Nodule INception (NIN)-independent epidermal events lead to bacterial entry during nodule development in peanut (Arachis hypogaea)

Abstract

Summary Legumes can host nitrogen-fixing rhizobia inside root nodules. In model legumes, rhizobia enter via infection threads (ITs) and develop nodules where infection-zone contains a mixture of infected and uninfected cells. Peanut (Arachis hypogaea) diversified from model legumes ~50-55 million years ago. Rhizobia enter through ‘cracks’ to form nodules in peanut roots where the cells of infection-zone are uniformly infected. Phylogenomic studies indicated symbiosis as a labile trait in peanut. These atypical features prompted us to investigate the molecular mechanism of peanut nodule development. Combining cell biology, genetics, and genomic tools, we visualized the status of hormonal signaling in peanut nodule primordia. Moreover, we dissected the signaling modules of Nodule INception (NIN), a master regulator of both epidermal infection and cortical organogenesis. Cytokinin signaling operates in a broad zone, from the epidermis to the pericycle inside nodule primordia, while auxin signaling is narrower and focused. NIN is involved in the nodule organogenesis, but not in the crack entry. Nodulation Pectate Lyase (NPL), which remodels cell walls during IT-formation, is not required. Whereas Nodule enhanced Glycosyl Hydrolases (AhNGHs) is recruited for cell wall modification during crack entry. While the hormonal regulation is conserved, the function of the NIN signaling modules is diversified in peanut.