Origin and evolutionary dynamics of the miR2119 and ADH1 regulatory module in Legumes

Abstract

MicroRNAs are important regulators of gene expression in eukaryotes. Previously, we reported that in Phaseolus vulgaris, the precursor for miR2119 is located in the same gene as miR398a, conceiving a dicistronic MIR gene. Both miRNA precursors are transcribed and processed froma single transcript resulting in twomaturemicroRNAs that regulate themRNAs encodingALCOHOL DEHYDROGENASE 1 (ADH1) and COPPER-ZINC SUPEROXIDE DISMUTASE 1 (CSD1). Genes formiR398 are distributed throughout the spermatophytes;however,miR2119 is only found in Leguminosae species, indicating its recent emergence.Here,we used public databases to explore the presence of the miR2119 sequence in several plant species. We found that miR2119 is present only in specific cladeswithin the Papilionoideae subfamily, including important crops used for human consumption and forage.Within this subfamily, MIR2119 and MIR398a are found together as a single gene in the genomes of the Millettioids and Hologalegina. In contrast, in the Dalbergioids MIR2119 is located in a different locus from MIR398a, suggesting this as the ancestral genomic organization. To our knowledge, this is a unique example where two separate MIRNA genes have merged to generate a single polycistronic gene. Phylogenetic analysis of ADH1 gene sequences in the Papilionoideae subfamily revealed duplication events resulting in up to four ADH1 genes in certain species. Notably, the presence of MIR2119 correlates with the conservation of target sites in particular ADH1 genes in each clade.Our results suggest that post-transcriptional regulation ofADH1 genes bymiR2119 has contributed to shaping the expansion and divergence of this gene family in the Papilionoideae. Future experimentalwork on ADH1 regulation bymiR2119 inmore legume specieswill help to further understand the evolutionary history of theADH1 gene family and the relevance of miRNA regulation in this process.