Paralogous Gene Recruitment in Multiple Families Constitutes Genetic Architecture and Robustness of Pod Dehiscence in Legumes

Pod dehiscence facilitates seed dispersal in wild legumes while indehiscence is a key domestication trait in cultivated ones. However, the evolutionary genetic mechanisms underlying its diversity are largely unclear. In this study, we compared transcriptomes of two warm-season (Glycine spp. and Phaseolus spp.) and two cool-season (Pisum spp. and Medicago ruthenica) legumes in analysis of dehiscent and indehiscent pod genotypes. Differentially expressed genes in AP2/ERF-like transcription factors and seven structural gene families, including lactoperoxidase, laccase, and cellulose synthase-interactive proteins, which are involved in secondary cell wall component accumulation, were identified to exert key roles in pod dehiscence variation. In accordance with this, higher lignin and cellulose contents were observed in pod secondary cell wall of dehiscent accessions of soybean and pea; however, the variation patterns of lignin polymers in soybean (accumulation) and pea (proportion) differed between dehiscent and indehiscent pods. Moreover, genome-wide comparative analysis revealed that orthogroups represented <1% of all identified differentially expressed genes could be traced among the four genera of legumes, while recruiting paralogous members may constitute the genetic robustness of legume pod dehiscence. This study compared the genetic mechanism among several legumes in pod dehiscence formation and revealed a compensating role of paralogous redundancy of involved gene families in seed dispersal, which can guide crop breeding.