in place, the evolution of
water-conducting cells completed the basic bauplan needed
for plant homoiohydry (Raven & Edwards, 2004). What are
the transitional steps from undifferentiated mesophyll cells to
a bundle of directionally aligned hollow tubes, and what are
the biotic and abiotic signals responsible for this pattern in the
first place? Understanding vascular tissue ontogeny may
inform our interpretation of fossil material and its relevance to
the evolution of xylem.
Our current outlook on the differentiation of unspecified
plant cells into elongated tracheary elements is shaped by
model systems such as Zinnia, Arabidopsis and Populus
(Tuskan et al., 2006; Turner et al., 2007). In plants with
a meristematic, procambial region, cambial cells are programmed to differentiate into either phloem or vascular tissue.
However, under appropriate culture conditions, mesophyll
cells can also be made to de-differentiate and develop into
tracheary elements (Fig. 2). Auxin, the newly discovered xylogen hormone and other signalling compounds control these
changes and much progress has been made in elucidating the
genetic regulation of cell differentiation (Roberts & McCann,
2000; Chaffey, 2002). What makes this particularly relevant in
an evolutionary context is that the totipotency of plant cells
can be so easily manipulated with the appropriate signalling
compounds, most of which are produced by neighbouring
cells (Nieminen et al., 2004). In other words, the design of
even the most basic of vascular systems belonging to liverworts (Ligrone & Duckett, 1996) and bryophytes (Proctor &
Tuba, 2002) required little more than the appropriate signal
to upregulate a suite of genes that control cell differentiation.
One of the critical steps to the formation of vascular tissue
may have been the establishment of a polar auxin gradient
because auxin stimulates the differentiation, patterning and
elongation of tracheary elements (McCann, 1997; Sieburth &
Deyholos, 2006). An auxin gradient can also arise due to
wounding, and generate a response characterized by cell
rotation in the new tissue formed near the injury (Kramer
et al., 2008). Interestingly, evidence for this rotated cell
arrangement was recently discovered in secondary vascular tis-
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Fig. 2 The differentiation of mesophyll and procambial cells into vascular conduits according to Turner et al. (2007). Different combinations of hormones may act on
the procambial or mesophyll cells to initiate the formation of tracheary elements or conduits. Conduit expansion and elongation is followed by the deposition of the
secondary wall and followed by cell death and digestion of cell endwalls. Lignification completes this developmental sequence.
sue belonging to an Archeopteris (upper Devonian, 375 Mya;
Rothwell & Lev-Yadun, 2005) as well as in wood of tree-sized
fossil equisetophytes and arborescent lycophytes belonging to
different lineages (Rothwell et al., 2008). In these plants, the
independent origins of secondary vascular tissue suggest a role
for the parallel evolution of regulation by auxin in each clade
(Rothwell et al., 2008).
There is evidence that vascular tissue differentiation is a
homologous phenomenon in land plants. Indeed, molecular
data indicate that auxin metabolic pathways are present in
basal plant lineages such as the Charales, liverworts and bryophytes (Cooke et al., 2002). Of further interest are computer
models showing close correspondence between predicted
procambial vascular patterns based on theoretical input auxin
concentrations, and their close correspondence to actual
stelar patterns observed in the Early Devonian Psilophyton
and several members of the pro-gymnosperm group, the
Aneurophytales (Stein, 1993). Altogether, there is growing
evidence for the contribution of auxin to the evolution of vascular plants, and the subsequent diversification of Silurian and
Devonian plant lineages.
Following cell differentiation, the process of expansion is
driven by mechanical forces that are a function of osmotic pressurization, which in mature plant cells can generate pressures
ranging from 0.1 to 3 MPa (Somerville et al., 2004; Taiz &
Zeiger, 2006). Brassinosteroid hormones are thought to play
a role in the complex co-ordination of the simultaneous expansion of multiple cells, although several auxin-mediated
enzymes acidify and loosen the fibrous, cellulose cell wall
matrix (Wang & He, 2004; Turner et al., 2007). Importantly,
a class of proteins known as expansins regulates the loosening
of the cell wall (Cosgrove, 2005; Popper, 2008). Expansins
are not only ubiquitous across the land plant taxa, but also
thought to be integral to the development of xylem and evolution of the plant vascular system (Popper, 2008). The genetic
toolbox required for cell wall expansion is present in algae,
so the only other key innovation in the evolution of plant
vascular tissue would have been the development of the cellulosic secondary cell wall for increased rigidity. In plants, this secondary wall is deposited interior to the primary cell wall
following cell expansion, but excluded from the vessel endwall
and the pitted regions of the conduit that allow water to move
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The evolution of water transport in plants
from one cell to another (Somerville et al., 2004; Choat et al.,
2008).
The rigidification of cell walls with polyphenols probably
occurred synchronously, or nearly so with the evolution of
early plant vascular systems (see next section). Developmentally, the deposition of lignin or its precursors such as lignan
into the cellulose, pectin and protein wall matrix of the secondary wall is the final step towards increasing the stiffness
and compressive resistance of the conducting cell as well as its
impermeamility to water (Niklas, 1992; Lewis, 1999; Koehler
& Telewski, 2006). For example, Arabidopsis and Nicotiana
mutants with disrupted lignin synthesis not only exhibit malformed vasculature, but also show a high frequency of
crimped or collapsed conduits (Turner & Somerville, 1997;
Piquemal et al., 1998; Jones et al., 2001).
The complex genetic and chemical components of lignification have been identified (Boerjan et al., 2003; Peter & Neale,
2004) so a solid grasp of the functional implications of the
process on plant hydraulics is in the near future. Recently, 12
genes were targeted as the probable candidates of vascular lignification in Arabidopsis (Raes et al., 2003) whereas the Black
Cottonwood genome-sequencing project uncovered a high
number of gene families responsible for ligno-cellulosic wall
formation (Tuskan et al., 2006). However, the genetics of
herbaceous model systems such as those of Arabidopsis and
Zinnia are easily manipulated (McCann, 1997; Roberts &
McCann, 2000) so, at this point in time, we know more about
tracheary element formation from these plants than from
woody taxa. Interestingly, evidence from the Zinnia model of
tracheary element formation suggests that lignification follows
cell death, which means that surrounding parenchyma tissue
may be responsible for the synthesis and release of lignin
precursors (Turner et al., 2007). Certainly, once the digestion
of cell contents begins, cell growth has ceased so lignin deposition is the logical, final stage of creating a functioning, but
dead water-filled xylem conduit.
Lignins were generally thought to be absent from the algae,
but the cell walls of the Charophyte Coleochaete were found to
contain lignin-like compounds, adding further support for
their close association with land plants (Delwiche et al.,
1989). True lignin was recently discovered in the flexible,
joint-like tissue, the red algae Calliarthron, prompting the
suggestion that lignin biosynthetic pathways may have had an
early function in biomechanics, in addition to protecting cells
from microbial attack and UV damage (Martone et al., 2009;
see also Niklas, 1992). Both studies indicate that the fundamental pathways of lignin biosynthesis are deeply conserved,
so the lignification of xylem was essentially a function of time
and increased tissue specificity.
On a final note, the biosynthesis of lignin is dependent on
oxygen, leading some workers to speculate that elevated O2
produced by the abundant land plants during the Mid-Devonian to the Early Carboniferous, may have spurred the evolution of xylem lignification (Graham et al., 1995; Berner,
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119
2006; Berner et al., 2007). In the proposed sequence of
events, a rise in O2 levels due to photosynthesis facilitated
lignification, which in turn supported the evolution of
arborescence, further increasing photosynthetic biomass in a
feedforward cycle. Interestingly, some would argue that lignin
is not even a prerequisite for conferring stiffness to the plant
body per se and is merely a secondary requirement for arborescence because non-lignified tissues can impart rigidity to the
plant body (Rowe & Speck, 2004), thereby eliminating the
necessity for the role of oxygen in the first place. However, lignin is essential to preventing cell implosion at the negative
water potentials that can occur at the tops of trees as a result of
gravity (Koch et al., 2004; Domec et al., 2008), so modern
trees would probably have not evolved beyond a height of
5 m without this phenolic (Niklas, 1992). It is unlikely that
selection would favour a combination of weak xylem and nonlignifed support tissue when the economy of modern wood
yields higher dividends courtesy of simultaneous canopy
support and water transport. Whether O2 facilitated this
streamlining of plant form and function cannot be directly
tested, but a quantitative model, although limited, may
provide us with useful insights.
The transport advantages of conducting tissue
With the basic blueprint for the vascular network in place, the
next step in the evolution of xylem was to maximize the transport gains of this low resistance pathway. Indeed, the need to
reliably move water and solutes throughout the plant body
selected for the evolution of vascular tissue in even the most
primitive plants such as liverworts (Ligrone & Duckett, 1996;
VanAller Hernick et al., 2008). Furthermore, the near simultaneous appearance of vascular systems and stomata during
the Mid-Silurian suggests that selection not only favoured the
functional coupling between these traits (Sperry, 2003; Raven
& Edwards, 2004), but also their co-ordinated optimization
to maximize photosynthesis (Brodribb, 2009).
The frictional resistance to water transport is significantly
reduced when water travels through microscopic, hollow
channels rather than the nanoscopic pathways that characterize symplastic water movement. Not surprisingly, water
transport through elongated, hollow single cells is 106 times
more efficient than transport through parenchymal tissue via
plasmodesmatal channels (Raven, 1977). Similarly, ectohydric
water transport, which describes the wicking of water through
external capillary structures, is common in both terrestrial
Charophycean algae and bryophytes (Proctor & Tuba, 2002;
Franks & Brodribb, 2005) but is insufficient for taller plants.
