Roles of Arbuscular Mycorrhizas in Plant Phosphorus Nutrition: Interactions between Pathways of Phosphorus Uptake in Arbuscular Mycorrhizal Roots Have Important Implications for Understanding and Manipulating Plant Phosphorus Acquisition
Year: 2011
Type: review
Abstract: In this Update, we review new findings about the roles of the arbuscular mycorrhizas (mycorrhiza = fungus plus root) in plant growth and phosphorus (P) nutrition. We focus particularly on the function of arbuscular mycorrhizal (AM) symbioses with different outcomes for plant growth (from positive to negative) and especially on the interplay between direct P uptake via root epidermis (including root hairs when present) and uptake via the AM fungal pathway. The results are highly relevant to many aspects of AM symbiosis, ranging from signaling involved in the development of colonization and the regulation of P acquisition to the roles of AM fungi in determining the composition of natural plant assemblages in ecological settings and their changes with time. P is critical for plant growth and makes up about 0.2% of dry weight, but it is one of the most difficult nutrients for plants to acquire. In soil, it may be present in relatively large amounts, but much of it is poorly available because of the very low solubility of phosphates of iron, aluminum, and calcium, leading to soil solution concentrations of 10 μm or less and very low mobility (Schachtman et al., 1998). In consequence, uptake of orthophosphate (Pi) by root epidermal cells including root hairs (the direct pathway) leads to lowering of Pi concentrations in the rhizosphere (so-called depletion zones), because replacement does not keep pace with uptake (Fig. 1). Plants and fungi take up P as negatively charged Pi ions (H2PO4 −), which poses additional problems, because the concentration in cells is about 1,000-fold higher than in the soil solution and the cell membrane has an inside-negative electric potential. Pi uptake, therefore, requires metabolic energy and involves high-affinity transporter proteins in the Pht1 family (Bucher, 2007). Accordingly, plants have evolved a range of strategies that increase either Pi uptake capacity or availability of Pi in soil (Marschner, 1995). The most common of these strategies worldwide is AM symbiosis. Scattered through the plant kingdom are other strategies that enhance Pi availability or uptake, such as the formation of dense “cluster roots” that produce organic anions that release Pi from poorly available inorganic forms, but these are much less common (Cheng et al., 2011; Lambers et al., 2011). In many cases, it appears that cluster root formation may be an alternative strategy to AM formation, as in most Proteaceae and also white lupin (Lupinus albus), but some plants, such as Casuarina, develop both cluster roots and AM (Lambers et al., 2008). The two pathways of P uptake in an AM root involve different regions of the root, different cell types, and different Pi transporters. In the direct pathway (DP), Pi is absorbed from the rhizosphere by plant Pi transporters in epidermis and root hairs (green circles) close to the root surface. Uptake is normally faster than replacement by diffusion from the bulk soil, resulting in reduced Pi concentrations (depletion) close to the roots (callout 1). In the mycorrhizal pathway, Pi is taken up into AM fungal hyphae by fungal Pi transporters (blue circles) several centimeters from the root and translocated to intracellular fungal structures (arbuscules and hyphal coils) in root cortical cells (callout 2). Plant Pi transporters, induced in colonized cells (yellow circle), transfer Pi from the interfacial apoplast to plant cortical cells (callout 3). The majority (probably 70%–80%) of terrestrial plant species are capable of interacting with AM fungi in nature, and the activities of AM fungi and plant roots are closely integrated as a result of coevolution over at least 450 million years (Smith and Read, 2008). The major advantage of the AM symbiosis for plants in acquiring P is that AM fungi provide a very effective pathway (the AM pathway) by which P is scavenged from large volumes of soil and rapidly delivered to cortical cells within the root, bypassing direct uptake. The AM pathway can reduce the impact of Pi depletion in the rhizosphere and so improve plant P nutrition and growth (Fig. 1). The extent to which an AM plant grows better than a nonmycorrhizal (NM) counterpart (as in a pot experiment) depends in part on the size of its root system, including numbers and extent of root hairs. In general, plants with low root-shoot biomass ratios, slow root growth rates, and/or poor development of root hairs show relatively larger growth