Heart of Endosymbioses: Transcriptomics Reveals a Conserved Genetic Program among Arbuscular Mycorrhizal, Actinorhizal and Legume-Rhizobial Symbioses

Alexandre Tromas,Alexandre Tromas,Alexandre Tromas,Nathalie Diagne,Benoit Lahouze,Valérie Hocher,Valérie Hocher,Valérie Hocher,Boris Parizot,Boris Parizot,Antony Champion,Antony Champion,Antony Champion,Maïmouna Cissoko,Didier Bogusz,Didier Bogusz,Sergio Svistoonoff,Sergio Svistoonoff,Sergio Svistoonoff,Amandine Crabos,Hermann Prodjinoto,Laurent Laplaze,Laurent Laplaze,Laurent Laplaze,Didier Bogusz

doi:10.1371/journal.pone.0044742

Abstract

To improve their nutrition, most plants associate with soil microorganisms, particularly fungi, to form mycorrhizae. A few lineages, including actinorhizal plants and legumes are also able to interact with nitrogen-fixing bacteria hosted intracellularly inside root nodules. Fossil and molecular data suggest that the molecular mechanisms involved in these root nodule symbioses (RNS) have been partially recycled from more ancient and widespread arbuscular mycorrhizal (AM) symbiosis. We used a comparative transcriptomics approach to identify genes involved in establishing these 3 endosymbioses and their functioning. We analysed global changes in gene expression in AM in the actinorhizal tree C. glauca. A comparison with genes induced in AM in Medicago truncatula and Oryza sativa revealed a common set of genes induced in AM. A comparison with genes induced in nitrogen-fixing nodules of C. glauca and M. truncatula also made it possible to define a common set of genes induced in these three endosymbioses. The existence of this core set of genes is in accordance with the proposed recycling of ancient AM genes for new functions related to nodulation in legumes and actinorhizal plants.

Highlights

Mutualistic interactions between plants and microorganisms are an essential and widespread adaptive response whose origin can be traced back to land colonisation by plants: fossil evidence demonstrates that,450 million years ago primitive plants were already associated with fungi to form arbuscular mycorrhizal (AM) symbioses [1]
The ability to form root nodule symbioses (RNS) evolved only in fabids and gave rise to two main types of symbioses: (1) rhizobial RNS involve gram negative proteobacteria collectively called rhizobia that associate with plants from the Fabaceae superfamily and a few species from the genus Parasponia (Cannabaceae), (2) actinorhizal symbioses combine fabids distributed into 8 families, collectively called actinorhizal plants, and the gram positive actinomycete Frankia [3,4,5]
Many genetic mechanisms making it possible to accommodate symbiotic bacteria originate in more ancestral AM symbiosis [4,7,8]: the symbiotic signals emitted by rhizobia and AM fungi are chemically related [9]

Summary

Introduction

Mutualistic interactions between plants and microorganisms are an essential and widespread adaptive response whose origin can be traced back to land colonisation by plants: fossil evidence demonstrates that ,450 million years ago primitive plants were already associated with fungi to form arbuscular mycorrhizal (AM) symbioses [1]. We used comparative transcriptomics to identify genes induced during AM and nodulation (actinorhizal or rhizobial) in several plants, including legumes [14,15], rice [16] and the actinorhizal tree Casuarina glauca [17]. This analysis revealed 84 C. glauca genes up-regulated in AM similar to M. truncatula and O. sativa AM-induced genes

Results

Conclusion