Download Mosses and alternative adaptation to life on land

FORUM
New Phytol. (2000), 148, 1–6
Commentary
Mosses and
alternative
adaptation to life on
land
It is easy to dismiss bryophytes as ‘ lower ’ plants, mere
primitive precursors long since left behind in the evolutionary race, and of only rather esoteric and incidental
biological interest. But this is to let oneself be led astray by
a simplistic image of a tidy evolutionary tree – an image
that served Darwin well a century and a half ago (Desmond
& Moore, 1992), but which we should now see as an
intricately branched evolutionary bush with innumerable
shoots reaching out from all depths to the growing apices
that represent the present day. The earliest land plants
may indeed have been at a bryophyte level of organization,
but modern bryophytes, no less than vascular plants, are
the product of some 450 million years ’ evolution since that
time (Edwards et al., 1998). Raven (1977, 1984) has
emphasized the importance of the evolution of supracellular transport systems in the origin of vascular land
plants. Bryophytes, on the other hand, evolved desiccation
tolerance and represent an alternative strategy of adaptation to life on land, photosynthesizing and growing
when water is available, and suspending metabolism when
it is not. They are limited by their mode of life, but also
liberated : they are prominent on hard substrates such as
rock and bark, which are impenetrable to roots and
untenable to vascular plants. Bryophytes (in species
numbers the second biggest group of green land plants)
may be seen as the mobile phones, notebook computers
and diverse other rechargeable battery-powered devices of
the plant world – not direct competitors for their mainsbased equivalents, but a lively and sophisticated complement to them.
have long been hypothesized (Proctor, 1979, 1990 ; Proctor
& Smith, 1994), but experimental test of many of the
details has been lacking.
A basic assumption is that water stored in the cushion
prolongs the time available for photosynthesis as the moss
dries out after rain. Because water storage relates to
the volume and evaporation to the surface area, large
cushions should have an advantage in this respect. Further
than this, Zotz et al. demonstrate the relatively greater rate
of evaporation resulting from the thinner boundary layer
of smaller Grimmia cushions. It becomes clear why
colonization of rock (or bark) surfaces from spores by small
cushion-forming mosses must take place during long,
more-or-less continuous moist periods – autumn and
winter in western Europe and the wet season at whatever
time of year it occurs in other climates. It also underlines
why mature cushions of such mosses can survive when
transplanted outside the range in which they would occur
naturally (Alpert, 1988). The early stages of growth are
thus vulnerable, and critical for establishment of a smallcushion moss dependent on intermittent moisture.
Zotz et al. emphasize the importance of taking scale into
consideration in making ecophysiological comparisons.
This cannot be stressed too highly, not only within the
range of scales with which they are immediately concerned,
but over the wider range of scales that separate bryophytes
and vascular plants. Some common assumptions of
vascular-plant biology are simply irrelevant at the physical
scale of bryophytes. Bryophyte leaves are not functionally
comparable to vascular-plant leaves (though Marchantia
thalli in many respects are). A bryophyte leafy canopy lies
midway in scale between a vascular-plant canopy and a
vascular-plant mesophyll. Analogies may be sought in
both directions, and those analogies may equally be useful
or misleading. What is important is to go back to physical
and cell-biological first principles at whatever scale is
appropriate. Even in vascular plants, water loss in the field
may often be determined more by micrometeorology than
by stomatal control (Jarvis & McNaughton, 1986). Bryophytes are not simply potential vascular plants that have
not yet got round to evolving stomata ; they represent a
radically different way of doing things. We do not try to tie
insect physiology to a Procrustean bed built around what
we know of mammals. Both work, but they work
differently, each at its own scale.
‘ Bryophytes represent a radically
different way of doing things.’
Ectohydry and drying–rewetting
cycles
Surviving without water
The paper by Zotz et al. (pp. 59–67 in this issue)
provides a welcome experimental analysis of some important aspects of the alternative pattern of adaptation to
land life that desiccation-tolerant bryophytes represent.
