Coordination of differentiation rate and local patterning in compound-leaf development.

The variability in leaf form in nature is immense. Leaf patterning occurs by differential growth, taking place during a limited window of morphogenetic activity at the leaf marginal meristem. While many regulators have been implicated in the designation of the morphogenetic window and in leaf patterning, how these effectors interact to generate a particular form is still not well understood. We investigated the interaction among different effectors of tomato (Solanum lycopersicum) compound-leaf development, using genetic and molecular analyses. Mutations in the tomato auxin response factor SlARF5/SlMP, which normally promotes leaflet formation, suppressed the increased leaf complexity of mutants with extended morphogenetic window. Impaired activity of the NAC/CUC transcription factor GOBLET (GOB), which specifies leaflet boundaries, also reduced leaf complexity in these backgrounds. Analysis of genetic interactions showed that the patterning factors SlMP, GOB and the MYB transcription factor LYRATE (LYR) coordinately regulate leaf patterning by modulating in parallel different aspects of leaflet formation and shaping. This work places an array of developmental regulators in a morphogenetic context. It reveals how organ-level differentiation rate and local growth are coordinated to sculpture an organ. These concepts are applicable to the coordination of pattering and differentiation in other species and developmental processes.

CLAUSA restricts tomato leaf morphogenesis and GOBLET expression.

Leaf morphogenesis and differentiation are highly flexible processes. The development of compound leaves is characterized by an extended morphogenesis stage compared with that of simple leaves. The tomato mutant clausa (clau) possesses extremely elaborate compound leaves. Here we show that this elaboration is generated by further extension of the morphogenetic window, partly via the activity of ectopic meristems present on clau leaves. Further, we propose that CLAU might negatively affect expression of the NAM/CUC gene GOBLET (GOB), an important modulator of compound-leaf development, as GOB expression is elevated in clau mutants and reducing GOB expression suppresses the clau phenotype. Expression of GOB is also elevated in the compound leaf mutant lyrate (lyr), and the remarkable enhancement of the clau phenotype by lyr suggests that clau and lyr affect leaf development and GOB in different pathways.

Dynamic growth program regulated by LANCEOLATE enables flexible leaf patterning.

During their development, leaves progress through a highly controlled yet flexible developmental program. Transcription factors from the CIN-TCP family affect leaf shape by regulating the timing of leaf maturation. Characterization of mutants in the tomato (Solanum lycopersicum) CIN-TCP gene LANCEOLATE (LA) led us to hypothesize that a threshold LA-like activity promotes leaf differentiation. Here, we examined the relationship between LA activity, leaf maturation, and final leaf size and shape. Leaves of diverse shapes from various Solanaceae species or from different positions on the tomato plant differed in the timing of growth and maturation, and these were often associated with altered LA expression dynamics. Accordingly, genetic manipulations of LA activity in tomato altered leaf growth and maturation, leading to changes in leaf size and shape. LA expression sustained until late stages of tomato leaf development, and stage-specific overexpression of miR319, a negative regulator of CIN-TCP genes, confirmed that LA-like proteins affect leaf development through these late stages. Together, our results imply that dynamic spatial and temporal leaf maturation, coordinated by LA-like genes, enables the formation of variable leaf forms.