Download Leaf Evolution: Gases, Genes and Geochemistry

Annals of Botany 96: 345–352, 2005
doi:10.1093/aob/mci186, available online at www.aob.oupjournals.org
BOTANICAL BRIEFING
Leaf Evolution: Gases, Genes and Geochemistry
DAVID J. BEERLING*
Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK
Received: 24 February 2005 Returned for revision: 23 March 2005 Accepted: 12 April 2005 Published electronically: 19 June 2005
Aims This Botanical Briefing reviews how the integration of palaeontology, geochemistry and developmental
biology is providing a new mechanistic framework for interpreting the 40- to 50-million-year gap between the
origination of vascular land plants and the advent of large (megaphyll) leaves, a long-standing puzzle in evolutionary
biology.
Scope Molecular genetics indicates that the developmental mechanisms required for leaf production in vascular
plants were recruited long before the advent of large megaphylls. According to theory, this morphogenetic potential
was only realized as the concentration of atmospheric CO2 declined during the late Palaeozoic. Surprisingly, plants
effectively policed their own evolution since the decrease in CO2 was brought about as terrestrial floras evolved
accelerating the rate of silicate rock weathering and enhancing sedimentary organic carbon burial, both of which are
long-term sinks for CO2.
Conclusions The recognition that plant evolution responds to and influences CO2 over millions of years reveals the
existence of an intricate web of vegetation feedbacks regulating the long-term carbon cycle. Several of these
feedbacks destabilized CO2 and climate during the late Palaeozoic but appear to have quickened the pace of
terrestrial plant and animal evolution at that time.
Key words: Carbon cycle, feedbacks, fossil plants, genetics, geochemistry, leaves, stomata.
INTRODUCTION
Plants evolved leaves on at least two independent occasions
and the legacy of these historic evolutionary events is represented in extant floras by microphylls in lycophytes
(clubmosses, spikemosses and quillworts) and megaphylls
in euphyllophytes (ferns, gymnosperms and angiosperms).
Microphylls, with a distinctive vasculature and (usually)
unbranched venation, are thought to have evolved from
spine-like enations and predate megaphylls in the terrestrial
plant fossil record (Gifford and Foster, 1988). Of greater
significance, however, was the origin of megaphylls in
vascular plants through the developmental modification
of lateral branches. Megaphylls altered the evolutionary
trajectory of terrestrial plant and animal life, the biogeochemical cycling of nutrients, water and carbon dioxide and
the exchange of energy between the land surface and the
atmosphere. The vast majority of the estimated 250 000 or
so extant species of flowering plants, as well as most
gymnosperms and (extinct) pteridosperms, utilize(d) a flatbladed megaphyll with a network of veins to capture
solar energy for photosynthetic carbon assimilation. A
true measure of their success in terrestrial environments
is the capacity of leaves to endure climatic extremes
between the tropics and the tundra whilst simultaneously
facilitating the global scale net fixation of approx. 207 billion tonnes of CO2 (564 · 1015 g C) year1 (Field et al.,
1998). This primary production provides energy for virtually all forms of terrestrial life on Earth, especially tetrapods
and insects, and links many ecosystem and biogeochemical
processes.
Evidently, leaves are a global success. However, the
advent of large megaphylls took place some 40–50 million
* E-mail [email protected]
years (Myr) after the origination of vascular land plants,
suggesting that they were far from an evolutionary inevitability. The earliest ancestral vascular plants, dating to the
late Silurian 410 Myr ago (Edwards and Wellman, 2001),
were composed of simple or branched axial stems with
sporangia but no leaves. Surprisingly, plants continued to
remain leafless for the next 40–50 Myr, with megaphylls
finally becoming widespread at the close of the Devonian
period (360 Myr ago) (Kenrick and Crane, 1997; Boyce and
Knoll, 2002; Osborne et al., 2004a,b). Surprise in the
delayed appearance of a seemingly simple developmental
modification is 3-fold. First, palaeontological evidence
shows that the structural framework necessary for assembling a simple laminated leaf blade (meristem, vasculature,
cuticle and epidermis) (Kenrick and Crane, 1997) was in
place long before the advent of large megaphylls. Secondly,
the same interval marks an unparalleled burst of evolutionary innovation in the history of plant life, which witnessed
the rise of trees from herbaceous ancestors, and the evolution of complex life cycles, including the seed habit
(Kenrick and Crane, 1997). Thirdly, the tiny deeply incised
megaphylls of the rare early-Devonian plant Eophyllophyton bellum from Chinese rocks shows that plants had
the capacity to produce a simple megaphyll (Hao and Beck,
1993; Hao et al., 2003). Why were plants unable to release
this morphogenetic potential?