increases when AM. Conversely, growth differences between AM and NM plants tend to disappear as available soil P is increased, because of lower P depletion in rhizospheres (Smith and Read, 2008). Nevertheless, growth increases of AM plants over NM counterparts are maintained if high total soil P is poorly available (Bolan, 1991). Recent physiological and molecular research has revealed clearly that the AM pathway plays a major role in P uptake, regardless of the extent to which an AM plant benefits in terms of increased growth or P uptake. At the same time, plants provide all the organic carbon (C) requirements of the fungi, so that AM symbioses are mutualistic, based on an exchange of plant C for soil P and other nutrients that we do not consider here, including nitrogen (Smith and Read, 2008; Smith and Smith, 2011). Use of C by AM fungi can be offset at least partly by higher rates of photosynthesis and/or savings in C costs of root production in AM plants (lower root-shoot ratios than NM counterparts). Furthermore, costs of the AM fungi will not be deleterious if plant growth is not C limited. In the context of P nutrition, AM symbioses should not be regarded (as they sometimes are) as optional strategies that are “implemented” by plants when soil P supplies are low and are ineffective or even eliminated when P supplies are high. For plants capable of forming AM, the NM condition is nearly always “unnatural.” In other words, it is an artifact of growth in sterilized soil as in experiments or in horticulture or agriculture if soil is fumigated. The NM state can be regarded as “natural” only where potentially AM plants can survive and reproduce in soils lacking AM fungi or in nonhost species (such as members of the Brassicaceae) that never become mycorrhizal. High-P fertilizer application can greatly lower the percentage of root length colonized. The lower percentage of root length colonized at high P availability does not necessarily imply plant suppression or control of fungal activity, because high P increases root growth and hence reduces the ratio of colonized to noncolonized root length; there may be no effects of P on the fungus per se (Smith et al., 1992; Marschner, 1995). However, very high P application can certainly alter characteristics of root colonization (particularly reducing arbuscule development) and markedly decrease AM fungal biomass per plant, including both biomass in roots and in soil (Smith and Read, 2008). Bruce et al. (1994) showed that early (up to 15 d) reduction in colonization in cucumber (Cucumis sativus) with additional P was mediated by slower growth of fungal infection units within roots, but later there was also a reduction in the rate of formation of new entry points. The latter observation has been significantly extended by Balzergue et al. (2011), who showed marked reductions in appressorium formation on pea (Pisum sativum) roots at high P (750 μm; i.e. about 2 orders of magnitude higher than soil solution), which, importantly, was mediated by internal plant-derived signals. Agronomic practices may lower inoculum in soil and subsequent colonization as a result of frequent use of P fertilizer, long fallow periods, cultivation of nonhost crops (especially members of the Brassicaceae), or frequent soil tillage that disrupts networks of AM fungal hyphae in soil (Jansa et al., 2006). Alteration of the mycorrhizal status of a plant (by soil sterilization) from the AM condition, receiving P via both the direct and AM pathways, to an unnatural NM condition, receiving P only via the direct pathway, may induce physiological changes that can be classed as stress responses. Much of the research reviewed here has been done since the acceptance that plant responses to AM colonization vary from highly positive to negative (Johnson et al., 1997; Smith and Smith, 2011). Previously, it was assumed that responses should normally be positive (or zero), resulting in the neglect of mechanisms underlying the negative responses (or “growth depressions”). The use of plants that can grow better when AM symbiosis is eliminated (i.e. that show conventional AM growth depressions) is revealing unexpected aspects of the integration of plant and fungal processes. These plants include not only wild species but crops such as wheat (Triticum aestivum), barley (Hordeum vulgare), upland rice (Oryza sativa), and tomato (Solanum lycopersicum), and the findings have important consequences for understanding and potentially improving P uptake efficiency in agricultural systems. Plants that develop AM symbioses can in most cases be colonized by AM fungi from different In other words, there to be very in the symbiosis. However, plant species can have