Abstract

Plants interact with diverse microbes including those that result in nutrient-acquiring symbioses. In order to balance the energy cost with the benefit gained, plants employ a systemic negative feedback loop to control the formation of these symbioses. This is particularly well-understood in nodulation, the symbiosis between legumes and nitrogen-fixing rhizobia, and is known as autoregulation of nodulation (AON). However, much less is understood about the autoregulation of the ancient arbuscular mycorrhizal symbioses that form between Glomeromycota fungi and the majority of land plants. Elegant physiological studies in legumes have indicated there is at least some overlap in the genes and signals that regulate these two symbioses but there are major gaps in our understanding. In this paper we examine the hypothesis that the autoregulation of mycorrhizae (AOM) pathway shares some elements with AON but that there are also some important differences. By reviewing the current knowledge of the AON pathway, we have identified important directions for future AOM studies. We also provide the first genetic evidence that CLV2 (an important element of the AON pathway) influences mycorrhizal development in a non-legume, tomato and review the interaction of the autoregulation pathway with plant hormones and nutrient status. Finally, we discuss whether autoregulation may play a role in the relationships plants form with other microbes.

Highlights

  • Mycorrhizal symbioses between plants and fungi are widespread and ancient, with evidence from fossils and extant basal plants indicating that such interactions evolved during the colonization of land by plants between 450 and 475 mya (Field et al, 2015; Martin et al, 2017)

  • We examine our current understanding of autoregulation of mycorrhizae (AOM) and begin to extend this beyond legumes by providing evidence of a role for the key autoregulation of nodulation (AON) gene in legumes, CLAVATA2 (CLV2), in the AOM pathway of tomato

  • One study examining the effect of a pea clv2 mutant found only a small but not significant increase in arbuscular mycorrhizal (AM) colonization compared with wild type (WT), grafting and split root studies that would reveal if CLV2 plays a role in the systemic regulation of AM were not attempted (Morandi et al, 2000)

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Summary

Introduction

Mycorrhizal symbioses between plants and fungi are widespread and ancient, with evidence from fossils and extant basal plants indicating that such interactions evolved during the colonization of land by plants between 450 and 475 mya (Field et al, 2015; Martin et al, 2017). Studies in legumes suggest some key cross-overs in the autoregulation pathways, as plant mutants disrupted in the AON pathway display hypernodulation and hypermycorrhizal colonization (Morandi et al, 2000; Shrihari et al, 2000) and split root studies indicate nodulation can systemically suppress AM and vice versa (Catford et al, 2003).

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