Grimmia pulvinata is a common moss in and around our
town and cities, where its small hoary cushions are often
prominent on the tops of walls. General features of the
mode of life of this and other desiccation-tolerant mosses
Two particular points emerge from this study of G.
pulvinata. First, it emphasizes that this moss, like other
desiccation-tolerant mosses, is ‘ ectohydric ’ in its water
storage and movement. Most of the water associated with
the plant is extracellular, and can vary within wide limits
without affecting the water status of the cells (Dilks &
Proctor, 1979 ; Proctor et al., 1998). Ectohydry leads to
conflict between water storage and gas exchange, nicely
illustrated in the gas-exchange data presented by Zotz et
al. for G. pulvinata, which show a broad optimum for net
photosynthesis at water contents of about 200–400% DM
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2
Commentary
slowly than any of these (M. C. F. Proctor, unpublished
data). The general picture seems to be that in such species
as G. pulvinata and T. muralis, net photosynthesis returns
to a substantially normal rate within about 30–45 min of
remoistening, but that dark respiration takes considerably
longer to settle down to normal levels.
1
Fv /Fm
0.8
0.6
0.4
0.2
Racomitrium
lanuginosum
Tortula ruralis
0
1
Surviving without nutrients
Fv /Fm
0.8
0.6
0.4
0.2
0
1
Grimmia pulvinata
Pleurochaete
squarrosa
Ulota crispa
Anomodon
viticulosus
Fv /Fm
0.8
0.6
0.4
0.2
0
1
–400 –300 –200 –100 0
Water potential (MPa)
Fv /Fm
0.8
0.6
20 min after re-wetting
0.4
0.2
24 h after re-wetting
Porella platyphylla
0
–400 –300 –200 –100 0
Water potential (MPa)
Fig. 1. The chlorophyll-fluorescence parameter Fv\Fm
measured 20 min and 24 h after remoistening, following
desiccation for 15 d at four different water potentials. The
unstressed value of Fv\Fm is typically approx. 0n8. Note
the rapid recovery of Grimmia pulvinata and Tortula
ruralis, hardly affected by the intensity of the preceding
desiccation. The other species all recover somewhat more
slowly, and show greater effects of desiccation intensity, at
least on initial recovery. G. pulvinata still showed good and
relatively fast recovery after 60 d desiccation (Proctor,
2000).
(dry mass), falling to about half the maximum at 600–800%
DM. Such oversaturation probably persists less often
under natural conditions than in a laboratory cuvette ;
bryophytes often appear well adapted to maintain clear leaf
area for gas exchange even at high water contents (Dilks &
Proctor, 1979). Probably too, for a plant like G. pulvinata,
maximizing photosynthesis is less important than maintaining a hold on a hard-won patch of substrate. Growing
bigger and heavier may only mean that you fall off sooner !
The second point is that adapting to intermittent
availability of water by desiccation tolerance presupposes
recovery of normal metabolism on remoistening quickly
enough to take useful advantage of wet periods as they
happen. The length and frequency of drying–rewetting
cycles will vary with habitat and season, and taking a broad
view of desiccation-tolerant plants it is clear that recovery
rates differ very widely between species (Tuba et al.,
1998). There is certainly much variation among bryophytes. Grimmia pulvinata and Tortula ruralis recover
more rapidly than Racomitrium lanuginosum, Pleurochaete
squarrosa, Porella platyphylla, Anomodon viticulosus or
Rhytidiadelphus loreus (Fig. 1 ; Csintalan et al., 1999 ;
Proctor & Smirnoff, 2000 ; Proctor, 2000), and Mnium
hornum and Polytrichum formosum appear to recover more
Two other papers should remind us that another bryophyte
genus, Sphagnum, is responsible for more fixed carbon on
the surface of the earth than perhaps any single genus of
vascular plants, and that its biology has more than trivial
implications for the C balance of the atmosphere (Clymo,
1998). Gunnarsson & Rydin (2000), in the previous issue
of New Phytologist (see pp. 527–537), reported negative
effects of added nitrogen (as NH NO ) on the growth of
%
$
Sphagnum at sites in southern and central Sweden differing
by a factor two in their atmospheric N deposition. This
underlines the efficiency of these ectohydric plants in
acquiring limiting nutrients from an extremely nutrientpoor environment. What significance should be attached to
the depression of growth by added N at the N-limited site
is perhaps an open question. Sphagnum species have
substantial inducible nitrate reductase activity (Press &
Lee, 1982 ; Woodin et al., 1985), and there is some
indication that even rather low concentrations of NH +
%
are inimical to them (Rudolph & Voigt, 1986). Be that as
it may, it is clear that the bog mosses are subsisting on
extremely low nutrient inputs, and that quite subtle shifts
in atmospheric deposition may have substantial effects on
the functioning of the extensive and important peatland
ecosystems of which they are a key component.
