Functional Adaptation of a Plant Receptor- Kinase Paved the Way for the Evolution of Intracellular Root Symbioses with Bacteria

Abstract

Nitrogen-fixing root nodule symbioses (RNS) occur in two major forms—Actinorhiza and legume-rhizobium symbiosis—which differ in bacterial partner, intracellular infection pattern, and morphogenesis. The phylogenetic restriction of nodulation to eurosid angiosperms indicates a common and recent evolutionary invention, but the molecular steps involved are still obscure. In legumes, at least seven genes—including the symbiosis receptor-kinase gene SYMRK—are essential for the interaction with rhizobia bacteria and for the Arbuscular Mycorrhiza (AM) symbiosis with phosphate-acquiring fungi, which is widespread in occurrence and believed to date back to the earliest land plants. We show that SYMRK is also required for Actinorhiza symbiosis of the cucurbit Datisca glomerata with actinobacteria of the genus Frankia, revealing a common genetic basis for both forms of RNS. We found that SYMRK exists in at least three different structural versions, of which the shorter forms from rice and tomato are sufficient for AM, but not for functional endosymbiosis with bacteria in the legume Lotus japonicus. Our data support the idea that SYMRK sequence evolution was involved in the recruitment of a pre-existing signalling network from AM, paving the way for the evolution of intracellular root symbioses with nitrogen-fixing bacteria.

Transcriptomics of Actinorhizal Symbioses Reveals Homologs of the Whole Common Symbiotic Signaling Cascade

“…The recent demonstration that the common SYM pathway gene SymRK is also required for actinorhizal nodulation (Gherbi et al, 2008;Markmann et al, 2008) led us to reconsider to what extent the nodulation signaling pathway is conserved in legumes and actinorhizal plants. In this study, we were able to highlight the fact that, beyond SymRK, the whole array of compounds of the Nod factor signal transduction pathway is shared between RNS in legumes and actinorhizal plants.…”

“…The symbiotic determinants of the actinorhizal plants are still poorly known (Perrine-Walker et al, 2011), aside from the recent demonstration that SymRK is a linchpin in Casuarina and Datisca (Gherbi et al, 2008;Markmann et al, 2008) and plays a role similar to that played in legumes. These results raise two important questions: do all endosymbioses share a unique pathway?…”

Exogenous glucosinolate produced by Arabidopsis thaliana has an impact on microbes in the rhizosphere and plant roots

“…However, the development of arbuscular mycorrhizal fungi in the host roots involved a complex cellular relationship both controlled by the plant branching factors strigolactones (Akiyama et al 2005) and the Common Symbiosis Pathway (CSP) plant-signalling pathway. This pathway is common to arbuscular mycorrhizal, rhizobial and actinorhizal root symbioses representing mutualistic relationships in plant root (Markmann et al, 2008). Strigolactone is found in root exudates of many species including A. thaliana (Goldwasser et al, 2008) but most CSP gene orthologs were not predicted in the A. thaliana genome, whereas a non nodulating mycorrhized plant, O. sativa possesses all CSP ortholog candidates (Zhu et al, 2006).…”

The Nod factor-independent nodulation in Aeschynomene evenia required the common plant-microbe symbiotic "toolkit"

“…Interestingly, two so-called common symbiotic genes, CgSYMRK/DgSYMRK and CgCCaMK, have been shown to be also necessary for the establishment of the symbiosis between actinorhizal plants (Casuarina glauca and Datisca glomerata) and Frankia spp. (Gherbi et al, 2008;Markmann et al, 2008;Svistoonoff et al, 2013).…”