SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria

Abstract

Root endosymbioses vitally contribute to plant nutrition and fitness worldwide. Nitrogen-fixing root nodulation, confined to four plant orders, encompasses two distinct types of associations, the interaction of legumes (Fabales) with rhizobia bacteria and actinorhizal symbioses, where the bacterial symbionts are actinomycetes of the genus Frankia. Although several genetic components of the host-symbiont interaction have been identified in legumes, the genetic basis of actinorhiza formation is unknown. Here, we show that the receptor-like kinase gene SymRK, which is required for nodulation in legumes, is also necessary for actinorhiza formation in the tree Casuarina glauca. This indicates that both types of nodulation symbiosis share genetic components. Like several other legume genes involved in the interaction with rhizobia, SymRK is also required for the interaction with arbuscular mycorrhiza (AM) fungi. We show that SymRK is involved in AM formation in C. glauca as well and can restore both nodulation and AM symbioses in a Lotus japonicus symrk mutant. Taken together, our results demonstrate that SymRK functions as a vital component of the genetic basis for both plant-fungal and plant-bacterial endosymbioses and is conserved between legumes and actinorhiza-forming Fagales.actinorhizal symbioses ͉ Casuarina glauca ͉ mycorrhizae ͉ signaling R oot endosymbioses are associations between plants and soil microorganisms involving intracellular accommodation of microbes within host cells. The most widespread of these associations is arbuscular mycorrhiza (AM), which is formed by the majority of land plants with fungi belonging to the phylum Glomeromycota (1). In contrast, nitrogen-fixing nodulation symbioses of plant roots and bacteria are restricted to four orders of eurosid dicots (2). Actinorhiza, formed by members of the Fagales, Rosales, and Cucurbitales with Gram-positive Frankia bacteria, differs from the interaction of legumes with Gramnegative rhizobia in several morphological and cytological aspects (3). Although these differences suggest independent regulatory mechanisms, the close relatedness of nodulating lineages indicates a common evolutionary basis of root nodulation symbioses (2). In the legume-rhizobia interaction, among the key factors mediating recognition between the plant and the bacteria are Nod factors (NFs). NFs are bacterial lipochitooligosaccharides with an N-acetylglucosamine backbone (4). The perception of NFs induces a series of responses in host roots, including ion flux changes and membrane depolarization, rhythmic calcium oscillations in and around the nucleus (calcium spiking), cytoskeletal modifications and root hair curling, and activation of cortical cell divisions (5). Extensive mutant screenings performed in legumes led to the identification of several loci involved in this signaling cascade, and recently most of the corresponding genes were identified by map-based approaches (6). In Lotus japonicus, two genes, NFR1 and NFR5 encoding receptor-like serine/threonine kinases with L...

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

“…For others, it is likely that their transcripts were not detected and have not been sequenced in one of the two actinorhizal species. For instance, this was the case of SymRK, whose symbiotic role has already been demonstrated in C. glauca (Gherbi et al, 2008) but was not present among C. glauca unigenes. Interestingly, expression analysis of these symbiosis homologs in A. glutinosa and C. glauca revealed that the accumulation of transcripts in nodules versus uninfected roots was not only comparable between the two actinorhizal species but also similar to those found in legumes (Fig.…”

“…Complete descriptions of BLAST results and related references are given in Supplemental Tables S5 and S6. * DMI2/SymRK was not found in the C. glauca unigene database, and expression results of Gherbi et al (2008) were used for comparison with A. glutinosa.…”

“…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?…”

SYMRK, an enigmatic receptor guarding and guiding microbial endosymbioses with plant roots

“…This task is (still) difficult because of the lack of genomics and genetics tools, but rewarding when the outcome proves some long-standing assumptions and suggests new ways to address old questions. A nice example is the work of Gherbi et al (1) presented in this issue of PNAS. Their article deals with a nonmodel plant, Casuarina glauca, whose roots interact with both symbiotic fungi and nitrogen-fixing bacteria, and evidences the central and ancestral role of the plant receptor SYMRK in the establishment of the three major types of root endosymbioses.…”