Comprehensive allelic series analysis uncovers the novel function of the tomato FALSIFLORA gene in the cessation of floral meristem activity

Abstract

Plants undergo continuous growth thanks to meristems, specialized groups of pluripotent stem cells that remain undifferentiated throughout the plant's life. Meristem transition from the vegetative to the reproductive phase heavily influences plant reproductive success and agricultural productivity. In tomato (Solanum lycopersicum L.), FALSIFLORA (FA), the orthologue of the Arabidopsis LEAFY gene, promotes floral transition by specifying floral meristem identity and regulating the expression of genes responsible for floral organ identity and development. This study expanded the FA allelic series by combining the screening of an EMS mutant collection with overexpression, silencing and CRISPR/Cas9 genome editing approaches, aimed to deepen the understanding of the functional role of FA during reproductive development. The phenotypic and molecular characterization of the FA allelic series revealed its multifaceted role in both early and late stages of floral ontogeny. Besides promoting floral transition and specifying floral meristem identity, FA also plays a role in inflorescence meristem maturation and termination, thereby regulating the inflorescence architecture. Furthermore, FA potentially exerts regulatory control over the expression of the AGAMOUS homolog (TOMATO AGAMOUS1, TAG1), which in turn may contribute to the deregulation of WUSCHEL (SlWUS) during floral development, underscoring its function in promoting carpel development and suppressing floral stem cell activity, thereby establishing floral determinacy. Our findings reveal for the first time the novel role of FA in the cessation of floral meristem activity in tomato, and demonstrate the value of mutant allelic series as powerful tools for elucidating gene functions and understanding the intricate molecular basis underlying biological processes.