Surviving in a hazardous
environment
In another paper in the current issue (pp. 105–116),
Sundberg & Rydin show that Sphagnum can form a
significant spore bank with a half-life in the region of a
decade. This is contrary to currently accepted expectation,
that a persistent propagule bank is not generally found in
perennial species of stable habitats (During, 1997). But
perhaps Sphagnum is ‘ the exception that proves the rule ’.
Sphagnum largely makes its own habitat, and it is a habitat
liable to the hazards of erosion and fire. During points to
the ecological similarity with Calluna vulgaris, dominant
over large tracts of fire-prone moorland landscape, and
with a persistent seed bank. All perennials are not
necessarily similar in their population biology ; their
similarities and differences can illuminate important
aspects of the functioning of the ecosystems in which they
occur. Sphagnum protonemata are very rarely seen in the
field, but isoenzyme evidence suggests that establishment
of sphagna from spores cannot be an excessively rare
occurrence (Daniels, 1993). We know all too little of what
happens to spores between shedding and germination and
establishment of a new gametophyte. What is certain is
that consequences of chance events of dispersal and
establishment could be be greatly amplified by subsequent
growth and ecological interactions.
Conclusion
Bryophytes have much to offer plant science research.
Apart from being fascinating plants in their own right (and
sometimes a source of surprises), they can provide us with
simpler systems to work with than vascular plants
FORUM
Commentary
(avoiding such complications as stomata and diploidy) –
though that simplicity may need to be approached with a
certain critical caution. As a stimulus to lateral thinking
they can lead us to question facile assumptions we may
make from long familiarity with vascular plants, and get us
back to thinking physiological problems through from first
principles.
M. C. F. P
School of Biological Sciences, University of Exeter,
Hatherly Laboratories, Prince of Wales Road,
Exeter, EX4 4PS, UK
(tel j44 1392 263 263 ; fax j44 1392 263 700 ;
e-mail m.c.f.proctor!exeter.ac.uk).

Alpert P. 1988. Survival of a desiccation-tolerant moss, Grimmia
laevigata, beyond its observed microdistributional limits.
Journal of Bryology 15 : 219–227.
Clymo RS. 1998. Sphagnum, the peatland carbon economy, and
climatic change. In : Bates JW, Ashton NW and Duckett JG,
eds. Bryology for the twenty-first century. Leeds, UK : Maney
Publishing and British Bryological Society, pp. 361–368.
Csintalan Zs, Proctor MCF, Tuba Z. 1999. Chlorophyll
fluorescence during drying and rehydration in the mosses
Rhytidiadelphus loreus (Hedw.) Warnst., Anomodon viticulosus
(Hedw.) Hook. & Tayl. and Grimmia pulvinata (Hedw.) Sm.
Annals of Botany 84 : 235–244.
Daniels RE. 1993. Phenotypic and genotypic variation in
Sphagnum. Advances in Bryology 5 : 31–60.
Desmond A, Moore J. 1992. Darwin. London, UK : Penguin
Books.
Dilks TJK, Proctor MCF. 1979. Photosynthesis, respiration, and
water content in bryophytes. New Phytologist 82 : 97–114.
During HJ. 1997. Bryophyte diaspore banks. Advances in
Bryology 6 : 103–134.
Edwards D, Wellman CH, Axe L. 1998. The fossil record of
early land plants and interrelationships between primitive
embryophytes : too little and too late ? In : Bates JW, Ashton
NW and Duckett JG, eds. Bryology for the twenty-first century.
Leeds, UK : Maney Publishing and British Bryological Society,
pp. 15–43.
Gunnarsson U, Rydin H. 2000. Nitrogen fertilization reduces
Sphagnum production in bog communities. New Phytologist
147 : 527–537.
Jarvis PG, McNaughton KG. 1986. Stomatal control of
transpiration : scaling up from leaf to region. Advances in
Botanical Research 15 : 1–49.
