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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 FORUM 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 % $ 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. Tansleys – in-depth reviews from a personal perspective The New Phytologist ‘ Tansleys ’ are commissioned in-depth reviews written from a personal perspective by leading international researchers in plant science. These reflect our commitment to easy communication and discussion, an ethos established when this journal was founded, by Sir Arthur Tansley, some 100 years ago. Tansleys are always peer-reviewed. If there are particular subjects which you feel should be covered, or if you are interested in the possibility of writing a Tansley review, get in touch with the Editor, Alistair Hetherington (a.hetherington!lancaster.ac.uk), or let us know at Central Office (newphytol!lancaster.ac.uk) or the USA Office (newphytol!ornl.gov). 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. FORUM 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). Bolan NS. 1991. A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant and Soil 134 : 189–207. Brundrett M. 1991. Mycorrhizas in natural ecosystems. Advances in Ecological Research 21 : 171–313. 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