A deep dive into the FALSIFLORA contribution to tomato reproductive development through a comprehensive allelic series analysis

Abstract

Plants undergo continuous growth and development thanks to meristems, specialized groups of pluripotent stem cells that remain in their undifferentiated state throughout the plants life cycle. 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. In this study, the allelic series of FA has been expanded by combining the screening of a tomato EMS mutant collection with overexpression, gene silencing and CRISPR/Cas9 genome editing approaches, aimed to deepen the understanding of the functional role of FA during tomato reproductive development. The phenotypic and molecular characterization of the FA allelic series revealed the multifaceted role of FA acting in both early and late stages of floral ontogeny. Thus, in addition to 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 exerts regulatory control over the expression of the tomato homologs of AGAMOUS (TOMATO AGAMOUS1, TAG1) and WUSCHEL (SlWUS), underscoring its function in promoting carpel development and suppressing floral stem cell activity, thereby establishing floral determinacy. In conclusion, our findings demonstrate the potential of employing mutant allelic series as powerful tools for elucidating gene functions and deciphering the intricate molecular basis underlying biological processes. Plain Language SummaryOur research aims to gain a deeper understanding of the role of FALSIFLORA in tomato reproductive development. The FALSIFLORA allelic spectrum was expanded through mutant screening, along with overexpression, silencing, and CRISPR/Cas9 editing approaches. Our findings reveal that FALSIFLORA has a dual function in early and late floral development stages. In addition to promoting floral transition and specifying floral meristem identity, FA regulates the expression of tomato genes homologous to WUSCHEL and AGAMOUS, which play an essential role in stem cell regulation and carpel development. This study highlights the value of allelic series in elucidating gene functions and intricate biological mechanisms.