Both pathways present such high degrees of resistance that
plants exclusively relying on non-vascular water transport
rarely exceed heights of a few centimetres and are typically
poikilohydric (Niklas, 1992; Proctor & Tuba, 2002).
The hydraulic advantage of wide, hollow conduits over narrow channels is evident in the context of the Hagen–Poiseuille
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J. PITTER MANN
equation, which predicts water-transport efficiency through
smooth-walled capillaries. Here, the flow rate of water, Q,
with a viscosity g, passing through a capillary with a diameter
of D is proportional to the pressure gradient dP ⁄ dx driving
the flow such that,
pD 4 dP
Q ¼
:
ð1Þ
128g dx
Equation 1 demonstrates that hydraulic efficiency is proportional to the conduit diameter raised to the fourth power, so a
modest increase in conduit diameter leads to significant gains
in transport (Tyree et al., 1994; Tyree & Zimmermann,
2002). Single conduit measurements of hydraulic efficiency
agree with the predictions of the Hagen–Poiseuille equation
(Zwieniecki et al., 2001). Functionally, this means that all else
being equal, 16 conduits with a 20-lm diameter are required
to achieve the hydraulic efficiency of one 40-lm vessel
(Fig. 3).
The higher area-specific conductivity of larger conduits
confers several advantages, an important one being that a
plant can invest less carbon in transport tissue, particularly as
the conduits are dead. Secondly, the lower transport resistance
associated with large conduits reduces the pressure drop that
is required to move water from the roots to the leaves. Very
negative water potentials can predispose the xylem to dysfunction (see Part III) and stress the leaf tissue, both of which can
lead to reductions in gas exchange. Lastly, high transport
efficiencies characteristic of xylem with large conduits can support increased transpiration rates, which in turn allow higher
rates of photosynthesis (Brodribb & Feild, 2000; Brodribb
et al., 2002; Santiago et al., 2004). Predictably, plants have
exploited the relationship between diameter and efficiency
such that there has been a 60-fold increase in conduit diameter since the evolution of the early 5- to 8-lm wide Cooksonian
tracheids from the upper Silurian (416 Mya; Niklas, 1992;
A
B
Fig. 4) to the nearly 500-lm wide vessels of extant tropical
vines and lianas (Ewers, 1985).
PART II: VASCULAR PLANTS IN THE FOSSIL
RECORD
Conducting tissue in protracheophytes and early vascular
plants
The Late Silurian to the Early Devonian represent a period of
remarkable terrestrial plant speciation as well as exploration of
different forms of vascular structure. Geochemically based
models suggest that elevated atmospheric CO2 coupled with
2–4 C warmer sea surface temperatures characterized the
climate during this initial phase of plant diversification (Berner,
2006; Came et al., 2007). Some of the extinct taxa from this
period may well be the ancestors of certain bryophytic lineages
or true vascular land plants, while others were early experiments in the homoihydric lifestyle. The most well-studied
(though neither the oldest nor most ancestral) plants of this
period are from the Early Devonian Rhynie Chert (398–
396 Mya). This group has traditionally occupied the position
of the simplest vascular plants but this perspective has changed
as it became clear that Rhyniophytes share features of both
bryophytes and vascular plants (Kenrick & Crane, 1997;
Taylor et al., 2009). Kenrick & Crane (1997) provide the most
widely accepted cladistic treatment of the evolution of early
land plants, using among other character traits, the anatomy of
vascular tissue to decide placement on the phylogeny. What
emerges is a trend towards xylem comprised of progressively
larger tracheids with an increasingly complex and mechanically
robust wall anatomy (Kenrick & Crane, 1991, 1997; Edwards,
2003; Taylor et al., 2009) presumably reflecting selection for
efficient vascular transport and conduit support under negative
xylem pressures. The evolution of angiosperm vessels and
Fig. 3 All else being equal, 16 conduits (vessels)
with a 20-lm diameter (A: Populus sp., diffuseporous wood) are required to achieve the hydraulic
efficiency of one 40-lm diameter conduits (B:
Quercus sp., ring-porous wood). Note that the
vessels are embedded in a matrix of fibres.
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The evolution of water transport in plants
121
Fig. 4 Tracheid diameters increased almost 18-fold from 8 lm during the Upper Silurian, to a maximum of 140 lm in the Upper Devonian (Niklas, 1985; courtesy of
Blackwell Publishing) representing substantial gains in hydraulic efficiency.
fibres for water transport and support respectively represents
the pinnacle of vascular specialization in woody plants. Informative photographs and detailed commentary of the taxa
described in this section can be found in Taylor et al. (2009),
Edwards (2003), Kenrick & Crane (1991), Stewart & Rothwell (1993) and Kenrick & Crane (1997).
Liverworts occupy the basal position in the land plant phylogeny so the nearest analogue to the most primitive form of
vascular tissue probably resides in the gametophyte of the
extant, stomatalless liverwort Symphyogyna brasiliensis and its
relatives in the Pallaviciniineae. Non-lignified, elongate waterconducting cells with thickened secondary walls are packed
together in the central regions of Symphyogyna’s thallus in
what may ostensibly be the most primitive vascular bundle.
Water travels from one cell to another via plasmodesmatal
pores and perforated, primary wall regions along the length of
the cell (Ligrone & Duckett, 1996; Ligrone et al., 2000).
Close examination of the recently discovered fossil liverwort
Metzgeriothallus sharonae (Mid-Devonian, 390 Mya) could
2010 Blackwell Publishing Ltd
confirm that vascular tissue may have been present in this
extinct species, although the authors do not discuss this possibility (VanAller Hernick et al., 2008; Fig. 5). It is not unlikely
however, that M. sharonae may represent one of the earliest
experiments in the design of transport tissue as both the
extant Symphyogyna and this fossil liverwort are ascribed to the
order Metzgeriales.
The oldest macrofossil vascular land plants are the cooksonioids of the Mid-Silurian (Wenlockian, 428–422 Mya) represented by Cooksonia (Edwards & Feehan, 1980), and similar
fossils such as Tortilicaulis (Edwards, 1996; Bateman et al.,
1998; Boyce, 2008). Early land plants from the Silurian and
Early Devonian form a diverse group with nebulous evolutionary affinities, but currently accepted hypotheses suggest
that, despite its antiquity in the fossil record, Cooksonia is
derived from the protracheophytes, and belongs between the
rhyniopsids and the lycophytes (Kenrick & Crane, 1997).
Efforts to confidently place Cooksonia on the land plant phylogeny are also hampered by limited and partially preserved
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A
J. PITTER MANN
B
fossil material which may or may not actually by Cooksonia in
the strict sense (Boyce, 2008).
Cooksonioids were probably only a few centimetres tall,
with erect, bifurcating axial stems that ranged in diameter
from <100 lm to 1.5 mm (Boyce, 2008). Lacking roots
and leaves, the shoots of these simple plants terminated in
sporangia. Although Cooksonia is accepted as the first
vascular plant (Taylor et al., 2009), the actual contribution
of the limited vascular tissue to water transport is questionable because the conduits are so narrow (<5 lm; Boyce,
2008). Close examination has shown that the conduits of
Cooksonia pertonii exhibit thick annual and spiral wall rings,
when compared with the thinner primary wall thickenings
found in modern protoxylem (Edwards, 2003). These rings
rigidify an otherwise highly perforated and what appears to
be a mechanically weak conduit wall. Despite their small
size, Cooksonia’s conduits may have adequately delivered
water to axial tissues in order to maintain the necessary
turgor pressure for an erect stature (Bateman et al.,
1998). Cooksonia possessed stomata, but they were low in
frequency and occurred primarily in the vicinity of the
sporangia, prompting the suggestion that their role was to
facilitate nutrient transport via transpiration-driven water
flow rather than increase CO2 diffusion for photosynthesis
(Edwards et al., 1996, 1998; Boyce, 2008).
The younger, more derived flora of the famous Rhynie
Chert has provided an abundance of specimens that reveal the
diversity of conducting tissues in early land plants (Taylor
et al., 2009). The cherts, which were formed in a hot-spring
environment, preserve a terrestrial and freshwater floodplain
habitat containing numerous species of early land plants (Rice
et al., 2002; Trewin et al., 2003). Of these, one the best
understood is Aglaophyton major, an 18-cm tall plant consisting of bifurcating, stomatiferous, cylindrical axes that lie
loosely on the substrate surface and function as rhizomes
(Taylor et al., 2009). Aglaophyton lacked a root system and
leaves, but possessed a central bundle of vascular tissue (proto-
Fig. 5 Fossils of the liverwort, Metzgeriothallus
sharonae from the Middle Devonian of eastern
New York, USA (VanAller Hernick et al., 2008;
courtesy of Elsevier Press). A single vein is evident in
each lobe of the gametophyte thallus (A: 10· magnification). The elongate cells present in the vein
closely resemble vascular tissue (B: 120· magnification).
stele), parenchyma with intercellular air spaces, a cuticle and
stomata (Edwards et al., 1998; Taylor et al., 2009). Aglaophyton’s conducting tissue is composed of smooth, thin and
thick-walled cells of variable diameter (18–50 lm; Edwards,
2003) and is understood to be much more primitive than that
of Cooksonia. Indeed, this is one of several reasons why Aglaophyton is placed with the protracheophytes, a group more closely allied with the mosses rather than true vascular plants
(Edwards, 1986; Kenrick & Crane, 1997; Edwards, 2003).