3
Press MC, Lee JA. 1982. Nitrate reductase activity of Sphagnum
in the South Pennines. New Phytologist 92 : 487–494.
Proctor MCF. 1979. Structure and eco-physiological adaptation
in bryophytes. In : Clarke GCS and Duckett JG, eds. Bryophyte
systematics. London, UK : Academic Press, pp. 479–509.
Proctor MCF. 1990. The physiological basis of bryophyte
production. Botanical Journal of the Linnean Society 104 :
61–77.
Proctor MCF. 2000. Patterns of desiccation tolerance and
recovery in bryophytes. Plant Growth Regulation (In press).
Proctor MCF, Nagy Z, Csintalan Zs, Taka! cs Z. 1998. Watercontent components in bryophytes : analysis of pressure–volume
curves. Journal of Experimental Botany 49 : 1845–1854.
Proctor MCF, Smirnoff N. 2000. Rapid recovery of photosystems on re-wetting desiccation-tolerant mosses : chlorophyll
fluorescence and inhibitor experiments. Journal of Experimental
Botany (In press).
Proctor MCF, Smith AJE. 1994. Ecological and systematic
implications of branching patterns in bryophytes. In : Hoch PC
and Stephenson AG, eds. Experimental and molecular approaches to plant biosystematics. St Louis, MO, USA : Missouri
Botanical Garden, pp. 87–110.
Raven JA. 1977. The evolution of land plants in relation to
supracellular transport processes. Advances in Botanical Research 5 : 153–219.
Raven JA. 1984. Physiological correlates of the morphology of
early vascular plants. Botanical Journal of the Linnean Society
88 : 105–126.
Rudolph H, Voigt JU. 1986. Effects of NH -N and NO -N on
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growth and metabolism of Sphagnum magellanicum. Physiologia
Plantarum 66 : 339–343.
Sundberg S, Rydin H. 2000. Experimental evidence for a
persistent spore bank in Sphagnum. New Phytologist 148 :
105–116.
Tuba Z, Csintalan Zs, Proctor MCF. 1998. Photosynthetic
responses of a moss, Tortula ruralis ssp. ruralis, and the lichens
Cladonia convoluta and C. furcata to water deficit and short
periods of desiccation, and their ecophysiological significance :
a baseline study at present CO concentration. New Phytologist
#
133 : 353–361.
Tuba Z, Proctor MCF, Csintalan Zs. 1998. Ecophysiological
responses of homoichlorophyllous and poikilochlorophyllous
desiccation tolerant plants : a comparison and an ecological
perspective. Plant Growth Regulation 24 : 211–217.
Woodin SJ, Press MC, Lee JA. 1985. Nitrate reductase activity
in Sphagnum fuscum in relation to wet deposition of nitrate from
the atmosphere. New Phytologist 99 : 381–388.
Zotz G, Schweikert A, Jetz W, Westerman H. 2000. Water
relations and carbon gain are closely related to cushion size in
the moss Grimmia pulvinata. New Phytologist 148 : 59–67.
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4
FORUM
Commentary
Measuring the
influence of
mycorrhizas
‘ The view that nutrient acquisition by most plants growing
in natural ecosystems is mediated by mycorrhiza-forming
symbiotic fungi is now largely accepted ’ (Read, 2000). Is
this bold claim really true for the whole suite of mineral
nutrients that plants require ? The case is strongest for
nutrients that are not very mobile in soil, especially when
present in growth-limiting amounts, and phosphate (P) is
the classic example. Arbuscular mycorrhizas are by far the
most widespread mycorrhizal symbioses, and the ability of
arbuscular mycorrhizal (AM) fungi to take up soil
nutrients such as P and transfer them to the host plant is
an area of intense research. However, there is great
variation in the extent to which AM plants benefit in
measurable terms from the symbiosis under a given set of
environmental conditions, and a paper in this issue, by
Koide et al., addresses this problem (Koide et al., pp.
