KEEL LOSS1 Regulates Petal Number Along the Floral Dorsoventral Axis in Lotus Japonicus and Pisum Sativum

Although variation of floral organ numbers has been a prevalent phenomenon during the evolution of zygomorphic flowers among many species, most legumes in the subfamily Papilionoideae possess pentamerous corollas. Previous work showed that dorsoventral asymmetrically expressed CYCLOIDEA (CYC)-like genes have been recruited to the establishment of floral zygomorphy. However, the mechanism determining petal number along the dorsoventral axis remains unknown. Here we address this question by a comparative study of floral development between two papilionoid legumes and characterization of two new genetic loci, KEEL LOSS1 (KEL1) from Lotus japonicus and RED BULL1 (REB1) from pea (Pisum sativum L.). kel1 and reb1 mutants show varying degrees of petal absence along the dorsoventral axis, resembling diverse floral morphologies in legumes with non-pentamerous corollas. Ontogenetic analysis shows that the kel1/reb1 phenotype is caused by the defect of early stage common primordia shared between petal and stamen. KEL1 and REB1 are orthologs encoding APETALA2 (AP2) type transcription factors and are both expressed in the ventral or ventral/dorsal region of the floral meristem, consistent with the predominant absence of petals at the corresponding positions in respective mutants. We also find that KEL1 is independent of the CYC pathway, and interacts with PROLIFERATING FLORAL ORGANS (PFO) to control the common primordia indeterminacy by regulating LjWUSCHEL and LjAGAMOUS expression in L. japonicus. We conclude that KEL1/REB1 regulates position-specific floral patterning and confers robust petal numbers along the dorsoventral axis in papilionaceous flowers. While its major role of controlling petal number is largely conserved between L. japonicus and pea, loss of KEL1 in different ontogenetic or genetic background often leads to distinct floral morphologies, suggesting that KEL1 may be a key dorsoventral factor driving the evolution of legume flowers.