Similarly, Horneophyton lignieri, an abundant and well-documented 20-cm tall species from the Rhynie Chert, has also
been grouped with the protracheophytes (Kenrick & Crane,
1997; Wellman et al., 2004).
The tracheids of more advanced rhynioids such as Sennicaulis, Stockmanesella, Huvenia, Sciadophyton and Rhynia
gwynne-vaughanii are typically <25 lm in diameter, and
reveal increasing complexity and ornamentation in the form
of helical thickenings and spongy tissue layers (Kenrick &
Crane, 1991; Edwards, 2003; Taylor et al., 2009). These
plants represent the first tracheophytes (Kenrick & Crane,
1997). The so-called G- and P-type tracheids found in eutracheophytes and euphyllophytes respectively, range from 30 to
80 lm in diameter and may exhibit scalariform (ladder-like)
pitting and a decay-resistant inner layer that covers the pit
apertures (Kenrick & Crane, 1991, 1997; Edwards, 2003). At
first glance, the P-tracheid xylem of the euphyllophyte
Psilophyton resembles that of ferns, thereby representing the
most modern conduit anatomy of Lower Devonian taxa.
Taken together, the general impression from the fossil
record is that vascular tissue in the earliest land plants became
progressively more efficient due to selection for larger lumen
diameters. Simultaneously, tracheids became increasingly
more robust as evidenced by the helical and annular thickenings in S- and G-type tracheids, relative to the smooth, thinwalled conduits of Aglaophyton. Such fortified conduits would
have withstood the negative xylem pressures associated with
water stress, rather than collapsed. Implosion-resistant, and
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The evolution of water transport in plants
perhaps to some extent lignified vasculature may have allowed
Early Devonian taxa to exploit periodically drier environments. Concurrently, increased perforation of the conduit
walls allowed water to move from one conduit to another,
which not only increased transport efficiency, but also maintained transport continuity should one or several conduits
become dysfunctional.
True tracheids are a key synapomorphy of the tracheophytic
land plants, but the first appearance of lignin in the vascular
plant fossil record is equivocal (Friedman & Cook, 2000; Boyce et al., 2002). However, the recent use of novel micro-analytical techniques to analyse fossil material has lead to
breakthroughs in our understanding of lignification and thus
the structure and function of tracheophytes from both fossil
and extant lineages. Specifically, soft X-ray carbon spectromicroscopy combined with isotope ratio mass spectrometry has
proved useful in analysing the wall chemistry of conducting
tissues belonging to fossil plant material (Boyce et al., 2002,
2003). Because lignin has a carbon isotopic signal that is 4&–
8& lighter than cellulose within the same plant, it is possible
to test for tissue lignification by comparing the 13C signal of
taphonomically equivalent fossils that possess lignified tissue
with those whose tissue chemistry is unknown. Concurrent Xray spectroscopy can identify the presence of aromatic carbon
compounds that are characteristic of lignin.
These microanalytical techniques allowed Boyce et al.
(2003) to demonstrate that the vascular strand of Aglaophyton
major lacked lignified water-conducting cells unlike the ring
of lignified fibrous cells just beneath the epidermis. These
fibres probably served a mechanical function that rigidified
Aglaophyton’s narrow, cortex-filled stems (Bateman et al.,
1998; Boyce et al., 2003). By contrast, more derived taxa such
as Rhynia gwynne-vaughnii exhibited lightly lignified xylem,
with significant lignification evident in the tracheids of Asteroxylon mackiei (see also Kenrick & Crane, 1991). The greater
xylem fraction, and perhaps to some degree, the greater stiffness afforded to taxa with progressively more lignified tissue is
consistent with Rhynia’s and Asteroxylon’s tendency towards
increased height and horizontal branching (Boyce et al.,
2003). New methods, such as X-ray carbon spectromicroscopy, are exciting and may offer greater insight into the hydraulic
and mechanical properties of the first vascular plants, particularly those with equivocal phylogenetic affinities.
Vascular tissue in advanced land plants
For nearly 300 million years, tracheid-based xylem remained
the most prevalent transport tissue in the plant kingdom.
The ornate tracheids of the Early Devonian tracheophytes
eventually led to the hydraulically efficient, large-diameter,
scalariform tracheids of more derived groups such as the
horsetails and ferns, and eventually to the thick-walled
tracheids that provided a biomechanical and a transport function in progymnosperms, gingkos and conifers (Tyree &
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123
Zimmermann, 2002; Pittermann et al., 2006a). According
to the classic scenario of Bailey & Tupper (1918) the subsequent evolution of tracheids into the fibres and vessel
elements of angiosperm xylem capitalized on the functional
specialization of each cell type. Fibres are short and thickwalled, providing the necessary strength for increasingly
lateral canopies while the large vessel elements reduce
resistance to water transport.
Not surprisingly, competition for light and the need for
effective spore dispersal prompted the evolution of arborescence (Niklas, 1985, 1992; Mosbrugger, 1990), well before
the appearance of secondary xylem, that is wood. In fact, the
evolution of secondary xylem is not even a requirement for
elevated canopies assuming that other tissues such as a
hypodermal sterome, thick external periderm or cortex tissue
provide structural support (Niklas, 1997; Rowe & Speck,
2004, 2005). This means that during the Devonian, the tree
habit was free to arise independently and more or less
simultaneously in ferns, lepidophytes, horsetails and progymnosperms (Mosbrugger, 1990).
Modern and extinct tree ferns lack secondary xylem so
structural support comes from abundant schlerenchymatous
(i.e. lignifed) fibres, support roots, numerous thin axes and
other plant matter that makes up the false trunk (Mosbrugger,
1990; Taylor et al., 2009). The Mid-Cretaceous fern, Tempskya is a good example of this strategy as its main axis looks disproportionately large relative to the size of the emerging
fronds due to the accumulation of roots, fibres and plant debris (Taylor et al., 2009). Modern ferns, such as those in the
genera Dicksonia and Cyathea rarely exceed heights of 10 m,
but the reasons for this height limit have not been examined.
Buckling is unlikely to occur given the compressive strength
of fern trunks (Mosbrugger, 1990; Niklas, 1997). Although
hydraulic limits in ferns may arise from limited conduit size
and conduit density (Gibson et al., 1984) it may be that there
is little to gain by growing tall in a light-limited environment
already dominated by tall angiosperms with expansive canopies.
The evolution of the vascular cambium (the axial meristem
that gives rise to secondary xylem) relaxed the restrictions on
axial height and girth imposed by primary xylem. Fossil
evidence suggests that the vascular cambium originated early
in the evolution of land plants and may have evolved in
response to strong selective pressure for increased plant size.
The primitive progymnosperm group Aneurophytales were
the first to show limited secondary xylem by the Mid-Devonian, but by the Late Devonian, secondary xylem was present
in representatives of nearly all major plant groups including
Lepidodendrales, horsetails, seed ferns, progymnosperms and
perhaps even in the Cladoxylopsids (fern affiliates), although
the vascular patterns of these fern allies are highly variable even
within a specimen (Niklas, 1997; Taylor et al., 2009).
Of the three types of vascular cambia that evolved in plants,
the bifacial and monocot ‘etagen’ cambia are present in mod-
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J. PITTER MANN
ern taxa, while the unifacial vascular cambium disappeared
after the Late Devonian (Esau, 1943; Niklas, 1997). The
unifacial vascular cambium was present in Sphenophyllum
(relatives of horsetails), and Sigillaria and Lepidodendron,
both representatives of Carboniferous arborescent Lycopods
(Thomas & Watson, 1976; Taylor et al., 2009). Lepidodondron was a dominant element of the swampy Carboniferous
landscape, whereas Sigillaria may have occupied drier sites
(Phillips & DiMichele, 1992; Stewart & Rothwell, 1993;
Taylor et al., 2009). Because the unifacial cambium was
capable of only producing new xylem cells to the interior of
the main axis (periclinal division), and unable to divide radially
to generate new cambial initial cells (anticlinal division), the
girth of these plants was thought to be determinate and
established early in their development by a large number of
fusiform initials (Eggert, 1961; Cichan, 1985a,b). Consequently, lateral expansion of the secondary xylem as well as the
stem axis in Sphenophyllum and the tree like Lycopods could
only be achieved by the progressive, centrifugal enlargement
of the cambial initials rather than an increase in the number
cambial cells (Cichan, 1985a,b).
Despite the limited cambial expansion of these early trees,
they often reached heights of 40 m and their basal diameters
exceeded 2 m. Reconstructions suggest that Sigillaria and
Lepidodendron were characterized by vertical, monopodial
axes that lacked side-branches but terminated in a large, profusely branched crown of leafy twigs (Phillips & DiMichele,
1992; Taylor et al., 2009). With greater height, girth and leaf
area presumably became a higher demand for water. The
increased length and diameter of the lateral tracheids (25 mm
long, 120 lm diameter) relative to the central tracheids
(14 mm long, 85 lm diameter) of the main axis (Cichan,
1985a,b) may have adequately supplied this demand, albeit in
a limited capacity. Simple predictions using the Hagen–
Poiseuille equation suggest that hydraulic transport in the
periphery of a Lepidodendron stem may have been over fourfold higher (on a cell basis) than in the interior of the axis.
