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

Abstract

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.

• arbuscular mycorrhiza
• phosphate uptake
• plant growth

Acknowledgments

We thank the Mycological Society of America for the invitation to Sally Smith to present the Karling Lecture in 2010, on which this review is based. We also thank Rebecca Stonor for permission to quote unpublished results and friends and colleagues who have contributed to the development of ideas and collaborated in our recent research, particularly Iver Jakobsen, Lisa Li, Helle Christophersen, Evelina Facelli and Rebecca Stonor.

Our research was financially supported by the Australian Research Council, the South Australian Grain Industry Trust and the Waite Research Institute.

Notes

2 We use arbuscular mycorrhiza to denote the symbiotic structure formed between an arbuscular mycorrhizal (AM) fungus and an underground organ of a plant (usually a root). AM is used for the adjective as in arbuscular mycorrhizal (AM) fungus. We do not use the term mycorrhiza to denote the fungal symbiont.

3 Fungal arbuscules and hyphal coils are often described as intracellular because they grow from hyphae that penetrate the walls of root cortical cells. However these fungal structures remain in an apoplastic compartment outside the cortical cell plasma membranes, which become invaginated and often also modified as the fungal structures grow.

4 We assume that when Fitter and Helgason (2009) say “AM fungi actively (our italics) transport phosphate across the arbuscular membrane…” they mean that there is fungal control of efflux from the fungus to the interfacial apoplast, not that the efflux is itself energetically demanding or active, which is unlikely given the probable cellular and apoplastic P concentrations and inside negative electrical potential.