163–168). The variability is especially apparent in the
field, thus obscuring the possible roles of mycorrhizas in
community structure and succession (Fitter, 1985 ;
McGonigle, 1988).
demand and supply. Demand was defined as the optimum
rate of P uptake (i.e. the lowest rate of P uptake that would
give maximum plant performance). When external P is
low, plants with inherently high demand for P would be
expected to have high mycorrhizal responsiveness, unless
they have other mechanisms for overcoming the demand.
Taking for simplicity growth rate as the measure of
performance, the actual growth rate at any given time is
the product of P supply and P utilization efficiency (PUE),
where the latter term is growth per unit amount of
absorbed P (Koide, 1991). This relationship is formalized
in Eqn 1 (see Box 1). Growth increases by mycorrhizal
plants at a given time can occur when P supply is greater
than can be achieved by the comparable nonmycorrhizal
plant, but may be modified by changes in PUE at that
time. Koide (1991) discussed the implications of this
analysis in terms of root morphology and architecture (the
spatial configuration in soil) and also variability in PUE.
Because of ontogenetic changes, there is temporal variation
in the P required for maximal growth, so plant performance relates not only to the current growth rate but to
aspects of fitness that include the potential for maximum
reproduction (Koide, 1991). Apparent ‘ luxury ’ uptake at a
given time, resulting in low PUE, may relate to storage for
future needs. The time dimension is also very relevant to
rates and patterns of colonization and nutrient acquisition
by mycorrhizal fungi and their control by the host.
Efficiency of phosphate acquisition
‘ The analysis developed is a
great step forward in examining
quantitatively how mycorrhizal
plants influence the efficiency of
phosphate uptake ’
Mycorrhizal responsiveness : nutrient
demand and supply
Many factors help produce high ‘ mycorrhizal responsiveness ’ of the plant, which is usually defined in terms of
improved vegetative growth but is also definable in terms
of improved nutrition or reproductive capacity. Table 1
divides these factors into properties of the fungus, plant
(root) and interface(s) across which transfer of resources
occurs ; and ‘ structural ’ and ‘ physiological ’ factors. Low
mycorrhizal responsiveness will be produced by the
converse of the factors listed (e.g. for ‘ fast ’ or ‘ high ’ read
‘ slow ’ or ‘ low’). The list is not all-embracing and ignores,
for example, hyphal connections between mycorrhizal
plants and other ecological factors that can limit plant
growth, such as plant density, effects of pathogenic
organisms and grazing above- and below-ground (Fitter,
1985 ; Brundrett, 1991).
Mycorrhizal responsiveness is frequently considered in
relation to demand for nutrients by plants versus supply
from the soil, and benefits of the symbiosis versus costs.
Koide (1991) suggested that where P is the growthlimiting nutrient, the maximum extent to which mycorrhizal colonization can improve plant performance is a
function of P deficit, the difference between current P
Koide et al. (1999, 2000) have pointed out that the cost of
acquiring P can be measured in terms of any resource in
the plant, including P itself. They refer to the efficiency
with which internal P is used to acquire external P as the
P efficiency index (PEI) (i.e. (dP\dt)(1\P)). Accordingly,
the growth rate of the plant can be expressed in relation to
three factors : PEI, P content and PUE (Eqn 2 ; Box 1).
Koide et al. (1999) demonstrated the usefulness of PEI
by comparing a constitutively nonmycorrhizal plant, Beta
vulgaris (beet), with nonmycorrhizal and AM lettuce. The
PEI for AM lettuce was higher than for nonmycorrhizal
lettuce, and about the same as for beet. The increase
relates to the ability of the fungal hyphae in soil to supply
P to the plant without using the plant’s P. In this issue,
Koide et al. describe a more detailed study of beet, lettuce
and Abutilon theophrasti. Mycorrhizal colonization significantly increased the PEI and P content of lettuce and
Abutilon. Colonization had no significant effect on the
PUE of Abutilon, but decreased that of lettuce. Consequently, although colonization greatly increased the
growth rate of Abutilon, there was only a slight increase in
growth rate of lettuce – in that case the P concentration
(P\W) was higher than in the nonmycorrhizal lettuce.
Box 1. Growth rate equations
dW\dt l dP\dtidW\dP
Eqn 1
dW\dt l (dP\dt)(1\P)iPidW\dP
Eqn 2
(dW\dt)(1\W) l
(dP\dt)(1\RA)idW\dPiRA\W
Eqn 3
(dW\dt)(1\W) l
(dP\dt)(1\RA)idW\dPiRA\RWiRW\W Eqn 4
Abbreviations : W, weight ; P, phosphorus content ;
t, time ; RA, root surface area ; and RW, root weight.