However, the trunks of arborescent lycopods contained a
high fraction of cortex tissue (Mosbrugger, 1990), so a determinate meristem producing only a limited amount of xylem
may have been the transport bottleneck failing to deliver
enough water to both maintain turgor and support gas
exchange during drought. This is consistent with the idea
that arborescent lycopods disappeared in response to a drier
climate in the Late Carboniferous (Phillips & DiMichele,
1992). Concurrently, the apparent developmental inflexibility
of the unifacial cambium may have limited structural diversity
and branching, which also would have placed these early trees
at a competitive disadvantage for resources and perhaps contributed to their demise (Rowe & Speck, 2005). Alas, this
‘nascent innovation’ was successful for only 50 million years.
By constrast, the bifacial vascular cambium first characterized by the Mid-Devonian progymnosperms Archaeopteris
(Beck, 1960, 1970; Meyer-Berthaud et al., 1999) is found in
all modern trees. As its name implies, the bifacial cambium
produces secondary xylem towards the inside of the stem axis,
and phloem to the outside. Its primary advantage lies in the
capacity of the cambial initials to divide both anticlinally and
periclinally such that each year, new cells are added in a manner that allows for the indeterminate expansion of the stem
axis as well as the addition of branches. Of the two cambial
strategies discussed thus far, selection has favoured the bifacial
vascular cambium because it successfully combines water
transport with mechanical support of the canopy (Rowe &
Speck, 2004, 2005).
The monocot ‘etagen’ cambium is recently derived in the
angiosperm monocots (Lower Cretaceous; Herendeen &
Crane, 1995) and produces lignified fibres in well-ordered,
discrete vascular bundles containing both xylem and phloem
(Esau, 1943; Rudall, 1995; Tomlinson, 2006). There is no
secondary xylem in monocots. Arborescent monocots such as
palms are unusual in the plant world because most of the stem
volume is occupied by primary vascular tissue that is thought
to remain fully functional over the life of the plant (Tyree &
Zimmermann, 2002; Tomlinson, 2006).
On the whole, the evolutionary trajectory of plant vascular
systems has selected for some combination of increasing
hydraulic efficiency and biomechanical support. The evaluation of Murray’s law in the context of different wood types
now serves as a classic example of the support structure versus
hydraulic efficiency trade-off. Murray’s law was originally
developed for cardiovascular design, and states that for a fixed
investment in blood and vessel volume, the optimal transport
arrangement equalizes the sum of conduit radii cubed along
the flow path. Interestingly, this axiom also applies to vascular
plants but only if the support requirement is entirely separate
from the transport function, as in the xylem of leaves, ringporous species (see Fig. 3), vines and some ferns (McCulloh
et al., 2003; McCulloh & Sperry, 2005). Significant deviation
from Murray’s law occurs when vascular tissue increasingly
performs a structural function, as in the case of conifers
(McCulloh et al., 2004). Murray’s law has not been evaluated
in extinct taxa such as the Sphenophyllum or Lepidodenron, but
it is unlikely that the unifacial cambium compromised the
water transport in tissue that was largely decoupled from canopy support. In other words, transport efficiency is likely to
have selected for adherence to Murray’s law even in morphologically complex, although extinct taxa, but this hypothesis
remains to be tested.
Because the structural and hydraulic performance of fossil
taxa is impossible to examine directly, the remaining option is
to uncover the biophysical priciples that underlie modern
plant structure and function, and to apply them to ancient
taxa, or towards models of new morphologies. Indeed, the
theoretical approach has yielded a vast array of spectacularly
diverse, yet realistic plant ‘morphospace’ that accurately
describes both modern and fossil flora (Niklas, 1997, 2004).
Because the plant vascular system reflects the overall construc-
2010 Blackwell Publishing Ltd
The evolution of water transport in plants
tion of a broad array of plant life forms including herbaceous,
woody, lianecescent and mococot plants, we can utilize the
structure–function relationships of modern xylem to generate
reasonable hypotheses about the physiology and habitat of
ancient plants.
PART III: THE FUNCTIONAL ANATOMY OF
MODERN PLANT VASCULAR TISSUE – THE
HYDRAULIC TRADE-OFFS OF RESISTANCE TO
ABIOTIC STRESS
A good grasp of anatomy is useful to correctly interpret the
relationships between xylem structure and function. This is
because the transport characteristics of the xylem impose
physical constraints on the rate at which water can be supplied
to the leaves, and on the maximum transpiration rates allowed
by stomata (Tyree & Sperry, 1989; Sperry et al., 1998;
Brodribb, 2009). The following discussion will focus on
conifers and woody angiosperms simply because most vascular
structure function work has been performed on woody
species. However, there is no apparent reason why the
principles derived from this research should not apply equally
well to non-woody plants.
The structure of conifer and angiosperm xylem
Conifer wood is homogenous, meaning that it is composed
entirely of overlapping individual cells referred to as tracheids.
Modern conifer tracheids range in size from about 0.5 to
nearly 4 mm in length and 8–80 lm in diameter (Panshin &
de Zeeuw, 1980; Pittermann & Sperry, 2003; Pittermann
et al., 2006a) and their size depends on, among other factors,
their location within the tree and whether or not they function
in supporting the canopy. In general, root tracheids tend to
be longer and wider with thinner conduit walls rather than
stem tracheids (Pittermann et al., 2006b). This is because
root tissue is optimized for the delivery of water to the canopy
whereas stem tissue must compromise between water transport and structural support (Sperry et al., 2006; Pittermann
et al., 2006a,b).
Angiosperm xylem is slightly more complex than that of
conifers and exhibits a greater capacity for variation. Water
transport occurs through multicellular conduits known as vessels. Vessels are composed of two or more single-celled vessel
elements that are stacked one on top of the other to form an
elongated tube that may be up to 0.5 mm in diameter and
2 m in length. Unlike in the tracheids, the distal regions of the
individual vessel elements (known as endwalls) are digested
away either entirely, or in a scalariform pattern with the
end-result resembling an elongated pipe that offers a low resistance pathway for water movement from the root to the canopy (Ewers, 1985; Schulte & Castle, 1993; Ellerby & Ennos,
1998). The vessels are embedded in a matrix of short, thickwalled fibres (Fig. 3). Consequently, angiosperm xylem is
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thought to reflect a more optimized vascular strategy that capitalizes on the division of labour to efficiently deliver water
through the vessels and while relegating storage and mechanical requirements to the fibres.
In conifers as well as in angiosperms, water moves from one
conduit to another via perforations in the cell wall, also known
as bordered pits (Fig. 6; Choat et al., 2008). These pits are
composed of a water-permeable, cellulosic pit membrane that
is surrounded on either side by the overarching secondary cell
wall, the pit border. The perforated cell wall provides an aperture through which water can pass from one conduit to
another through the pit membrane.
Significant progress has been made in our understanding of
the evolution of xylem structure and function, and the tradeoffs that accompany pit structure, conduit length and conduit
diameter in conifers and angiosperms (Tyree et al., 1994;
Comstock & Sperry, 2000; Sperry et al., 2006). Specifically,
we now have a quantitative grasp of the functional consequences of wood bearing either vessels or tracheids, and are in
better position to consider the vascular performance of fossil
plants.
It is intuitive that conduit lumen diameter and conduit
length highly impact conducting efficiency and that as such,
selection has favoured the evolution of larger conduits
(Fig. 4). Indeed, this perspective has been emphasized in the
literature effectively arguing that angiosperm wood, with its
longer and wider vessels, is inherently more hydraulically
efficient that the homoxylous, tracheid-based wood of conifers (Tyree & Zimmermann, 2002). Broadly speaking, the
hydraulic properties of both plant forms are thought to have
significant implications for their resource competition, fitness
and ecological dominance (Bond, 1989). However, this
perspective has recently shifted because on closer inspection,
the transport issue is not just one of conduit volume but of
overall conduit structure: aside from length, the biggest difference between vessels and tracheids resides in the endwalls of
these conduits where the interconduit pits are located.
Conifers possess intertracheid pits that are composed of
two distinct regions: the outer margo region is rather porous
with micron-scale openings and thus offers minimal resistance
to water flow whereas the inner, thickened torus region is
impermeable. By contrast, the intervessel pit membranes of
angiosperms are composed of a homogenous, tightly woven
mesh of microfibrils. Pore sizes range from 5 to 420 nm and
the membrane lacks a central thickening (Choat et al., 2008).
The functional ramifications of this differing pit structure on
water transport are profound because the pit resistance to
water flow is almost 60· lower in conifer pit membranes
(6 ± 1 MPa s m)1) than in those of angiosperms
(336 ±81 MPa s m)1). This reduction in pit resistance is
equivalent to an almost eightfold increase in tracheid length,
and thus hydraulically compensates for the otherwise
increased resistance that would be associated with greater
number of endwall crossings due to short tracheids. By
126
J. PITTER MANN
Fig. 6 A diagram describing the events of freeze–
thaw and air-seeding cavitation in conifers (see
text). Shaded tracheids are water filled and under
negative xylem pressure (PX), clear tracheids are air
filled and at atmospheric pressure (P0). In functional
tracheids, the thickened torus region of the pit
membrane is centrally located within the pit chamber. When a neighbouring tracheid is air-filled, the
pit membrane deflects against the pit border and
the torus is pressed against the pit aperture, thereby
isolating the dysfunctional tracheid. Air seeding
occurs when the torus becomes dislodged from its
sealing position. In angiosperms, air seeding occurs
through the largest pore in the deflected, homogenous pit membrane (see Choat et al., 2008 for
details).
contrast, the greater length of the angiosperm vessel counteracts the increased hydraulic resistance offered by the homogenous pit membrane. The end result is that conifer and
angiosperm xylem exhibits similar hydraulic efficiency at an
equivalent conduit diameter (Pittermann et al., 2005; Sperry
et al., 2006).
