Contrasting Expansion Patterns of Nodulation-Related Signaling Peptides

Small signaling peptides play an important role in the development of nodules, the symbiotic organs necessary for legume symbioses with nitrogen fixing Rhizobia. In this study, lineage-specific expansions of peptide families were analyzed in a systematic way, using nodule transcriptome data coupled with gene clustering. Our study discovered the expansion of two largely unstudied gene families with nodule-specific expression that are unique to either Trifoleae and Phaseoleae lineages. The first family, annotated as 'Embryo-Specific Protein' (ESP), has five nodule specific members that expanded by tandem duplication in Medicago truncatula. Synteny analyses suggest that a single copy of the nodule-specific syntenic ortholog was retained in Glycine max and was lost in Phaseolus vulgaris. The more distantly related legumes Arachis duranensis and A. ipaensis also have a copy of a nodule-specific ESP, yet phylogenetic analyses suggest these were co-opted for nodulation through a separate event. The second family of interest has previously been annotated as ‘Nodulin’, and appears to be unique to the Phaseoleae lineage. P. vulgaris has three nodulins in this family that expanded through tandem duplications. By contrast, the seven copies present in the soybean genome expanded through distant duplications and/or ancient whole-genome duplications, suggesting that the expansions occurred separately in the Glycine and Phaseolus lineages. Thus, parallel expansions (or co-opting?) of nodulation-related families have occurred across different legume lineages, yet they have to have occurred through different mechanisms.