for AM fungi, resulting in different of and in some cases colonization can be very low (Smith et al., These effects have been with fungi from and with plants that show positive growth responses. The in extent of colonization by different fungi is also to natural where the may have over or in agricultural where AM fungi may have been by by different AM fungi does not result in the same growth responses in a AM plant species et al., Smith et al., and colonization by the same AM fungus does not necessarily result in the same growth responses in different plant species (or even of responses was with plants and AM fungi from the same In this the growth responses in plant species from positive to is therefore, that there is fungal symbioses in terms of benefits to the plant, in this and costs to the plants in the will be colonized by many AM fungal and the total of benefits and costs to in terms of growth and The outcomes of the symbioses are by between plant and AM fungal as as soil and P The two pathways by which AM plants P involve different cell types, different Pi transporters, and P from different regions and volumes of soil (Fig. 1). uptake, by root including root hairs when they are Pi in the soil solution close to the of high-affinity Pi transporters in these cells is in the root and root hairs et al., and in is reduced with high P and by AM colonization et al., 2007). These reductions will to lower direct uptake in regions of the root, but their is not AM and hence the of the AM pathway, the root AM fungi grow in soil to a hyphal that Pi fungal high-affinity from up to several centimeters from the root and can markedly the depletion (Fig. 1). P is translocated rapidly to the roots (probably as the slow diffusion that in the soil The fungal hyphae have much than roots, to soil and hence the soil et al., Smith and Read, 2008; et al., 2011). These are the major of increased P uptake and positive AM growth responses. AM develop within root cortical with fungal structures as and also with hyphae (Smith and Read, 2008). These structures are by the plant so that the are by of plant and fungus with an between is important with to the control of between the (Smith and Smith, of Pi release from fungus to the interfacial apoplast are but uptake into the plant is plant which are different from in the direct pathway, are sometimes in the colonized cortical cells (Bucher, et al., 2007). These are involved in the uptake of Pi by the fungi and have been to in all potentially AM plants regardless of their to AM fungal the plant membrane the intracellular fungal Pi uptake (Smith and Read, 2008). The direct and AM pathways are potentially and it to be assumed that direct uptake a to total plant P uptake, with the AM pathway an in plants that to colonization (Smith and Smith, 2011). a of molecular and physiological that this is and that there is a interplay that results in highly of the two The of and and their subsequent exchange with soil P the of hyphal Pi uptake via the AM pathway from a soil P is with soil in a by a to which of hyphae but not roots, P uptake from that hyphal can be as where is the (i.e. available P per soil The relatively to the of a P and and this with the for the of AM fungal in soil the of AM These of the of the AM pathway to total plant P uptake and hence (by also the of direct uptake (Smith et al., of AM and direct uptake can also be where one P is to an and the other is to a to both hyphae and roots and have that uptake via the AM pathway does and may total P uptake, even in plants that do not grow better when colonized by AM the of the AM pathway can be they be from the total P of AM and NM plants the same The of the direct pathway in AM plants be by of the plant in root epidermis plus root hairs via the of AM fungi or via increased plant P and/or by for P between roots and hyphae in the depletion the root et al., 2008). will be in AM root is one in which direct and AM pathways potentially at the same but not necessarily in the same regions of the root or to the same The direct pathway will be most effective the where the root epidermis (including root with high-affinity grows into direct uptake certainly to reduced of in the of root and depletion of Pi in the However, the AM pathway will into and rapidly to plant P uptake (Fig. 1). The aspects of this in of the pathways is by a that showed that P P into a root be higher than that into AM fungal hyphae for a only and that hyphal pathway) root by of magnitude et al., 2011). of P via AM and direct pathways, Pi also show that the two pathways to plant P uptake even in the same because different AM fungi different of the same AM fungus does not the same of total P to different plant