The ancestral condition of tracheid-based wood relies on
homogenous pit membranes rather than the more efficient
torus–margo arrangement for the interconduit flow of water.
This suggests that these ancestral tracheids may have been up
to 38-fold less efficient than tracheids of equivalent size that
bear the more derived torus–margo membrane arrangement
(Sperry et al., 2006). Furthermore, it has been shown that
across a broad sampling of conifers and angiosperms, the endwall contribution to conduit resistance is 64 ± 4% and
56 ± 2% in conifer tracheids and eudicot vessels respectively
(Wheeler et al., 2005; Pittermann et al., 2006b). Since
cycads, ferns and the basal vesselless angiosperms possess
tracheids without a torus–margo pit membrane, how does pit
resistance scale with lumen resistance in these more primitive
taxa? So far, this has only been examined across a broad
sampling of vesselless angiosperms. Interestingly, vesselless
angiosperms exhibit pit resistances that are much closer to
those of conifers than angiosperms (16 ± 2 MPa s m)1)
despite having a homogenous membrane (Hacke et al.,
2007). On average, pit resistance accounted for 77 ± 2% of
the total vessel hydraulic resistance. Scanning electron
microscopy revealed that these pit membranes are much more
porous than those of eudicots, thereby presenting a relatively
lower resistance to water transport. Consequently, the
vesselless angiosperms show hydraulic conductivities that are
much higher than predicted, and surprisingly similar to the
xylem conductivities of conifers (Hacke et al., 2007).
How can we employ these structure–function relationships
in the context of plant palaeo-physiology? Xylem is preserved
extremely well in the fossil record so it is possible with good
sampling and sectioning techniques to re-construct hydraulic
transport in extinct taxa, or at the very least get a sense of it.
However, it is important to acknowledge the implicit assumption here, which is that xylem structure–function relationships
have been conserved over time. This is doubtful because many
extinct taxa combine suites of vascular traits that have no living
analogue. Archaeopteris, the Devonian pro-gymnosperm is
just such a case because its xylem employs tracheids with an
unusual clustered arrangement of intertracheid pits that lack a
torus–margo membrane (Beck, 1970; Meyer-Berthaud et al.,
1999; Taylor et al., 2009). Although it is currently impossible
to directly measure hydraulic efficiency in fossil xylem, it is
possible to construct and test a scaled, physical model much in
the way that Lancashire & Ennos (2002) used glycerine and
toy truck tyres to evaluate the resistance of interconduit pits.
Perhaps the most simplistic way of retrodicting watertransport efficiency is to use the Hagen–Poiseuille relationship to calculate the lumen conductivity (ks) on a xylem area
(A) basis,
P
p D4
;
ð2Þ
ks ¼
A128g
where A is the area represented by the sum of D4 or the total
xylem area. It is important to keep in mind that scalariform
2010 Blackwell Publishing Ltd
The evolution of water transport in plants
perforation plates in vessels, as well as interconduit pits reduce
the actual conductivity by well over 40% of what the Hagen–
Poiseuille relationship predicts (see discussion above, Sperry
et al., 2006; Schulte & Castle, 1993). Similarly, the helical
and annular thickenings found in the protoxylem of extant
plants, and the tracheids of Cooksonia and Sennicaulis can
reduce the effective diameter of the conduits, and thus reduce
ks (Jeje & Zimmermann, 1979).
The Hagen–Poiseuille method may be most readily applicable in a broadly comparative study of well-classified plants that
fall clearly into either the woody coniferous or woody angiosperm category, where we can assume that pit membranes are
likely to constitute a fraction of hydraulic resistance that is
comparable to their living relatives. However, equation 2 can
also be applied to taxa where pit membranes have not broadly
been examined such as in the cycads and ferns, but with much
less certainty. For example, Calkin et al. (1986) determined
that digestion of pit membranes with cellulase increased
hydraulic conductivity by 66% in Pteris vittata. Modelling fern
xylem may be challenging particularly in taxa that harbour vessels in addition to the more commonly observed tracheids
(Carlquist & Schneider, 2007).
However, another interesting exercise is to model fluid flow
in extinct taxa with xylem anatomy that is no longer found in
modern plants. Cichan (1986) was one of the first to recognize the value of this approach, and thus applied the Hagen–
Poiseuille relationship to tracheids in the secondary xylem of
Carboniferous pteridophytic and progymnosperm taxa in
order to estimate the comparative hydraulic performance of
these extinct plants. In his survey, tracheid diameters ranged
from a minimum of 36 lm in the Sphenophyte (i.e. horsetail)
Arthropitys communis to a maximum of 174 lm in the seed
fern Medullosa noei. The tracheid size of Medullosan wood is
exceptional by today’s standards because the largest conduits
in extant plants are found in the lianas, with vessels (not tracheids) commonly in excess of 150 lm (Ewers, 1985; Cichan,
1986). As expected, predicted ks was the highest in plants
with the largest tracheid diameters such as M. noei and Sphenophyllum plurifoliatum, reaching or exceeding the ks of extant
vines and lianas (Cichan, 1986). Clearly, these extinct plants
exploited a morphospace that was quite different from today’s
forms.
However, given what we know about pit resistance in
woody plants, we can build upon Cichan’s method to achieve
a higher level of precision in our transport models. In practice,
hydraulic conductance (K) quantifies the efficiency of water
transport through xylem, and is measured as the flow rate of
liquid water (Q) for a given pressure gradient (DW) driving
flow:
Q
K¼
:
ð3Þ
DW
However, K cannot be measured directly on fossil material,
so an alternative approach for estimating K is to separate
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127
hydraulic resistance (RCA, that is 1 ⁄ K) into its constituent
resistances, those being the conduit lumen resistance (RL)
and the endwall resistance (RW) not unlike resistors in series
(eqn 4; for model details, see Lancashire & Ennos, 2002;
Sperry & Hacke, 2004; Pittermann et al., 2006a,b; Wilson
et al., 2008).
RW ¼ RL þ RW ;
The endwall resistance can be broken down into
RW ¼
2Rpit
;
Npits
ð4Þ
ð5Þ
where Npits represents the number of pits per endwall. Pit
resistance, Rpit is described by the addition of the pit aperture
and pit membrane resistances, both of which can be separated
into their constituents including the porosity of the pit
membrane, the size of the pit membrane pores, the thickness
of the membrane microfibrils, and the depth and width of the
pit aperture (described in detail in Sperry & Hacke, 2004;
Wilson et al., 2008).
Lastly, the inverse of the Hagen–Poiseuille equation estimates flow across half of a tube’s length,
64gL
;
ð6Þ
pD 4
where L represents tracheid length.
Wilson et al. (2008) applied a more complete version of
the above model to investigate the hydraulic resistance of
Medullosa, Cordaites and a Pinus species. This choice of living
and extinct plants allowed the authors to compare the structure and function of tracheids with and without torus–margo
pitting. Interestingly, Medullosa and Cordaites have tracheids
that have angiosperm-like, homogenous pit membranes,
presumably a suboptimal combination of conduit size and
pitting that is expected to produce a substantial drop in
hydraulic efficiency (on a sapwood area basis) relative to
equivalently sized tracheids with torus–margo pitting
(Pittermann et al., 2005). However, the conduit-specific
conductivity of Medullosa was calculated to be over two
magnitudes higher than that of extant conifers, a reflection of
the unusually wide and long tracheids that constitute this
species’ xylem (Wilson et al., 2008). The authors suggest
that the vasculature and hydraulic performance of these fossil
plants is similar to angiosperm lianas, whose climbing habit
eliminates any need for the xylem to perform canopy support
function. This is consistent with the climbing hooks and
tendrils present on the branches and pinnae of Medullosa
specimens (Krings et al., 2003).
Because water transport sets the upper limit for transpiration, the relatively high hydraulic efficiency of Medullosan
xylem is in line with its large leaves and high leaf stomatal densities (Wilson et al., 2008). This plant probably required large
amounts of water to support photosynthesis, which may have
narrowed its habitat to humid tropical floodplains (DiMichele
et al., 2006).
RL ¼
128
J. PITTER MANN
The approach to partitioning resistances in fossil angiosperm xylem can be accomplished in manner similar to that of
Wilson et al. (2008) but it could prove to be more challenging
because vessels may be longer than tracheids by several orders
of magnitude and the vessel network may be tortuous, with
complex pitting patterns (Tyree & Zimmermann, 2002; Kitin
et al., 2004). We can however turn to the structure–function
relationships derived from extant angiosperms to find simple,
anatomically based correlates of hydraulic efficiency. Again,
vessel diameter may prove to be the most useful metric
because it scales well with length and the pitted endwall area,
and thus correlates strongly with xylem transport capacity
(Wheeler et al., 2005; Sperry et al., 2006).
