A Growth-Based Framework for Leaf Shape Development and Diversity

How do genes modify cellular growth to create morphological diversity? We study this problem in two related plants with differently shaped leaves: Arabidopsis thaliana (simple leaf shape) and Cardamine hirsuta (complex shape with leaflets). We use live imaging, modeling, and genetics to deconstruct these organ-level differences into their cell-level constituents: growth amount, direction, and differentiation. We show that leaf shape depends on the interplay of two growth modes: a conserved organ-wide growth mode that reflects differentiation; and a local, directional mode that involves the patterning of growth foci along the leaf edge. Shape diversity results from the distinct effects of two homeobox genes on these growth modes: SHOOTMERISTEMLESS broadens organ-wide growth relative to edge-patterning, enabling leaflet emergence, while REDUCED COMPLEXITY inhibits growth locally around emerging leaflets, accentuating shape differences created by patterning. We demonstrate the predictivity of our findings by reconstructing key features of C. hirsuta leaf morphology in A. thaliana. [Display omitted] [Display omitted] •Complete growth and fate maps are made for C. hirsuta and A. thaliana leaf surfaces•Patterning of the leaf margin modifies organ-wide growth pattern to produce leaf shape•Altering growth relative to patterning generates leaf shape diversity•Reconstructing dissected leaf shape by combining STM and RCO in A. thaliana leaves By understanding the impact of growth and patterning on leaf shape diversity, it is possible to convert the leaf morphology of A. thaliana to that of another plant species.