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Commentary
5
Table 1. Factors that may increase mycorrhizal responsiveness of autotrophic plants
Fungus
Root
Interface(s)
External hyphae
Short length (low
root : shoot ratio)
Little branching
Large diameter
Few or short root
hairs
Selectively flexible
root : shoot ratioa
Inability to modify
rhizosphereb
Low nutrient influx
capacity
Fast organic C delivery
to interface(s)
Fast development
Large area of contact
High longevity
High organic C flux from
roots
High nutrient flux to roots
Fast colonization
High growth rate
High extension into soil
High nutrient influx capacity
High nutrient translocation
Internal hyphae
High growth rate
Fast nutrient delivery to
interface(s)
Factors in italics are ‘ physiological ’, relating to mechanisms of resource acquisition and transfer.
a Inflexible in response to low soil nutrient levels, not to mycorrhizal colonization.
b Inability to modify rhizosphere to increase nutrient availability.
Taking growth analysis below ground
Although Eqns 1 and 2 suggests very useful ways of
analyzing how different combinations of plants and
mycorrhizal (not just AM) fungi respond to colonization in
terms of growth and P content, they do not focus directly
on the structural or physiological bases for the responses.
For example, their terms do not help explain why some
AM plants (e.g. lettuce) have lower PUE and so develop
high P concentrations compared with nonmycorrhizal
controls. The analytical approach can be extended further
in ways that may be helpful in this respect. Despite the
preference of Koide (1991) to consider P supply and
demand in terms of absolute growth rate (dW\dt), it seems
better to use as the basis relative growth rate (RGR) (i.e.
(dW\dt)(1\W )), which is the basis of conventional growth
analysis (e.g. Lambers & Poorter, 1992). Eqns 1 and 2 can
easily be converted to this basis. Eqn 3 (Box 1) relates
RGR to P influx, PUE and ‘ root area ratio ’ (RAR). To
avoid any implication that P influx is uniform across a
whole root system, it should be regarded as an average
value per unit surface area.
Root area ratio (RA\W) is the product of the specific root
area (SRA : RA\RW) and root weight ratio (RWR : RW\W).
Accordingly, Eqn 3 can be expanded to give Eqn 4 (Box 1).
Eqns 3 and 4 are essentially expansions of Eqn 1, based on
RGR and with root parameters added. They can easily be
converted to a basis of absolute growth rate by deleting W
throughout. They can also be based on root length and
hence use P inflow (rate of P uptake per unit root length).
Similar equations could of course be used for nutrients
other than P.
This more extended growth analysis focuses directly on
some of the factors in Table 1. In order to consider
mycorrhizal responsiveness in these terms, it is helpful
first to summarize strategies available to nonmycorrhizal
plants when growing in soils low in P. Such plants might
be constitutively nonmycorrhizal or potentially mycorrhizal ones growing in the absence of fungal inoculum.
Given that PUE is likely to be maximal in low-P soils
(where there is no ‘ luxury ’ uptake), Eqn 4 shows that as
soil P is further depleted, the plant might be able to sustain
a high RGR via increases in P influx, specific root area
(SRA) or root weight ratio (RWR), or some combination
of these. High P influx could involve – using membrane
transport jargon – increasing Vmax or decreasing Km of the
membrane transporter(s) for P. This might involve
increased activity of transporters via feedback regulation
of influx or changes in expression of transport-related
genes, or both (Schachtman et al., 1998). In fact, these
‘ physiological ’ strategies alone may not be very successful
where there is significant depletion of P in the rhizosphere
adjacent to the transport sites (e.g. Silberbush & Barber,
1983, 1984). However, the plant might also increase P
influx by increasing P availability at the root surface by
solubilizing P (e.g. by releasing organic acid). This
increases the P concentration for membrane transport and
is a strategy adopted by some constitutively nonmycorrhizal plants. The alternative strategy for nonmycorrhizal
plants in low-P soils is structural (increasing SRA and
RWR). High SRA involves thin roots and\or extensive
formation of root hairs. High RWR is expressed more
conventionally as high root : shoot ratio. Some plants are
more plastic in these respects than others. The problem
associated with large root biomass is that if it is achieved at
the expense of photosynthetic shoot biomass there may be
no advantage in terms of increased growth.