Lastly, the RCA of conifer tracheids with torus–margo
pitting can be inferred from the following summary equation,
128g rP D
RCA ¼
ð1 þ C Þ2 ;
þ
ð7Þ
pD 2
FP L 2
where RL and RW are described by [128g ⁄ (pD2)] and
[rPD ⁄ (FPL2)] respectively (Pittermann et al., 2006b). Essentially, mean RCA is determined by conduit lumen diameter
(D), the length of the conduit (L), intertracheid pit resistance
on an area basis (rP), the fraction of the tracheid wall area
occupied by pits (FP) and the ratio of the tracheid double wall
thickness to lumen diameter (C) (Pittermann et al., 2006b;
Sperry et al., 2006). The average intertracheid rP is
6 ± 1 MPa s m)1 but some degree of variation exists in the
north temperate conifer clades that may reflect tracheid location within the plant as well as species’ drought resistance and
habitat preference (Mayr et al., 2002; Burgess et al., 2006;
Pittermann et al., 2006b; Domec et al., 2008).
Relationships between xylem anatomy, and drought and
freeze–thaw induced cavitation
Not only can wood anatomy be used to describe species’
hydraulic efficiency but it can also help identify species’ limits
to water transport. This is because the vascular features that
allow us to model conductivity can also capture the susceptibility of xylem to hydraulic failure caused by drought or
freeze–thaw induced cavitation. In this way, wood anatomy
can potentially serve as an additional indicator of a fossil
plant’s access to water and ⁄ or palaeoclimate.
Water transport by the C–T mechanism works remarkably
well but it is not without its limitations. When leaf transpiration exceeds the transport capacity of the xylem such as during
a drought, the pressure in the water column can become negative enough to allow the phase change of water from a liquid
to a vapour state. This transition is known as cavitation or
air-seeding, and it is caused by the aspiration of air into the
transpiration stream through the pit membrane. If the pull of
the transpiration stream creates sufficient tension in the sap,
the air bubble expands and the conduit is simultaneously
drained of water. Ultimately, a mixture of air and vapour fills
Fig. 7 The per cent loss of conductivity (PLC) and cavitation pressure (P50) in
response to either a combination of freeze–thaw and water stress, or water
stress alone at the range of xylem pressures in stems of Utah Juniper (from
Pittermann & Sperry, 2005).
the entire conduit to create an embolism, which blocks water
transport in that cell (Fig. 6). Because embolism reduces the
number of functional conduits, water must subsequently
travel from the root to the leaf at progressively more negative
xylem pressures through a higher resistance pathway. Under
increasing drought conditions, these higher tensions predispose the xylem to further cavitation events that can potentially
lead to the dangerous situation of runaway embolism and
plant death (Tyree & Sperry, 1988; Hacke & Sperry, 2001;
Tyree & Zimmermann, 2002; Choat et al., 2008).
Species’ cavitation resistance is typically presented in the
form of vulnerability curves, which express the per cent loss of
hydraulic conductivity due to embolism in response to more
negative water potentials (Fig. 7; Hacke & Sperry, 2001).
Vulnerability curves can be generated from almost any portion
of a plant such as roots, stems and leaves. The xylem pressure
at which a segment exhibits 50% loss of hydraulic conductivity
is referred to as the P50, or the ‘cavitation pressure’, and can
be used to compare cavitation resistance between plant organs
or species.
Despite the looming threat of a hydraulic catastrophe,
plants are only as cavitation resistant as their environment
requires them to be. This is because there are several costs
associated with embolism resistance, namely carbon investment and reduced transport efficiency. Progressively negative
water potentials can threaten xylem conduits with implosion
because the tension exerted on the water column exposes the
conduit walls to a combination of hoop and bending stresses
(Hacke et al., 2001). Hence, xylem conduits must be sufficiently, but not overly reinforced to withstand wall collapse.
Anatomically, this translates to a tight, positive correlation
between the ratio of conduit double wall thickness (t) to
hydraulic mean lumen diameter, that is the empty space confined by the inner walls of the conduit [b; (t ⁄ b)h2] and species’
cavitation pressure (Fig. 8; Kolb & Sperry, 1999; Hacke
2010 Blackwell Publishing Ltd
The evolution of water transport in plants
Fig. 8 Species’ cavitation pressure as a function of the wall thickness to lumen
diameter ratio (data from Hacke et al., 2001; Pittermann et al., 2006a,b; Pratt
et al., 2007, J. Pittermann, unpublished data). Archaeopteris cavitation
pressure was estimated from fossil root and stem material (courtesy of D.
Erwin).
et al., 2001; Hacke & Sperry, 2001; Pittermann et al., 2006a;
Jacobsen et al., 2007). Consequently, the greater investment
in xylem wall content is reflected in higher wood densities as
well as improved mechanical strength, and thus represents the
carbon cost of cavitation resistance (Hacke et al., 2001; Baas
et al., 2004; Jacobsen et al., 2007; Pratt et al., 2007).
However, the thickness:span relationship is driven by variation
in conduit diameter rather than wall thickness, which explains
the general trend for reduced hydraulic conductivity with
increased resistance to cavitation (Hacke et al., 2006; Pittermann et al., 2006a; Sperry et al., 2006). Although conduit
diameter is also coupled with species’ cavitation pressure,
there is much variation in this relationship and a broad
sampling is required to achieve adequate resolution (Fig. 9).
Hence, conduit (t ⁄ b)h2 serves a much better structural
correlate with cavitation pressure than conduit diameter.
Unlike angiosperm xylem which features fibres for structural support and vessels for water transport, conifer xylem is
homoxylous, meaning that its tracheids serve both a transport
as well as a support role. This means that on average, stem
tracheids exhibit greater (t ⁄ b)h2 than vessels at a given cavitation pressure (Fig. 8; Sperry et al., 2006; Hacke et al., 2001).
To achieve improved cavitation resistance, an increase in
tracheid (t ⁄ b)h2 is accomplished by shrinking the tracheid
lumen diameter rather than increasing tracheid wall thickness.
Consequently, conifer xylem exhibits a 46-fold range in hydraulic conductivity – a significant strength versus transport efficiency
trade-off (Pittermann et al., 2006a; Sperry et al., 2006).
A similar cavitation safety versus efficiency trade-off is
evident in angiosperms but unlike in the conifers, it may be
more tightly coupled to the process of air seeding at the pit
level. The recently proposed ‘pit area hypothesis’ suggests that
vulnerability to air seeding is related to the intervessel pit area
on a conduit. As air seeding in angiosperms is thought to
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129
Fig. 9 The relationship between species cavitation pressure and conduit diameter (data from Sperry et al., 2006; J. Pittermann, unpublished data).
occur through the largest pore on a pit membrane, the likelihood of an air seeding event rises with increasing pit area
(Wheeler et al., 2005; Sperry et al., 2006; Choat et al., 2008).
Intervessel pit area scales with vessel diameter, thus providing
an explanation for the weak, although consistent relationship
between vessel diameter and vulnerability to cavitation.
In conifers, air seeding is also thought to occur through the
pit membrane but no relationship exists between the pit area
and cavitation pressure (Pittermann et al., 2006b). In water
filled tracheids, water moves from one tracheid to another
through the porous margo region of the pit membrane.
Should one tracheid become embolized, surface tension in
the margo deflects the pit membrane such that the torus is
appressed against the pit aperture and air is prevented from
entering the neighbouring, functional tracheid. Air seeding
occurs when the xylem pressure is negative enough to dislodge the torus from its sealing position (Fig. 6). Consequently, it is the ratio of the torus diameter to the pit aperture
diameter that is thought to control air seeding in conifers,
while the progressive reductions in pit aperture with P50 may
represent the pit-level hydraulic cost of cavitation resistance
(Burgess et al., 2006; Domec et al., 2008; Hacke & Jansen,
2009).
Lastly, hydraulic dysfunction may also be caused by freeze–
thaw cavitation, a common phenomenon in plants inhabiting
seasonal or high elevation climates. When xylem sap freezes,
dissolved gases are coalesced into bubbles during ice formation. This is because air is insoluble in ice. The bubbles remain
inert while the sap is frozen, but may expand as it melts and
tensions are re-introduced into the xylem. If xylem pressures
are sufficiently negative during thawing, the largest of these
bubbles may expand and nucleate an embolism (Figs 6 and 7).
The likelihood of freeze–thaw induced embolism is described
by a modification of the capillary equation, such that the xylem
pressure (PX) must be more negative than the critical freeze–
thaw cavitation pressure (PXF) in order for the bubble to
expand and embolism to occur,
130
J. PITTER MANN
PXF ¼
2T
;
rb
ð8Þ
where T is the surface tension of water and rb is the radius of
the largest bubble. Hence, the larger the bubble, the less
negative the PXF required for bubble expansion (Davis et al.,
1999; Pittermann & Sperry, 2003).
In contrast to drought-induced embolism, conduit diameter is explicitly linked to species’ vulnerability to freezing
induced embolism. This is because rb is a function of radial air
content, which is directly proportional to conduit diameter
(Pittermann & Sperry, 2003, 2005). Practically, this means
that species with an average conduit diameter >30 lm are
highly susceptible to freeze–thaw cavitation, even under
mildly negative xylem tensions. By contrast, plants with
narrow conduit diameters are largely protected from this form
of stress because the smaller bubbles that are produced upon
freezing have a greater tendency to shrink and redissolve
during the thaw (Pittermann & Sperry, 2005). Hence, taxa
with narrow conduits such as alpine conifers are freeze–thaw
cavitation resistant but at the cost of reduced hydraulic
conductance, while the opposite is true of plants with
large-diameter conduits.