Until recently, our understanding of the evolution of
megaphylls largely stemmed from Zimmermann’s telome
theory (Zimmermann, 1930, 1952) describing the sequence
of overtopping, planation and webbing leading to appearance of the laminated leaf blade. The ancestral form of
a dichotomizing axis branching out in three dimensions
and typified by the rhyniophytes (Fig. 1) represents the
basal state in the telome theory. Evolutionary ‘overtopping’
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Beerling — Leaf Evolution: Gases, Genes and Geochemistry
Overtopping
Planation
410 Myr ago
390 Myr ago
Simple branching
(e.g. Rhynia)
Main stem bearing
side branches
(e.g. Psilophyton)
Webbing
380 Myr ago
Side branches
dividing in the
same spatial plane
(e.g. Actinoxylon)
370 Myr ago
Infilling between
side branches
to produce a
true leaf
(e.g. Archaeopteris)
F I G . 1. Stages in the evolution of the megaphyll as documented by Zimmermann’s telome theory (Zimmermann, 1930), with representative fossil plants for
each stage illustrated below. Upper schematic: Osborne et al. (2004b), images of Rhynia, Psilophyton and Archaeopteris after Gifford and Foster (1988),
image of Actinoxylon after Matten (1968).
followed producing a main axis bearing reduced, lateral,
determinate photosynthetic stems, branching out in three
dimensions (e.g. trimerophytes). These 3-D lateral branch
systems of terete stem segments then became ‘flattened’
into a single plane (e.g. cladoxyaleans). Finally, a webbing
of photosynthetic mesophyll tissue joined the flattened
segments of the lateral branches to form a laminate leaf
blade (e.g. some progymnosperms) (Fig. 1). In this scheme,
transformation of a branch into a leaf was achieved by
simple modification of existing organs rather than a major
change in body plan.
Over 70 years ago, Zimmermann’s scholarly telome
theory provided a first glimpse of the ‘how’, but left
unanswered the thorny question of ‘why’ it took 40–
50 Myr to evolve leaves. This Botanical Briefing provides
an overview of a new mechanistic explanation linking
atmospheric CO2 decline with the delayed widespread
appearance of megaphylls, and ideas concerning its molecular genetic basis and the resulting global environmental
and evolutionary consequences. The explanation emerges
from a theoretical analysis incorporating modern-day
plant processes and biophysical principles governing the
energy balance of photosynthetic organs (Beerling et al.,
2001). Developmental genetic mechanisms underpinning
aspects of stomatal and leaf formation (Gray et al., 2000;
Cronk, 2001; Floyd and Bowman, 2004; Harrison et al.,
2005; Sano et al., 2005) provide additional new insight
allowing progress towards a unified framework for understanding leaf evolution. In the final section of this Briefing, I
consider how recognizing a role for CO2 in leaf evolution
has shed new light on multiple biotic feedbacks within the
geochemical carbon cycle and on evolutionary processes
themselves (Oddling-Smee et al., 2003; Beerling and
Berner, 2005).
