Sally E. Smith

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.

Mycorrhizas of autotrophic higher plants.

(1) The range of mycorrhizal types is briefly compared, with respect to structure and nutritional mode of the symbionts. Ectotrophic, vesicular‐arbuscular and erica‐ceous mycorrhizas of autotrophic plants are selected for further consideration, both because the symbionts have nutritional similarities, and because recent experimental work provides a basis for useful comparisons.

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.

A mutant inLycopersicon esculentumMill. with highly reduced VA mycorrhizal colonization: isolation and preliminary characterisation

This paper reports the successful isolation and preliminary characterisation of a mutant of Lycopersicon esculentum Mill. with highly reduced vesicular-arbuscular (VA) mycorrhizal colonization. The mutation is recessive and has been designated rmc . Colonization by G. mosseae is characterised by poor development of external mycelium and a few abnormal appressoria. Vesicles were never formed by this fungus in association with the mutant. Gi. margarita formed large amounts of external mycelium, complex branched structures and occasional auxiliary cells. Small amounts of internal colonization also occurred. Laser scanning confocal microscopy (LSCM) gave a clear picture of the differences in development of G. intraradices and Gi. margarita in mutant and wild-type roots and confirmed that the fungus is restricted to the root surface of the mutants. The amenability of tomato for molecular genetic characterisation should enable us to map and clone the mutated gene, and thus identify one of the biochemical bases for inability to establish a normal mycorrhizal symbiosis. The mutant represents a key advance in molecular research on VA mycorrhizal symbiosis.

Mineral nutrition, toxic element accumulation and water relations of arbuscular mycorrhizal plants

Publisher Summary This chapterpresents an overview of the current understanding of the role of arbuscular mycorrhizas (AM) in the mineral nutrition of plants, focusing on the mechanisms that have been suggested to account for the AM effects. There is excellent evidence demonstrating that external hyphae of AM fungi absorb nonmobile nutrients from soil and translocate them rapidly to the plants, thus overcoming problems of depletion in the rhizosphere which arise as a consequence of uptake by roots. Transfer across the symbiotic interface often results in increased nutrient acquisition by the plant. These processes act in series and, with efficient fungi producing extensive external mycelium, lead to depletion of nutrients in the soil well beyond the rhizosphere. Molecular and physiological mechanisms underlying the integration of plant and fungal uptake pathways are increasingly being revealed. At the cellular level, details of fungal phosphorus (P) and nitrogen (N) metabolism are being revealed that together with information on the effects of AM symbiosis on expression of both fungal and plant nutrient transporters, is beginning to lead to a coherent general picture of how fungal and plant nutrient acquisition processes are integrated. The interactions between AM colonization and accumulation of heavy metals and other toxic elements are areas of considerable interest, in relation both to production of safe food and bioremediation programs. A number of different mechanisms may be involved, including tissue dilution of the toxic element due to interactions with P nutrition and growth, sequestration of the toxic metal in the fungus, and development of tolerance by the fungi. Furthermore, the effects of AM on the water relations of plants are also discussed.

Arbuscular mycorrhizal fungi can induce the production of phytochemicals in sweet basil irrespective of phosphorus nutrition

The potential of three arbuscular mycorrhizal fungi (AMF) to enhance the production of antioxidants (rosmarinic and caffeic acids, RA and CA) was investigated in sweet basil (Ocimum basilicum). After adjusting phosphorus (P) nutrition so that P concentrations and yield were matched in AM and non-mycorrhizal (NM) plants we demonstrated that Glomus caledonium increased RA and CA production in the shoots. Glomus mosseae also increased shoot CA concentration in basil under similar conditions. Although higher P amendments to NM plants increased RA and CA concentrations, there was higher production of RA and CA in the shoots of AM plants, which was not solely due to better P nutrition. Therefore, AMF potentially represent an alternative way of promoting growth of this important medicinal herb, as natural ways of growing such crops are currently highly sought after in the herbal industry.

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.