Shoot Branching and Leaf Dissection in Tomato Are Regulated by Homologous Gene Modules

Aerial plant architecture is predominantly determined by shoot branching and leaf morphology, which are governed by underlying developmental processes, axillary meristem formation and leaf dissection, that appear fundamentally unrelated. In tomato these processes share essential functions in boundary establishment. We identified Potato leaf (C), a key regulator of leaf dissection, to be the closest paralog of the shoot branching regulator Blind (Bl). Comparative genomics revealed that both R2R3 MYB genes are orthologs of the Arabidopsis branching regulator RAX1. Expression studies and complementation analyses indicate that these genes have undergone sub- or neofunctionalisation due to promoter differentiation. Bl is expressed in the axils of leaves whereas C transcripts accumulate in the boundary zones of leaflets. Furthermore, the known leaf complexity regulator Goblet (Gob) is crucial for axillary meristem initiation and leaf dissection acting in parallel to C and Bl. Finally, RNA in-situ hybridization revealed that the branching regulator Lateral suppressor (Ls) is also expressed in leaves. All four boundary genes, C, Bl, Gob and Ls, may act by suppressing growth, as indicated by gain of function plants. In addition, these gene activities condition a cellular environment that enables the formation of new meristems. Thus, leaf architecture and shoot architecture rely on a conserved mechanism of boundary formation preceding the initiation of leaflets and axillary meristems.