EVOLUTION OF THE LEAF AND
ATMOSPHERE
The mechanistic hypothesis of Beerling et al. (2001) links
the gap between the earliest vascular plants and the advent
of large megaphylls with a dramatic 90 % drop in the
atmospheric CO2 concentration during the late Palaeozoic
(Berner, 2004). The large fall in CO2 corresponded with a
marked rise in the stomatal density of vascular land plants,
with densities increasing a 100-fold from 5–10 mm2 on
early vascular plant axes to 800–1000 mm2 on the cuticles
of late Carboniferous megaphylls (McElwain and Chaloner,
1995; Edwards, 1998). These evolutionary shifts in leaf
anatomy are consistent with the effects of CO2 on stomatal
development observed in modern plants cultivated in
controlled conditions under different CO2 concentrations
(Woodward, 1987).
According to theoretical calculations with a model of leaf
biophysics and physiology, the rise in stomatal density held
special significance for the evolution of leaves by permitting
greater evaporative cooling and alleviating the requirement
for convective heat loss (Beerling et al., 2001). Simulations
indicate that archaic land plants with axial stems, few stomata, and low transpiration rates only avoided lethal overheating because they intercepted a minimal quantity of solar
energy (Beerling et al., 2001; Roth-Nebelsick, 2001).
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Beerling — Leaf Evolution: Gases, Genes and Geochemistry
Devonian
Early
Mid
CO2 (ppmv)
Frs
Carbonif.
Tou Vis
Has
Aru
Chd
Ivo
5000
Late
Fam
Lok
Giv
Eif
Ems
Pra
A
4000
3000
2000
1000
Maximum width (mm)
80
60
40
20
Calculated maximum
height (m)
0
C
10
1
4
Organic C burial
(1018 mol Myr–1)
B
D
Burial rate
Terrestrial fraction
0·8
3
0·6
2
0·4
1
0·2
0
0·0
410 400 390 380 370 360 350 340
Age (Myr)
Fraction of total
organic C burial
In contrast, a megaphyll intercepting at least twice as much
solar energy (per unit area of the photosynthetic organ)
reached temperatures approaching the highly conserved
lethal threshold of extant tropical taxa (Beerling et al.,
2001) because the same limited evaporative cooling was
inadequate to dissipate the absorbed thermal energy. Theoretical arguments therefore indicate that early vascular
land plants were prevented from developing large laminate
leaves because their low stomatal densities placed a tight
constraint on evaporative cooling.
Even if the stomatal density of the early vascular land
plants was not under the influence of atmospheric CO2, and
megaphylls evolved a high density, the transpiration rates
required to maintain cool temperatures (approx. 9–13 mmol
H2O m2 s1) are calculated to outstrip the capacity of
xylem to supply it by factor of ten, assuming the primitive
stele of Psilotum nudum is a reasonable analogue for that of
the early rhyniophytes (Schulte et al., 1987). In this case,
dehydration precluded the evolution of large megaphylls
with high stomatal densities in early land plants; no fossils
of such an anatomically modified organ have yet been
discovered.
By the time large laminate leaves became widespread in
late Devonian/early Carboniferous fossil floras, the concentration of atmospheric CO2 had fallen, and stomatal densities had increased by up to a 100 times the value of early
vascular land plant axes. Large leaves of late Devonian/
early Carboniferous plants attained transpiration rates sufficiently high to maintain temperatures well below the lethal
threshold, despite intercepting more solar energy (Beerling
et al., 2001). Greater evaporative cooling also meant that
large leaves stayed cool despite diminished convective heat
loss, a flux that declines with increasing leaf size as friction
across the surface slows the passage of air and the transfer of
heat. Large-leaved perennials in today’s deserts similarly
rely on a high transpiration rate to prevent overheating and
maintain leaf temperatures 8–18 C below that of the air
(Smith, 1978; Ehleringer, 1988), with some species in
southern California even evolving a correspondingly
lower temperature optimum for photosynthesis (Smith,
1978). For these large-leaved desert species, summertime
precipitation permits high transpiration rates. But in the late
Palaeozoic, the evolution of large leaves required the coevolution of the root and vascular systems for improved
water delivery and transport to sustain higher transpiration
rates (Knoll et al., 1984; Raven and Edwards, 2001). Deeper
roots accessed water and nutrients from a greater volume of
soil, whilst xylem conduit enlargement and the appearance
of secondary growth of xylem by the end of the Devonian
increased the hydraulic conductance through stems and
trunks to the leafy canopy, helping to maintain higher transpiration rates (Rowe and Speck, 2005).