Mycorrhizal plants show combined structural and
physiological strategies that can help the plant meet P
demand. These can be considered in terms of Eqn 4. Even
if there is no increase in RGR, P influx at a given time may
be higher, resulting in higher P concentration (lower
current PUE). The extensive external hyphae produce a
very large absorbing surface for a given mass of root,
equivalent to a very high SRA. There is no evidence that
P transporters on mycorrhizal fungi have especially high
affinity for P (low Km). However, nutrient depletion
throughout the extensive ‘ mycorrhizosphere ’ will be less
dramatic, so that P concentrations for uptake will be more
adequate than in the much smaller rhizosphere around a
nonmycorrhizal root (Li et al., 1991 ; Schweiger &
Jakobsen, 1999). It is still uncertain as to whether AM
plants in general can acquire P from sources unavailable to
nonmycorrhizal plants of the same species (Bolan, 1991 ;
Li et al., 1991), but this is potentially another way of
increasing P influx. Sometimes, RWR of plants is
decreased by mycorrhizal colonization, but much of the
carbon saved is used as the fungal biomass that supplies P
to the plant. Mycorrhizal colonization is often (though not
always) decreased when external P levels are high. This
means that the plant can save carbon costs and possibly
6
FORUM
Commentary
further decrease RWR when its roots can meet the demand
for scarce nutrients.
Eqn 4 is relevant to differences in inherent growth rates
in plants that are discussed with respect to mineral
nutrition by Lambers & Poorter (1992). It is sometimes
proposed that slow-growers might have low mycorrhizal
responsiveness in low-P soils because they have relatively
low demand for P (Koide, 1991). However, it seems
equally plausible that slow-growers might have high
responsiveness because of the formation of P-depletion
zones around their slow-growing roots (when nonmycorrhizal). This second possibility refers to supply of P.
In fact, there appears to be no simple relationship between
inherent growth rates and mycorrhizal responsiveness.
This should not be surprising, given that responsiveness
will depend on the differential effects and interactions of
all the terms in Eqn 4 as they relate to nutrient demand
versus supply in nonmycorrhizal and mycorrhizal conditions.
Among the problems in analyzing growth below ground
are practical difficulties of measuring the details of root
morphology, especially root hairs and their dimensions.
Root architecture (e.g. branching patterns) should also be
taken into account (Hetrick, 1991 ; Lynch, 1995). As it
stands, Eqn 4 is entirely plant-oriented but can be modified
to introduce fungal parameters, including length or density
of external hyphae per unit root length, and areas of
symbiotic interfaces (arbuscules and hyphae). If emphasis
is to be placed on costs in terms of drain of organic C (see
Johnson et al., 1997), extent of fungal structures within
and outside the root certainly should be measured and
metabolic activity estimated. In other words, there is a
need for fungal growth analysis to mirror belowground
plant growth analysis.
Summary
The analysis developed by Koide and associates is a great
step forward in examining quantitatively how mycorrhizal
plants influence the efficiency of uptake of P, and indeed
other nutrients, without going into details of belowground
processes. It also has strong implications for understanding
the complex issues of how formation of mycorrhizas
influences community structure via competition between
plants for growth-limiting nutrients. Where an additional
aim is to identify structural and physiological traits of
roots that are involved in nutrient absorption, such as
those summarized in Table 1, the more extensive analysis
may also be useful, if it is possible for practical reasons.
The analysis is also compatible with attempts to quantify
P uptake kinetics of nonmycorrhizal and AM plants
(Schweiger & Jakobsen, 1999), and will help combine
research into structural aspects of root systems with
molecular mechanisms of P transport (Schachtman et al.,
1998 ; Smith et al., 1999).
F. A S
Department of Environmental Biology and Centre for
Plant Root Symbioses, The University of Adelaide,
SA 5005, Australia
(tel j61 8 83034695 ; fax j61 8 83036222 ;
e-mail andrew.smith!adelaide.edu.au).

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