Leaf dissection and margin serration are independently regulated by two regulators converging on the CUC2-auxin module in strawberry.

ABSTRACT

The remarkable diversity of leaf forms allows plants to adapt to their living environment. In general, leaf diversity is shaped by leaf complexity (compound or simple) and leaf margin pattern (entire, serrated, or lobed). Prior studies in multiple species have uncovered a conserved module of CUC2-auxin that regulates both leaf complexity and margin serration. How this module is regulated in different species to contribute to the species-specific leaf form is unclear. Furthermore, the mechanistic connection between leaf complexity and leaf serration regulation is not well studied. Strawberry has trifoliate compound leaves with serrations at the margin. In the wild strawberry Fragaria vesca, a mutant named salad was isolated that showed deeper leaf serrations but normal leaf complexity. SALAD encodes a single-Myb domain protein and is expressed at the leaf margin. Genetic analysis showed that cuc2a is epistatic to salad, indicating that SALAD normally limits leaf serration depth by repressing CUC2a expression. When both Arabidopsis homologs of SALAD were knocked out, deeper serrations were observed in Arabidopsis rosette leaves, supporting a conserved function of SALAD in leaf serration regulation. We incorporated the analysis of a third strawberry mutant simple leaf 1 (sl1) with reduced leaf complexity but normal leaf serration. We showed that SL1 and SALAD independently regulate CUC2a at different stages of leaf development to, respectively, regulate leaf complexity and leaf serration. Our results provide a clear and simple mechanism of how leaf complexity and leaf serration are coordinately as well as independently regulated to achieve diverse leaf forms.