The hypothesis of Beerling et al. (2001) makes the clear
prediction that larger leaves gradually appeared as CO2
levels declined and stomatal numbers rose to increase evaporative cooling and ease the thermal burden of absorbed
solar energy. Osborne et al. (2004a, b) achieved a successful
test of this prediction with a morphometric analysis of 300
fossil specimens archived in major European collections.
Their results showed a 25-fold enlargement of leaf blades as
F I G . 2. Evolution of the atmosphere and land plants in the late Palaeozoic.
(A) Changes in atmospheric CO2, modelled (open circles) or reconstructed
from fossil soils (closed). (B) Observed increase in maximum width of
megaphylls. Points indicate average maximum size for 5- or 10-Myr
intervals. (C) Maximum plant height calculated from measurements of
fossil stem diameter, assuming modern stem diameter–height
relationships. (D) Changes in terrestrial carbon burial. Modified after
Beerling and Berner (2005).
atmospheric CO2 fell during the late Palaeozoic (Fig. 2B).
Leaf enlargement occurred first in the progymnosperms
during the mid- to late-Devonian with the initial radiation
of Archaeopteris and soon afterwards in the pteridosperms,
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Beerling — Leaf Evolution: Gases, Genes and Geochemistry
a group attaining a larger maximum size coincident with a
lower atmospheric CO2 concentration.
The consistent pattern of leaf blade enlargement seen in
these two phylogenetically independent clades (Boyce and
Knoll, 2002; Osborne et al., 2004a,b) is consistent with the
argument that CO2 acted as an environmental driver for this
aspect of plant evolution. But as the concentration of atmospheric CO2 declined to permit the evolution of leaves,
competition for light and space between neighbouring
plants intensified. Competition is therefore envisaged as
providing a powerful selective force for plants to become
leafier and taller. These shifting ecological interactions were
most obviously manifested as the well-documented increase
in plant size (Chaloner and Sheerin, 1979) that tracked
historical patterns of leaf enlargement (Fig. 2C).
GENES, LEAVES AND STOMATA
Leaves in vascular plants are produced by determinate
growth on the flanks of indeterminate shoot apical meristems. Inderminate growth of the shoot apical meristem
is controlled by the knotted-like homeobox gene family
(KNOX) (reviewed in Hake et al., 2004). KNOX genes
are present in some green algae (e.g. Acetabularia), mosses,
ferns, gymnosperms and angiosperms and their function
may be highly conserved (Sano et al., 2005). Overexpression of fern KNOX-like genes in Arabidopsis
thaliana, for example, produces a similar phenotype (altered
leaf shape) as over-expression of arabidopsis KNOX-like
genes in Arabidopsis (Sano et al., 2005). Proper development of leaves requires permanent negative repression of
KNOX genes and several genes have so far been discovered
in euphyllophyte species for maintaining the KNOX-off
state, including PHANTASTICA (PHAN) isolated from
snapdragon (Antirrhinum majus) (Waites and Hudson,
1995) and homologues of PHAN in maize (Timmermans
et al., 1999) and Arabidopsis (Byrne et al., 2000). The two
sets of genes operate in a co-ordinated manner with KNOXlike transcription factors repressing determinate growth promoted by PHAN, and PHAN-like transcription factors
repressing KNOX to promote indeterminacy.
The system is likely controlled by auxin, which determines the site of leaf initiation and is correlated with
decreased KNOX and increased PHAN activity. Environmental influences on KNOX and PHAN are not known.
However, it is interesting to note that the original PHAN
mutation in Antirrhinum was temperature-sensitive so that
plant morphology was approximately normal at 25 C but
altered at lower temperatures (Waites and Hudson, 1995),
implying an interaction of PHAN-mediated morphogenesis
with temperature-sensitive elements of leaf development.
