Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species.

Mireille Chabaud,Luis G Wall,Elodie Pirolles,David G Barker,Lukas Brichet,Claudine Franche,Didier Bogusz,Hassen Gherbi,Valérie Hocher,Leandro Imanishi,Iltaf Abdou-Pavy,Joëlle Fournier,Sergio Svistoonoff,Laurent Brottier

doi:10.1371/journal.pone.0223149

Abstract

Mutualistic plant-microbe associations are widespread in natural ecosystems and have made major contributions throughout the evolutionary history of terrestrial plants. Amongst the most remarkable of these are the so-called root endosymbioses, resulting from the intracellular colonization of host tissues by either arbuscular mycorrhizal (AM) fungi or nitrogen-fixing bacteria that both provide key nutrients to the host in exchange for energy-rich photosynthates. Actinorhizal host plants, members of the Eurosid 1 clade, are able to associate with both AM fungi and nitrogen-fixing actinomycetes known as Frankia. Currently, little is known about the molecular signaling that allows these plants to recognize their fungal and bacterial partners. In this article, we describe the use of an in vivo Ca2+ reporter to identify symbiotic signaling responses to AM fungi in roots of both Casuarina glauca and Discaria trinervis, actinorhizal species with contrasting modes of Frankia colonization. This approach has revealed that, for both actinorhizal hosts, the short-chain chitin oligomer chitotetraose is able to mimic AM fungal exudates in activating the conserved symbiosis signaling pathway (CSSP) in epidermal root cells targeted by AM fungi. These results mirror findings in other AM host plants including legumes and the monocot rice. In addition, we show that chitotetraose is a more efficient elicitor of CSSP activation compared to AM fungal lipo-chitooligosaccharides. These findings reinforce the likely role of short-chain chitin oligomers during the initial stages of the AM association, and are discussed in relation to both our current knowledge about molecular signaling during Frankia recognition as well as the different microsymbiont root colonization mechanisms employed by actinorhizal hosts.

Highlights

A limited number of soil microorganisms have acquired the remarkable capacity to colonize plant roots and form mutually beneficial endosymbiotic associations
In this article we have investigated early symbiotic signaling between Arbuscular mycorrhizal (AM) fungi and the two distantly-related actinorhizal host plants, C. glauca and D. trinervis, examples of either intracellular or intercellular Frankia root colonization respectively
Host perception of AM fungal signals was studied for both plants using a nuclear-localized Ca2+ reporter to monitor the activation of the conserved symbiotic signal transduction pathway (CSSP) in epidermal root tissues

Summary

Introduction

A limited number of soil microorganisms have acquired the remarkable capacity to colonize plant roots and form mutually beneficial endosymbiotic associations. Whilst intracellular root entry via infection thread compartments constructed within root hairs has been well-documented in model legume hosts such as Medicago truncatula [5,6], intercellular modes of colonization in legumes are only poorly understood at the molecular/ cellular levels. Both types of root colonization by Frankia have been observed for actinorhizal hosts [4,7]. In the case of initial root colonization by AM fungi, experiments performed on both legume and non-legume hosts have demonstrated that AM fungal hyphae traverse atrichoblast (non-root hair) cells of the root epidermis within host-constructed transcellular compartments by a mechanism reminiscent of root hair infection thread-mediated colonization by nitrogen-fixing bacterial symbionts [2,3]

Methods

Results

Conclusion