The interdependence between xylem pressure and conduit
diameter was examined in conifer wood, and used to roughly
approximate the freeze–thaw vulnerability curves from a
tracheid diameter distribution according to,
PXF ¼ 120Df1:53 ;
ð9Þ
where Df is the critical cavitation diameter, which is the
conduit diameter that will embolize due to freezing and thawing at a pressure PXF (Pittermann & Sperry, 2005). Whether
equation 9 applies to angiosperm wood is currently unknown.
Although the relationships between wood anatomy
and resistance to drought and freeze-thaw stress are well
developed and could potentially be applied to fossil material,
it is important that any inferences about species’ habitat or
microhabitat based on xylem anatomy be approached with
caution. If possible, conclusions should consider the evolutionary lineage, the overall plant form, and leaf venation
patterns, which are coupled to species hydraulic and photosynthetic capacity (Sack & Frole, 2006; Brodribb et al., 2007;
Brodribb, 2009), and may also be related to habitat (Royer
et al., 2008). For example, inferences about species’ resistance
to drought-induced cavitation based on diameter alone may
be erroneous, because conduit diameter can be weakly linked
to cavitation in angiosperms (Wheeler et al., 2005; Sperry
et al., 2006) but may be influenced by evolutionary lineage in
both angiosperms and conifers (Cavender-Bares & Holbrook,
2001; Pittermann et al., 2006a,b). We know that despite
having xylem with large diameter conduits, ring-porous species such as oaks, are actually resistant to drought-induced
cavitation and exhibit low water potentials in situ (Cochard
et al., 1992) and may thus deviate from the seemingly simple
relationship that should exist between conduit diameter and
P50. However, the relationship between vessel diameter and
vulnerability to freezing-induced cavitation in oaks is generally
consistent with theory (Sperry & Sullivan, 1992; Davis et al.,
1999; Cavender-Bares et al., 2005).
The relationship between stomatal conductance and the
structure and function of xylem
The guiding principle of effective water transport is that the
hydraulic supply of water must meet the transpirational
demands of the leaves (Sperry et al., 1998; Sperry, 2000).
Not surprisingly, the stomata play a key role because should
the water supply become compromised, or transpiration
exceed the plant’s hydraulic capacity, stomatal closure is the
first line of defence against desiccation. However, stomatal
conductance (gs) must also be well regulated because an inappropriately low gs will impose a carbon limitation on photosynthesis. Hence, photosynthesis and stomatal conductance
are closely coupled in what was probably the first of an
integrated sequence of adaptations that transformed the
gas-exchange characteristics of plants during their colonization of land (Hetherington & Woodward, 2003; Franks &
Brodribb, 2005; Franks & Beerling, 2009a,b). Stomatal
distributions have been used to infer palaeoclimates from
fossil leaves but can leaf stomatal distributions lead us to an
improved understanding of plant palaeophysiology?
The close coupling between stomatal conductance and
water transport is well documented and several studies have
shown that alterations in stem water transport can cause either
stomatal closure or stomatal opening. Stomatal behaviour is
governed by the vapour pressure deficit between the leaf interior and ambient atmosphere, water status, the leaf boundary
layer, soil-to-leaf water transport and chemical signals such as
abscisic acid. However, it is the leaf water status that encapsulates the holistic effect of these factors on stomatal conductance because leaf water potential regulates the turgor
pressure of both stomatal guard cells as well as the subsidiary
cells surrounding the stomata (Meinzer & Grantz, 1990;
Saliendra et al., 1995; Buckley, 2005). Not surprisingly, the
leaf water potential is to a large extent, controlled by the
transport capacity of the xylem and its ability to recharge water
lost by transpiration. Indeed, an artificial reduction of xylem
transport rapidly induces stomatal closure and reduces transpiration, whereas root pressurization restores leaf water potential and induces stomatal opening (Saliendra et al., 1995;
Hubbard et al., 2001). Alternatively, partial de-foliation of
the plant canopy increases the supply of water relative to the
demand, thereby inducing an increase in stomatal conductance (Oren et al., 2001).
A strong relationship exists between stem hydraulic
conductance and photosynthesis suggesting that leaf gas
exchange is proportional to, or constrained by vascular supply (Brodribb & Feild, 2000; Hubbard et al., 2001; Santi-
2010 Blackwell Publishing Ltd
The evolution of water transport in plants
2010 Blackwell Publishing Ltd
0.6
–2
–1
s )
was well over 50% lower than that of the 340 ppm grown
plants. A similar response was observed across eight species of
conifers grown at 280 and 800 ppm (J. Pittermann, unpublished data, Fig. 10). These results imply that plants may have
been predisposed to a high degree of water stress during periods of low CO2 such as the Pleistocene glacial periods.
Increased susceptibility to drought stress combined with
reduced water use efficiency may have been a contributing factor to the reduced vegetation cover during the Pleistocene
(Cowling & Sykes, 1999).
If we accept that the apparent changes in stomatal densities
are consistent with the fluctuating CO2 levels of the Mid-toLate Phanerozoic, then atmospheric CO2 may have had a profound effect on the whole plant conductance to water. For
example, the ‘topdown’ stomatal response to CO2 may have
at various times selected for plant hydraulic architecture that
was better equipped to mine water via deeper and more complex root systems. Such plants may have also been more efficient at transporting water by allocating a greater proportion
of resources to xylem, or by increasing the transport efficiency
of their xylem tissue. Hence, under periods of good water
availability and low atmospheric CO2, it is tempting to speculate that selection may have favoured the presence of more
efficient, large-diameter conduits or a greater fraction of tissue
devoted to water transport, in order to meet the increased
transpirational demands inherent to leaves with high stomatal
densities.
The alternative hypothesis is that reduced atmospheric CO2
levels may have imposed a carbon limitation on growth in a
manner that reduced leaf area, such that whole-plant transpiration scaled with reduced plant size. Consequently, xylem
area ⁄ leaf area, leaf-specific hydraulic efficiency and conduit
diameter would remain unchanged. Indeed, several studies
have shown smaller leaf areas in plants grown under subambient CO2 (Dippery et al., 1995; Cowling & Sage, 1998).
However, the data do indicate that transpiration rates
continue to be higher in these plants than those grown at
ambient CO2 levels (Ward et al., 1999), suggesting that on a
whole-plant scale, the increased water loss may also impose a
Stomatal conductance (g, mol m
ago et al., 2004; Maherali et al., 2008; Brodribb, 2009).
These findings are corroborated by extensive work documenting the coupling between leaf vasculature, stomatal
conductance and gas exchange across a variety of plant life
forms (Brodribb et al., 2003, 2005). Because at least 25% of
the total resistance to plant water flow resides in the leaves,
leaves may exert a disproportionately high degree of control
over plant water relations (Sack et al., 2003). It may also be
that the leaf stomatal and vascular performance may affect
the structure and function of ‘upstream’ stem xylem,
although that possibility has not previously been discussed.
Certainly, such a co-ordinated response would require some
degree of phenotypic plasticity in both the leaves and the
xylem in the short term, but it may also have significant
long-term or even deep-time evolutionary implications on
the structure and function of xylem.
Atmospheric CO2 levels may have constrained the structure and function relationships of soil-to-leaf hydraulic transport in just such a manner. There is much geological,
biological and theoretical evidence to suggest that atmospheric CO2 levels have fluctuated dramatically over time
(Zachos et al., 2001; Beerling, 2002; Berner, 2006; Fletcher
et al., 2008). Indeed, CO2 levels are thought to have reached
highs well over 4000 ppm during the Devonian and lows
below 500 ppm during the Carboniferous (Fig. 1). Interestingly, much of the evidence for deep-time atmospheric CO2
fluctuations has either been derived from or corroborated by
measures of the leaf stomatal response. Specifically, it has
been shown that across a broad sampling of plants from the
angiosperms and conifers, stomatal density increases in
response to low atmospheric CO2 whereas the opposite is
true under elevated levels of CO2 (Woodward, 1987;
McElwain et al., 1999; Royer et al., 2001; Retallack, 2001;
Beerling, 2002; Kouwenberg et al., 2003). Data derived
from the stomatal index, a more refined measure of the
stomatal response that controls for leaf expansion, also
indicate that in some taxa, CO2 is a developmental driver of
leaf stomatal distributions (Lake et al., 2002). The discovery
that stomatal abundance is related to atmospheric CO2 augmented our understanding of palaeoclimates because CO2
could be retrodicted from leaves much older than ice cores.
In this way, stomatal density in combination with isotope and
palaeosol signals serves as a reasonable CO2 proxy with which
to evaluate the accuracy of climate models.
We know, however, that stomata play a dual role in regulating water loss as much as CO2 uptake, yet the effect of vacillating CO2 levels on the palaeo-physiology, especially water
relations of the sampled plants have attracted less attention.
The effect that increasing stomatal densities may have on leaf
water loss was apparent to Woodward (1987) who showed
that the stomatal conductance of Acer pseudoplatanus seedlings grown under 225 ppm of CO2 was twice as high as that
of seedlings grown under 340 ppm. Functionally, this meant
that the water-use efficiency of the 225 ppm-grown seedlings
131
0.5
800 ppm grown
280 ppm grown
0.4
0.3
0.2
0.1
0
ia
on
oia ns
uo es dium
dr
m equ vire
eq oid
en
o
tas trob Tax ichu S per
iad teum
e
o
t
m
M tos
qu an
dis
se
p
Se gig
gly
ga
s
us
rix lis
tsu i
nu sa
La enta Pin ottii
Pi ero
do si
eu nzie
lli
id
nd
s
e
c
P me
po
oc
Fig. 10 The stomatal conductance of Cupressaceaous and Pinaceous conifer
seedlings grown at 280 and 800 ppm in growth cabinets (mean ± SD; J. Pittermann, unpublished data).