Genes such as PHAN may be prime candidates for involvement in the first stage of the telome theory, i.e. the evolution
of determinant lateral shoot systems in trimerophytes
(Fig. 1) (Cronk, 2001).
Leaf production also requires differentiation between
adaxial (upper) and abaxial (lower) surfaces because the
former is specialized for the efficient capture of solar energy
and the latter for gas exchange. Deriving from the apical
vegetative meristem flank, the abaxial surface is as old as
land plants themselves, so genes specifying adaxial identity
constitute a key innovation in leaf evolution (Cronk, 2001).
Plants appear to have evolved a complex hierarchy of transcription factor activation and depression, with the HD-ZIP
(homeodomain–leucine zipper) gene family promoting
adaxial leaf surfaces and others promoting abaxial differentiation (Cronk, 2001). Interestingly, HD-ZIP gene expression is subject to a novel form of post-transcriptional
regulation involving microRNAs found in bryophytes, lycopods, ferns and seed plants suggesting that it may be very
ancient, dating back more than 400 Myr (Floyd and
Bowman, 2004). Interactions between HD-ZIP gene
and vascular tissue polarity have been demonstrated in
Arabidopsis (Emery et al., 2003) and, since vascular tissue
predates the leaf (Kenrick and Crane, 1997), this suggests
that the same developmental unit was recruited for leaf
polarity (Emery et al., 2003).
Whether megaphylls, which arose independently in four
vascular plant lineages (ferns, sphenopsids, progymnosperms and seed plants) (Boyce and Knoll, 2002; Osborne
et al., 2004a, b), recruited the same gene systems is open
to investigation (Cronk, 2001). However, this does seem a
possibility given that a common developmental mechanism
for leaf production appears to have been recruited independently at least twice in the evolution of land plants (Harrison
et al., 2005).
Current understanding of the genetic controls of stomatal
formation in response to environment signals is limited,
although it is clear that genetic modification more strongly
alters the relationship between stomatal density and pore
size, with attendant effects on leaf gas exchange, than shortterm changes in environmental conditions (Hetherington
and Woodward, 2003). Stomatal research on Arabidopsis
has identified the HIC (high carbon dioxide) gene, which
responds to CO2 and negatively regulates stomatal formation (Gray et al., 2000). HIC encodes a putative 3-ketoacyl
coenzyme-A synthase, an enzyme involved in the synthesis
of wax components found in the cuticle. Wax-deficient
mutant plants show a 42 % increase in stomatal density
with CO2 enrichment to 1000 ppm compared with that at
400 ppm CO2 (Gray et al., 2000). The possible involvement
of the HIC gene (or similar) in mediating stomatal formation
under different CO2 concentrations in other plant groups
remains to be seen.
VEGETATION FEEDBACKS AND
THE LONG-TERM CARBON CYCLE
The realization that aspects of plant evolution may be directed by changes in atmospheric CO2 gains greater significance when considered alongside the impact that plants
themselves exert on the long-term carbon cycle. Before
plants, Earth’s global climate and atmospheric CO2 were
regulated on a multi-million year timescale by the inorganic
carbon cycle, in which CO2 is supplied to the atmosphere by
volcanism and metamorphic degassing, and removed by
the chemical weathering of Ca–Mg silicate rocks (Walker
et al., 1981; Berner et al., 1983). The closed cycle can be
349
Beerling — Leaf Evolution: Gases, Genes and Geochemistry
D
B
Carbon
dioxide
Carbon
dioxide
Stomatal
density
Root and
symbiont
extent
Leaf/stem
temperature
Plant
size
Weathering
Climate
Weathering
Root and
symbiont
extent
Leaf/stem
temperature
Plant
size
A
Leaf
size
Leaf
size
Carbon
dioxide
Climate
C
Weathering
E
Carbon
dioxide
Carbon
dioxide
Stomatal
density
Organic
carbon
burial
Climate
Organic
carbon
burial
Leaf/stem
temperature
Plant
size
Leaf/stem
temperature
Plant
size
Leaf
size
Leaf
size
F I G . 3. Systems analysis diagrams of the long-term carbon cycle with and without geophysiological feedbacks involving land plants. (A) The inorganic
geochemical carbon cycle. (B and C) Geophysiological feedbacks introduced by plant evolutionary responses to changes in atmospheric CO2 that result in
changes in silicate rock weathering and organic carbon burial, respectively. (D and E) Geophysiological feedbacks as in B and C but including the direct
effects of CO2 on climate via the atmospheric greenhouse effect. Arrows originate at causes and end at effects. Blue, inorganic processes; green, organic
processes.