species et al., Smith et al., The AM with soil P as direct uptake increases et al., this is with a percentage of root length colonized. The that and tomato can a large of total P as P uptake via the AM pathway, even they do not take up total P when AM, that the of direct uptake be lower than in NM In an the direct pathway was in tomato when colonized by the AM fungus (Smith et al., have higher of in the direct pathway in NM with AM plants, which was not necessarily with lower plant P status and hence a et al., 2007). We that may be part of a of also including increased root-shoot ratio and length of root hairs (Marschner, which are if a normally AM plant is from forming mycorrhizas at low has also been that if lower direct uptake is not by a large of the AM pathway, the plants will become P one for the reduced growth of AM plants, especially when growth in plants with very low colonization et al., low colonization will result in very low P uptake via the AM pathway (Smith et al., is also some for low of direct uptake in plants that to AM. can be for by from Smith et al. to new of of P taken up by the direct pathway in AM are about and P root dry with the two fungi with about P root dry for the NM However, in AM also direct P uptake was only by one of the two AM The include the P by the direct pathway is mediated by reduced of in the direct pathway and/or by for uptake of Pi between direct and AM The latter certainly at high root and hyphal length in soil et al., and is an for the of positive mycorrhizal growth responses. However, to have impact at low length plant growth and percentage of reduced is this and by signaling pathways are to be between and the of a AM symbiosis involve the exchange of many and the molecular of early in the symbiosis that are with the symbiosis et al., However, are for the AM fungal or this is an of it is the of this of relevant to P nutrition include the et al., 2007). The underlying signaling for of is but has been as a for the of in (Solanum and tomato et al., 2007). all of the so on signaling involved in responses has been in AM nonhost particularly and also white lupin (Cheng et al., 2011). plants are to have evolved from AM AM other symbioses as a strategy to enhance the acquisition of but they only about of terrestrial plants (Smith and Read, 2008). The of AM P uptake potentially result in a higher of P and marked of responses when in to be in when from to responses of normally AM to responses in AM species in the and of AM fungal is In the AM nonhost and regulation of involved in the direct pathway are by a of signaling in to Pi low with to and responses et al., and 2011; et al., 2011). Pi a range of is induced by the the in the of most Pi in nonhost The is induced by and negatively the that normally the of of in plants leads to of and to a increase in Pi uptake via the direct pathway. The pathway is by including et al., of the signaling pathway are in plants that can become AM. have been in of several where one of the is is an and both are for of the et al., 2011). The for the in is to signaling and the of of in the AM pathway high Pi in AM plants with to colonization et al., 2011). of in AM roots with low of et al., The that be low to AM symbiosis, a high root P status in AM plants (Fig. 2). between signaling and AM signaling can also be in the AM and NM In is induced by AM colonization is induced both at high P and by AM colonization et al., The function of these is at but their a role in Pi signaling and interplay between direct and AM In a Pi et al., and to are rapidly in the AM symbiosis and 1998). the for these increase the understanding of the interplay between direct and AM signaling in AM roots based on of Pi in nonmycorrhizal plants and in AM In NM plants, low P increases the of the which to the in of several Pi and increases their also increases the of are in where they in AM than in NM plants (callout this the transfer of from root to in AM plants (callout 2). are from to in roots is by and by from (callout 3). low P reduce the of the by and hence increase including increased of (callout of in reducing can be by such as (callout responses and reduce the of from et al. a role in both through in root development and in signaling et al., In roots, are by and as as are in and are in root and root which is by Pi et al., as as by AM has been to in with to root development and in on the Pi in the growth et al., 2011). also as early between the in AM by plant roots, they induce of hyphae from AM fungal et al., and a role in arbuscule formation in cortical cells et al., with for the of the AM pathway. Furthermore, lower in plants is as one to reduced numbers of fungal and lower colonization at high P et al., 