132
J. PITTER MANN
significant physiological limitation. Lastly, an increase or
decrease in the pressure gradients within the xylem may alter
the flow rates such that transpirational demands are effectively
met without a need for anatomical changes in the xylem tissue
(Fig. 11). This response, would however predispose the plants
to a greater possibility of cavitation caused by air seeding.
We can begin to explore the impact of atmospheric CO2 on
plant water relations by returning to some basic relationships
between xylem transport, anatomy and stomatal conductance.
The relationship between gs and leaf-specific hydraulic
conductance (Kl) can be described such that,
gs ¼ K 1
DW
;
VPD
ð10Þ
where DW is the water potential difference between the soil
and the leaves (Wsoil ) Wleaf) driving water movement and
VPD represents the vapour pressure deficit between the leaf
interior and the ambient air (Bond & Kavanagh, 1999;
Hubbard et al., 2001). Kl is a measure of hydraulic efficiency
on a whole-plant basis (Bond & Kavanagh, 1999; Sperry,
2000; Hubbard et al., 2001). If we assume that ks scales with
Kl (certainly ks scales with leaf-specific conductivity, Kl; J. Pittermann, unpublished data), then substituting equation 2 for
Kl in equation 10 yields the final relationship,
gs 1
ðDWÞpRD 4
:
A128gVPD
ð11Þ
Equation 11 expresses a theoretical correlation between
stomatal conductance and the theoretical maximal transport
capacity of the xylem, as constrained by conduit diameter.
Simplistically, equation 11 implies that an overall rise in gs
requires an increase in conduit diameter, for a given xylem
area. Such a transport response would require the co-ordination between the vascular cambium and stomatal patterning
during leaf development, and there is evidence to suggest that
in some species, stomatal development is labile and thus
responsive to atmospheric CO2 (Lake et al., 2002; Beerling,
2005) but whether this couples to vascular development
remains unknown. Alternatively, xylem anatomy may exhibit
limited phenotypic plasticity, and thus impose fundamental
limits on leaf gas exchange as appears to be the case in diffuse
and ring porous angiosperm trees (Bush et al., 2008).
If a link does indeed exist between atmospheric CO2, stomatal conductance, stomatal density and vascular design, it is
tempting to speculate that the 70 million years during the
Mid-Devonian to Early Carboniferous provided atmospheric
conditions that supported the evolution of secondary xylem
(wood). Climate models suggest that this period of the Phanerozoic was characterized by CO2 levels that are thought to
have been at least as low or lower than those of today, and
which may have stimulated not only an increase in stomatal
densities but also the appearance of large leaves (Beerling
et al., 2001; Osborne et al., 2004). Furthermore, it is at this
time that elevated atmospheric oxygen levels are thought to
have supported an increase in xylem lignification and possibly
selection for woody taxa (Graham et al., 1995; Berner, 2005;
Berner et al., 2007). A concurrent argument is that low CO2
selected for high stomatal densities, which in turn increased
evaporative cooling thereby releasing leaves from the constraints of overheating. This is also consistent with survey
results from the fossil record showing a 25-fold enlargement of
leaf areas during this time (Osborne et al., 2004). In any case,
if atmospheric CO2 precipitated changes in leaf size and stomatal density, then we might expect a co-ordinated response from
the vascular system designed to increase transport efficiency.
A
B
Fig. 11 Some theoretical relationships between
xylem structure and function in response to low and
high ambient CO2.
2010 Blackwell Publishing Ltd
The evolution of water transport in plants
PART IV: CONCLUDING REMARKS
Plant water transport and climate
Plant water transport irrevocably changed our planet. Even
the earliest transpiring plants would have subtly modified their
local water regime, whereas the Devonian forests were probably key players in the formation of soils, carbon sequestration
and climate change (Retallack, 1997; Algeo & Scheckler,
1998; Berner, 2005; Berner et al., 2007) Xylem function certainly impacts atmospheric moisture, and the Amazon rainforest is a dramatic, modern day example of how large-scale
water transport controls continental climates as nearly 50% of
global precipitation is recycled from forests (Malhi et al.,
2008). Deep roots extract and potentially re-distribute the soil
water that is ultimately transpired back to the atmosphere, a
phenomenon that is critical to maintaining hydration when
high evaporative demand and reduced rainfall conspire to
reduce stomatal conductance, such as during the dry season
(Oliveira et al., 2005). Consequently, extensive deforestation
tends to lower evapotranspiration, cloud formation and rainfall by a feedforward effect that progressively reduces ecosystem water cycling. Model projections suggest that the
removal of 30–40% of the Amazonian forest could drive the
region into a permanently drier climate regime (Oyama &
Nobre, 2003). Regional meteorological phenomena will also
be affected by alteration of the forest canopy boundary effects
so, taken together, there is indisputable evidence that plant
water transport is a key element of large-scale ecosystem stability (Betts et al., 2004).
Evapotranspiration is a common metric of area-based
terrestrial water loss but recent work suggests that transpiration alone can modify continental hydrology. Extensive
field studies have shown that elevated CO2 reduces stomatal conductance and transpiration, an effect that generally
improves the water balance of terrestrial vegetation (Korner, 2003). However, the suppression of transpiration leads
to greater water retention in soils and ultimately higher
water discharge into rivers, a phenomenon referred to as
‘physiological forcing’ (Betts et al., 2007). How would this
scenario play out under low CO2 conditions, which typically
give rise to increased stomatal conductance? Given the
uncertainties of climate modelling, a simple answer may
not exist but all things being equal, a reasonable guess may
be that increased transpiration would lower soil moisture,
and thus impact terrestrial water levels.
Future directions
Plant vascular tissue is one of potential drivers of plant diversification (Donoghue, 2005), so much insight can be gained
into the evolution of plants by applying a neontological and
quantitative approach to fossil wood. Although the Hagen–
Poiseuille method of computing theoretical hydraulic efficien-
2010 Blackwell Publishing Ltd
133
cies is useful, incorporating pit resistance into fossil plant
transport models will allow us to broaden our understanding
of xylem function in extinct plants, as well as the significance
of evolutionary transitions from one conduit type to another
such as in the case of the Rhyniophytic plants. As we do this
however, comparative studies of xylem structure and function
in modern taxa need to develop within a broader evolutionary
framework. For example, we know little about the relationships between cavitation resistance, pit resistance and hydraulic efficiency in monocots and Gnetales.
Aside from the extensive descriptive work documenting the
anatomy of fern xylem, not much is currently known about
the comparative hydraulics of ferns, and the homogenous fern
intertracheid pit membrane in particular (Carlquist & Schneider, 2007). This is important information because tracheids
with homogenous pit membranes represent the ancestral state
of xylem in leafy tracheophytes (Euphyllophytes; Kenrick &
Crane, 1997). However, new data collected from across the
fern lineage show that fern xylem is as efficient on an
area basis as that of angiosperms and conifers (J. Pittermann
& E. Limm, unpublished data), suggesting that the large
tracheid size in combination with what appears to be a highly
permeable pit membrane (Carlquist & Schneider, 2007) combine
to ramp up water transport in an otherwise seemingly suboptimal combination of vascular traits (Pittermann et al., 2005).
We can also exploit our current understanding of the relationship between pit area and pit structure in angiosperms and
conifers respectively, to gain more insight into the drought
resistance of early land plants. The pit area hypothesis holds
across angiosperms of different evolutionary lineages,
although membrane porosity may also variably affect resistance to cavitation (Jarbeau et al., 1995; Hacke et al., 2006,
2007; see also Choat et al., 2008). Assuming that pit membranes are well preserved in fossil specimens, perhaps the best
approach may be to examine the pit membrane size, scaling
and porosity in a comparative manner, sampling taxa across
the land plant phylogeny.
Understanding the structure and function of xylem can
inform us not only about the physiological limits of plant
water transport and the constraints it places on photosynthesis, but this information also has potential to augment models
of palaeocommunity assembly. For instance, the Devonian
and Carboniferous are characterized by significantly different
climatic patterns than those of today, as well as changes in the
relative positions of land masses and tremendous diversification of the terrestrial flora (DiMichele & Gastaldo, 2008).
Plant distributions in these ancient and unfamiliar landscapes
will, to some extent, be determined by xylem efficiencies and
drought resistance. Altogether, this is an excellent time to
fruitfully study the evolution of plant water transport across a
multitude of scales, ranging from the molecular, organismal
and up to the ecosystem level. Certainly, the intersection of
plant physiology and palaeobotany offer much opportunity
for truly novel discoveries.
134
J. PITTER MANN
ACKNOWLEDGMENTS
I am very grateful to the three anonymous reviewers
whose thoughtful comments and copious advice dramatically
improved this manuscript. Also, many thanks to David
Beerling for the generous opportunity to contribute this
paper. I am also grateful to Lucy Lynn for editorial assistance,
and Brendan Choat, Emily Limm and Jim Wheeler for their
helpful comments. Dr Diane Erwin (UC Berkeley Museum of
Natural History) kindly loaned Archaeopteris fossil material,
and the Miller Institute for Basic Research at UC Berkeley
provided generous support during the preparation of this
manuscript.
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