F. Andrew Smith

Mycorrhizal Fungi Can Dominate Phosphate Supply to Plants Irrespective of Growth Responses

Arbuscular mycorrhizal (AM) fungi are vital components of nearly all terrestrial ecosystems, forming mutually beneficial (mutualistic) symbioses with the roots of around 80% of vascular plants and often increasing phosphate (P) uptake and growth. We present novel data showing that AM fungi can

Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales.

Root systems of most land plants form arbuscular mycorrhizal (AM) symbioses in the field, and these contribute to nutrient uptake. AM roots have two pathways for nutrient absorption, directly through the root epidermis and root hairs and via AM fungal hyphae into root cortical cells, where arbuscules or hyphal coils provide symbiotic interfaces. New physiological and molecular evidence shows that for phosphorus the mycorrhizal pathway (MP) is operational regardless of plant growth responses (positive or negative). Amounts delivered cannot be determined from plant nutrient contents because when responses are negative the contribution of the direct pathway (DP) is reduced. Nitrogen (N) is also delivered to roots via an MP, but the contribution to total N requirement and the costs to the plant are not clear. The functional interplay between activities of the DP and MP has important implications for consideration of AM symbioses in ecological, agronomic, and evolutionary contexts.

Plant and microbial strategies to improve the phosphorus efficiency of agriculture

BackgroundAgricultural production is often limited by low phosphorus (P) availability. In developing countries, which have limited access to P fertiliser, there is a need to develop plants that are more efficient at low soil P. In fertilised and intensive systems, P-efficient plants are required to minimise inefficient use of P-inputs and to reduce potential for loss of P to the environment.ScopeThree strategies by which plants and microorganisms may improve P-use efficiency are outlined: (i) Root-foraging strategies that improve P acquisition by lowering the critical P requirement of plant growth and allowing agriculture to operate at lower levels of soil P; (ii) P-mining strategies to enhance the desorption, solubilisation or mineralisation of P from sparingly-available sources in soil using root exudates (organic anions, phosphatases), and (iii) improving internal P-utilisation efficiency through the use of plants that yield more per unit of P uptake.ConclusionsWe critically review evidence that more P-efficient plants can be developed by modifying root growth and architecture, through manipulation of root exudates or by managing plant-microbial associations such as arbuscular mycorrhizal fungi and microbial inoculants. Opportunities to develop P-efficient plants through breeding or genetic modification are described and issues that may limit success including potential trade-offs and trait interactions are discussed. Whilst demonstrable progress has been made by selecting plants for root morphological traits, the potential for manipulating root physiological traits or selecting plants for low internal P concentration has yet to be realised.

Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas

Arbuscular mycorrhizal (AM) symbioses are formed by approximately 80% of vascular plant species in all major terrestrial biomes. In consequence an understanding of their functions is critical in any study of sustainable agricultural or natural ecosystems. Here we discuss the implications of recent results and ideas on AM symbioses that are likely to be of particular significance for plants dealing with abiotic stresses such as nutrient deficiency and especially water stress. In order to ensure balanced coverage, we also include brief consideration of the ways in which AM fungi may influence soil structure, carbon deposition in soil and interactions with the soil microbial and animal populations, as well as plant-plant competition. These interlinked outcomes of AM symbioses go well beyond effects in increasing nutrient uptake that are commonly discussed and all require to be taken into consideration in future work designed to understand the complex and multifaceted responses of plants to abiotic and biotic stresses in agricultural and natural environments.

More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses

Symbiosis is well recognized as a major force in plant ecology and evolution. However, there is considerable uncertainty about the functional, ecological and evolutionary benefits of the very widespread facultative arbuscular mycorrhizal (AM) associations, in which the plants can grow and reproduce whether or not they are colonized by AM fungi. Here we address the significance of new research findings that are overturning conventional views that facultative AM associations can be likened to parasitic fungus-plant associations. Specifically, we address the occurrence and importance of phosphate uptake via AM fungi that does not result in increases in total phosphorus (P) uptake or in plant growth, and possible signalling between AM fungi and plants that can result in plant growth depressions even when fungal colonization remains very low. We conclude that, depending on the individual AM fungi that are present, the role of facultative AM associations in the field, especially in relation to plant competition, may be much more subtle than has been previously envisaged.

Strategies and agronomic interventions to improve the phosphorus-use efficiency of farming systems

Phosphorus (P)-deficiency is a significant challenge for agricultural productivity on many highly P-sorbing weathered and tropical soils throughout the world. On these soils it can be necessary to apply up to five-fold more P as fertiliser than is exported in products. Given the finite nature of global P resources, it is important that such inefficiencies be addressed. For low P-sorbing soils, P-efficient farming systems will also assist attempts to reduce pollution associated with P losses to the environment. P-balance inefficiency of farms is associated with loss of P in erosion, runoff or leaching, uneven dispersal of animal excreta, and accumulation of P as sparingly-available phosphate and organic P in the soil. In many cases it is possible to minimise P losses in runoff or erosion. Uneven dispersal of P in excreta typically amounts to ~5% of P-fertiliser inputs. However, the rate of P accumulation in moderate to highly P-sorbing soils is a major contributor to inefficient P-fertiliser use. We discuss the causal edaphic, plant and microbial factors in the context of soil P management, P cycling and productivity goals of farms. Management interventions that can alter P-use efficiency are explored, including better targeted P-fertiliser use, organic amendments, removing other constraints to yield, zone management, use of plants with low critical-P requirements, and modified farming systems. Higher productivity in low-P soils, or lower P inputs in fertilised agricultural systems can be achieved by various interventions, but it is also critically important to understand the agroecology of plant P nutrition within farming systems for improvements in P-use efficiency to be realised.

Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth

Recent research on arbuscular mycorrhizas has demonstrated that AM fungi play a significant role in plant phosphorus (P) uptake, regardless of whether the plant responds positively to colonization in terms of growth or P content. Here we focus particularly on implications of this finding for consideration of the balance between organic carbon (C) use by the fungi and P delivery (i.e. the C–P trade between the symbionts). Positive growth responses to arbuscular mycorrhizal (AM) colonization are attributed frequently to increased P uptake via the fungus, which results in relief of P deficiency and increased growth. Zero AM responses, compared with non-mycorrhizal (NM) plants, have conventionally been attributed to failure of the fungi to deliver P to the plants. Negative responses, combined with excessive C use, have been attributed to this failure. The fungi were viewed as parasites. Demonstration that the AM pathway of P uptake operates in such plants indicates that direct P uptake by the roots is reduced and that the fungi are not parasites but mutualists because they deliver P as well as using C. We suggest that poor plant growth is the result of P deficiency because AM fungi lower the amount of P taken up directly by roots but the AM uptake of P does compensate for the reduction. The implications of interplay between direct root uptake and AM fungal uptake of P also include increased tolerance of AM plants to toxins such as arsenate and increased success when competing with NM plants. Finally we discuss the new information on C–P trade in the context of control of the symbiosis by the fungus or the plant, including new information (from NM plants) on sugar transport and on the role of sucrose in the signaling network involved in responses of plants to P deprivation.

What is the significance of the arbuscular mycorrhizal colonisation of many economically important crop plants

Arbuscular mycorrhizal (AM) symbioses are widespread in land plants but the extent to which they are functionally important in agriculture remains unclear, despite much previous research. We ask focused questions designed to give new perspectives on AM function, some based on recent research that is overturning past beliefs. We address factors that determine growth responses (from positive to negative) in AM plants, the extent to which AM plants that lack positive responses benefit in terms of nutrient (particularly phosphate: P) uptake, whether or not AM and nonmycorrhizal (NM) plants acquire different forms of soil P, and the cause(s) of AM ‘growth depressions’. We consider the relevance of laboratory work to the agricultural context, including effects of high (available) soil P on AM fungal colonisation and whether AM colonisation may be deleterious to crop production due to fungal ‘parasitism’. We emphasise the imperative for research that is aimed at increasing benefits of AM symbioses in the field at a time of increasing prices of P-fertiliser, and increasing demands on agriculture to feed the world. In other words, AM symbioses have key roles in providing ecosystem services that are receiving increasing attention worldwide.

Arsenic uptake and toxicity in plants: integrating mycorrhizal influences

Arsenic (As) contamination of soil and water is a global problem that impacts on many areas of biology. This review firstly covers aspects of soil chemistry and soil-plant interactions relevant to the ways plants take up As (particularly arsenate (As(V)) from aerobic soils, with especial attention to As-phosphorus (P) interactions. It then assesses the extent to which studies of plant As tolerance based on short-term uptake of As(V) from nutrient solutions can be extrapolated to longer-term growth in contaminated soil. Mycorrhizal symbioses are then highlighted, because they are formed by ~ 90% of higher plants, often with increased uptake of phosphate (Pi) compared with non-mycorrhizal (NM) counterparts. It is therefore likely that mycorrhizas influence As(V) uptake. Published work shows that arbuscular mycorrhizal (AM) plants (the most common mycorrhizal type) have higher P/As ratios than NM plants, and this would be expected to affect sensitivity to soil As. We discuss ways in which higher P/As selectivity might result from differential operation of P and As uptake pathways in AM compared with NM plants, taking into account new understanding of P uptake mechanisms. We also give suggestions for future research required to increase understanding of mechanisms of As(V) uptake, and its interactions with plant P.

Nutrient transfer in arbuscular mycorrhizas: how are fungal and plant processes integrated?

This review brings together recent work on the coordination of transport processes between fungus and plant symbionts in arbuscular mycorrhizal (AM) symbioses, and focuses on new information on the diversity in structure and function of interfaces and their potential roles in transport processes. We consider the way that fungal activity is polarised to absorb mineral nutrients (especially phosphorus, P) in soil, transport them to the root and release them to the plant. Conversely, the fungal structures within the root appear to be specialised to absorb sugars, which the external mycelium cannot do. The external mycelium depends on a supply of lipid, transported from within the root. High affinity P transporters expressed in the root apices and root hairs of non-mycorrhizal roots, and most probably mycorrhizal roots, absorb P actively. This can result in the development of P depletion zones, so that a low concentration of P at the absorbing surfaces limits further uptake. The external hyphae of AM fungi extend well beyond the depletion zone, accessing supplies of P at a distance and in narrow soil pores, that is absorbed actively by a high affinity P transporter expressed in these small diameter hyphae. Translocation of P within the hyphae and transfer to the plant results in much higher rates of uptake (inflows) by mycorrhizal than non-mycorrhizal roots. The possible role of polyphosphate (polyP) in this process is discussed in the light of new data. Within the root, P is lost from the fungal structures to the interfacial apoplast by an unknown mechanism, and is absorbed by the root cortical cells. The expression of a high affinity P transporter and H + -ATPase in arbuscule-containing cells indicates that these are probably the sites of fungus/plant P transfer. The site of sugar transfer from plant to fungus has not yet been established. At the whole plant level, plant uptake systems located in the youngest regions of the root are positioned to absorb P from undepleted soil, into which the root apex has just grown. In older regions of the roots, colonised by mycorrhizal fungi, the external mycelium will take over the absorptive role and overcome the difficulties posed by the slow diffusion of P in soil.