2011). involved in and the development of AM colonization to an additional role in root production et al., 2011). these and with P nutrition has not been responses in plants are also with is the translocated between and root via the and a high root-shoot ratio of is for responses as as some such as and 2008; et al., 2011). in it has been that is a of a of responses et al., 2011). of to the root can induce some and high are for in roots at the of Pi in common which is a potentially AM plant but was not colonized in this research et al., In AM plants, to roots is this changes in the root-shoot ratio of and the outcomes of the signaling In there are many between AM symbiosis and signaling pathways that are with and a for between the direct and AM pathways, but for such have not been that the AM pathway plays a role in plant P uptake and that the of direct uptake may be reduced over the range of plant growth and P uptake responses to be in many here, we present some The of AM plant responses (Johnson et al., which has very be The was based on the to be in that a of positive mycorrhizal growth was by costs of the symbiosis benefits (i.e. at least of the of P via the AM pathway) with high fungal C use The fungi can no be regarded as because the AM pathway P in with regardless of the plant of their normally than status should on the function of AM symbioses and their (Smith and Smith, 2011). fungal C use with a of P as the of AM growth should also be because reduced growth may with very low AM fungal biomass et al., Smith et al., We have an alternative in which poor growth of AM plants is the result of a reduction in P via the direct pathway, which is not for by uptake via the AM pathway, leading to reduced total plant P uptake and P (Smith et al., Smith and Smith, 2011). has up new the interplay between fungal and plant at the of signaling and molecular control as as in for in experiments have new on the of the of the AM pathway in plant it was that AM plants a advantage over plants when they with an AM fungal even they biomass when regardless of with AM fungi et al., et al. in a hyphal to show that P uptake from soil and via the AM pathway by the AM tomato to P uptake by the reductions in direct uptake in the uptake to a positive growth in which was not when the These results that AM symbioses may have ecological benefits that be from AM growth responses for plants in with AM fungal of the interplay between the AM and direct uptake pathways is by the effects of AM colonization on uptake by and Pi are taken up by the same plant in the direct pathway, so that reduced uptake capacity of the direct pathway as as Pi uptake. that the AM pathway to plants, so the of these two effects to ratios and increased of AM with NM plants et al., effects that are for crops on soils with The of different of P present in soils on the availability and uptake of P from natural and fertilizer the of research et al., 2011). is that AM and NM plants the same of inorganic soil including P that is to soil and with the soil solution (Marschner, et al., 2011). AM plants can total P than NM plants from the same soil, which is to involve increased by hyphae in soil (Marschner, 1995). The for P in soil between AM fungal hyphae and roots has been as a for reduced uptake via the direct pathway, but it is to in where plants are poorly colonized and root and hyphal length are mycorrhizal growth responses can increase if poorly available P is to soil, even for plants that show or no positive at low that AM plants can poorly available P than NM plants, but the mechanisms by which they do so are not (Bolan, 1991). is some that AM fungi can of organic P in but the of this to the of P to plants is et al., of poorly available soil P by AM plants is important in the of understanding AM and the of fertilizer these if we are to the plant to P uptake. are a on which in of fertilizer is and availability is to and in a where production will be critical et al., The majority of terrestrial plant including are normally AM in and a strategy that has plant and on soils for many of the involved in AM function the development of crops with The to is to the that in AM plants and not to on that are to be on the of and interplay between the two pathways of P uptake in AM plants and by a of plant physiological and molecular has up new on AM including the potentially deleterious reductions in P via the direct pathway and hence the of to increase agricultural plant We to we not to
Source: PLANT PHYSIOLOGY
Institutions: The University of Adelaide, Technical University of Denmark
Language: English
Subfield: Plant Science
Domain: Life Sciences
SDG: Zero hunger
Open Access status: green
OpenAlex ID: W1966364875