The Azolla fern symbiosis sexual reproduction requires far-red light and involves responsive CMADS1 homologue, miR319-controlled GAMYB, miR529 in the fern and transporters in the symbiont

Abstract

Azolla ferns and the filamentous cyanobacteria Nostoc azollae constitute a model symbiosis that enabled colonization of the water surface with traits highly desirable for development of more sustainable crops: their floating mats capture CO2 and fixate N2 at high rates phototrophically. Their mode of sexual reproduction is heterosporous. Regulation of the transition from vegetative to spore-forming phases in ferns is largely unknown, yet a pre-requisite for Azolla domestication, and of particular interest since ferns represent the sister lineage of seed plants. Far-red light (FR) induced sporocarp formation in A. filiculoides. Sporocarps obtained, when crossed, verified species attribution of Netherlands strains but not Irans Anzali lagoon. FR-responsive transcripts included CMADS1 MIKCC-homologues and miRNA-controlled GAMYB transcription factors in the fern, transporters in N.azollae, and ycf2 in chloroplasts. Loci of conserved miRNA in the fern lineage included miR172, yet FR only induced miR529 and miR535, and reduced miR319 and miR159. Suppression of sexual reproduction in both gametophyte and sporophyte-dominated plant lineages by red light is likely a convergent ecological strategy in open fields as the active control networks in the different lineages differ. MIKCC transcription factor control of flowering and flower organ specification, however, likely originated from the diploid to haploid phase transition in the homosporous common ancestor of ferns and seed plants.