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

Abstract

Aerial plant architecture is predominantly determined by shoot branching and leaf morphology, which are governed by apparently unrelated developmental processes, axillary meristem formation, and leaf dissection. Here, we show that in tomato (Solanum lycopersicum), these processes share essential functions in boundary establishment. Potato leaf (C), a key regulator of leaf dissection, was identified to be the closest paralog of the shoot branching regulator Blind (Bl). Comparative genomics revealed that these two R2R3 MYB genes are orthologs of the Arabidopsis thaliana branching regulator REGULATOR OF AXILLARY MERISTEMS1 (RAX1). Expression studies and complementation analyses indicate that these genes have undergone sub- or neofunctionalization due to promoter differentiation. C acts in a pathway independent of other identified leaf dissection regulators. Furthermore, the known leaf complexity regulator Goblet (Gob) is crucial for axillary meristem initiation and acts 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. Thus, leaf architecture and shoot architecture rely on a conserved mechanism of boundary formation preceding the initiation of leaflets and axillary meristems.

QTL hotspots in eggplant (Solanum melongena) detected with a high resolution map and CIM analysis

“…Characterization of C has shown it to be a member of a family of R2R3 MYB transcription factors that control shoot branching. Because fully functional copies of C have been found in S. melongena, the gene has been ruled out as the gene responsible for the differences in leaf dissection between cultivated and wild eggplant (Busch et al 2011). These authors suggest that the phenotype of the sf (solanifolia) mutant of tomato makes the Sf gene a more likely candidate for determining the degree of leaf indentation in eggplant.…”

Trifoliate encodes an MYB transcription factor that modulates leaf and shoot architecture in tomato

“…Secondary shoot meristems originate from cells in the leaf axil that show a similar characteristic as those of the marginal blastozone; they are small and undergo a low number of cell divisions (35). The defect of tf mutants in initiating new morphological structures from the marginal blastozone and from the leaf axil suggests that development of both tissues is regulated by similar mechanisms, which is supported by a recent study, demonstrating that shoot branching and leaf dissection are regulated by homologous gene modules (20). Mutations in LOF1 and LOF2, the closest Tf homologs from Arabidopsis, lead to a premature differentiation of boundary cells, resulting in lateral organ fusions and compromised accessory bud formation (25).…”

“…In the leaf, CUC genes repress growth at blade indentations and between leaflets (14-16) and promote the outgrowth of teeth (17). CUC genes are also important regulators of axillary meristem formation in Arabidopsis and tomato (18)(19)(20). In tomato, axillary meristem formation and leaf dissection require the activity of two paralogous MYB genes, Blind (21) and Potato leaf (20), which are expressed in the boundary zones of leaves and leaflets, respectively.…”

“…In tomato, axillary meristem formation and leaf dissection require the activity of two paralogous MYB genes, Blind (21) and Potato leaf (20), which are expressed in the boundary zones of leaves and leaflets, respectively. Furthermore, the branching regulator Lateral suppressor is expressed in both boundary zones, suggesting that axillary meristem formation and leaf dissection are regulated by homologous gene modules (20).…”

Micro-Tom mutants for functional analysis of target genes and discovery of new alleles in tomato

“…Recently published results highlight how powerful this approach can be in providing new alleles for deciphering the function of tomato genes involved in virus resistance Rigola et al 2009), plant growth and architecture (Busch et al 2011;MacAlister et al 2012;Martín-Trillo et al 2011) and fruit nutritional quality (Di Matteo et al 2013;Gady et al 2012;Jones et al 2012). In Micro-Tom, screening 3,052 EMS mutants from the Japan Micro-Tom collection for allelic series of 10 genes involved in ethylene signaling (the SlETR1, SlETR2, SlETR3, SlETR4, SlETR5 and SlETR6 genes), γ-aminobutyric acid (GABA) metabolism (the SlSSADH and SlGABAT1 and SlGABAT3 genes) and fruit softening (the SlPL gene) allowed the identification of up to 35 allelic mutants .…”