350
Beerling — Leaf Evolution: Gases, Genes and Geochemistry
represented as a simple systems diagram with arrows indicating a direct response (no bull’s-eyes) or an inverse
response (with bull’s-eyes) (Fig. 3A). In these diagrams
an even number of arrows with or without bull’s-eyes
defines a positive feedback and an odd number with
bull’s-eyes a negative feedback. The inorganic carbon
cycle (Fig. 3A) is stabilized by a negative feedback loop
because silicate-weathering rates increase with temperature
(Walker et al., 1981; Berner et al., 1983). Rising CO2 levels,
for example, strengthen the greenhouse effect, warm the
climate, accelerate the chemical weathering of Ca–Mg silicate rocks, remove CO2 from the atmosphere and lead to a
cooler climate (Fig. 3A).
The advent of rooted vascular land plants introduced a
potent biotic feedback into the long-term carbon cycle
(Berner, 2004). Plant activities greatly enhance silicate
rock weathering rates through a wide variety of processes.
Weathering proceeds as described by the overall reaction:
CO2 + ðCa, MgÞSiO3 ! ðCa, MgÞCO3 + SiO2
where Mg and Ca represent all calcium and magnesium
silicates and carbonates (e.g. dolomite). Equation (1) summarizes the net result of a wide variety of processes, the
most important being the secretion of organic acids and
chelates by rootlets (and associated symbionts) and the generation of CO2 by respiration of organic matter, both of
which break down silicate minerals and produce bicarbonate ions (Berner et al., 2003). Plant roots are especially
effective at accelerating chemical and physical weathering
of rocks and soils (Raven and Edwards, 2001; Berner et al.,
2003) by increasing the surface area of soil–root interface
directly and by fracturing mineral grains (Fig. 4). Roots also
anchor soils, and decelerate physical erosion, thus increasing the water contact time of primary minerals. At the
regional scale, recirculation of precipitation by evapotranspiration dissolves minerals more efficiently and enhances
transport of bicarbonate ions from soils into rivers (Berner
et al., 2003). After transport to the oceans by rivers, weathering products are removed by the formation of carbonates.
Plants are also the primary source of organic matter buried
in sediments.
For the past two decades, only two negative stabilizing
feedbacks on the long-term carbon cycle involving plants,
weathering and organic carbon cycle and have been identified (Volk, 1987, 1989). Recognizing CO2 as a driver of
plant evolution has revealed, through a systems analysis of
the intricate web of interactions, several new positive feedback loops (PFLs) that operate only when plants encounter a
warm climate (Beerling and Berner, 2005). These feedbacks
operate whether CO2 is rising or falling. However, in the
context of this Briefing, my comments are confined to the
late Palaeozoic (falling CO2) situation.
The four most important PFLs involve the action of CO2
on plant evolution and its feedback on rock weathering
rates, and sedimentary organic carbon burial (Fig. 3). In
the first PFL (Fig. 3B) a drop in the atmospheric CO2 concentration and a rise in stomatal density permits the evolution of larger leaves through the mechanisms discussed
earlier. Higher stomatal densities maximize CO2 diffusion
F I G . 4. Tropical weathering by deep-rooting trees on Kohala Mountain,
Hawaii. The image shows the weathering ‘halo’ around the roots caused by
mineral depletion. Depth of roots is approx. 7 m. Photograph courtesy of
Carl Bowser. Reprinted from Berner et al. (Treatise on Geochemistry 5,
p. 170; ª2003, with permission from Elsevier).
into the leaf under conditions favourable for photosynthesis,
and larger leaves capture more solar energy; both traits
promote primary production and leafier canopies (Beerling
and Berner, 2005). Higher densities are also associated with
smaller stomata that can open and close more rapidly helping to protect the xylem water pathway from cavitation and
allowing taller plants (Hetherington and Woodward, 2003).
Taller, leafier plants require deeper rooting systems and
more symbionts, including mycorrhizae, for uptake of
water and nutrients (Raven and Edwards, 2001). Deeper
roots and more abundant mycorrhizae increase nutrient
removal and the surface area of the soil–root interface,
accelerating the chemical weathering of silicates and further
enhancing the removal of CO2 from the atmosphere (Berner
et al., 2003).
In the second PFL, a similar chain of cause and effect
follows a drop in atmospheric CO2, but with larger more
productive plants enhancing organic carbon burial, both in
terrestrial wetlands and marine environments after transport
to the sea by rivers. Increasing organic carbon burial with
falling atmospheric CO2 reflects a major evolutionary trend
towards woody plants containing a high proportion of the
relatively non-biodegradable compound lignin (Berner,
2004). An expanding terrestrial biomass, promoting CO2
Beerling — Leaf Evolution: Gases, Genes and Geochemistry
removal from the atmosphere, is recorded as an enormous
increase in sedimentary organic carbon burial on land and
in the sea (Fig. 2D), most obviously manifested as
carboniferous coal deposits. Two further complementary
PFLs to those already described operate through the
direct action of CO2 on climate, via the greenhouse effect
(Fig. 3D and E).
The strengthening of this suite of PFLs during the late
Palaeozoic evolution of the terrestrial flora, especially
rooted forests, strongly amplified the extent and rate of
both silicate weathering and sedimentary organic carbon
burial. It was by way of these geochemical effects that
plants brought about the precipitous decline in atmospheric
CO2 that led ultimately to the Permo-Carboniferous glaciation (Berner, 2004; Beerling and Berner, 2005). The accelerated removal of CO2 from the atmosphere was only
stabilized by the negative CO2-climate feedback loop of
the inorganic carbon cycle (Fig. 3A), as the climate cooled
and decelerated rates of silicate weathering.
In the long term, plants brought about a gradual and
continual alteration of the global environment that modified
selection pressures on subsequent generations, effectively
facilitating their own evolution through the process of niche
construction (Odling-Smee et al., 2003). Moreover, plant
activities appear to have caused rates of evolution in terrestrial animals to accelerate. Late Palaeozoic insect and
tetrapod faunas diversified together with terrestrial plants,
and enhanced burial of organic carbon raised global oxygen
levels (Berner, 2004), fuelling a spectacular radiation of
insect gigantism (Graham et al., 1995).
CONCLUSIONS
Establishing a framework for understanding the origin and
diversification of leaves in the Palaeozoic requires information from a broad range of disciplines that include palaeontology, plant physiology, geochemistry and molecular
developmental genetics. Progress in many of these fields
of research has seen such a framework begin to emerge
and suggests that the exceptionally long 40- to 50-Myr
delay in the advent of large megaphylls was a product of
environmental opportunity and genetic potential. Once the
morphogenetic potential of plants was released by falling
atmospheric CO2 concentrations, leaf evolution entrained
global consequences not only for the regulation of CO2
and climate but also for terrestrial organisms. Plants themselves effectively policed their own evolution through their
influence on the silicate-rock-weathering–CO2-climate
feedback cycle.
ACKNOWLEDGEMENTS
I thank Robert Berner, Ben Fletcher and Colin Osborne for
comments on the manuscript, Andrew Fleming for discussions on the evolutionary developmental biology of leaves,
Carl Bowser (University of Wisconsin) for permission to
reproduce his photograph in Fig. 4 and Elizabeth and Robert
Berner for drawing it to my attention. I am indebted to Bill
351
Chaloner for many stimulating discussions on the evolution
of megaphylls.
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