A Growth-Based Framework for Leaf Shape Development and Diversity

Daniel Kierzkowski,Adam Runions,Francesco Vuolo,Sören Strauss,Rena Lymbouridou,Anne-Lise Routier-Kierzkowska,David Wilson-Sánchez,Hannah Jenke,Carla Galinha,Gabriella Mosca,Zhongjuan Zhang,Claudia Canales,Raffaele Dello Ioio,Peter Huijser,Richard S Smith,Miltos Tsiantis

doi:10.1016/j.cell.2019.05.011

Daniel Kierzkowski, Adam Runions + Show 14 more

Open Access

https://doi.org/10.1016/j.cell.2019.05.011

Copy DOI

Abstract

SummaryHow 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.Video

Highlights

How gene activity translates into distinct organ morphologies remains poorly understood (e.g., Runions and Tsiantis, 2017; Zuniga, 2015)
Development of Simple versus Dissected Leaf Primordia We developed an imaging protocol to understand how the balance of conserved versus diverged cellular growth patterns produce the simple leaf forms of A. thaliana and the dissected leaves of C. hirsuta (Figures 1A and 1B)
We computed complete lineage maps from these data (Barbier de Reuille et al, 2015) to understand how cells in the early primordium contribute to the development of the mature leaf form

Summary

Introduction

How gene activity translates into distinct organ morphologies remains poorly understood (e.g., Runions and Tsiantis, 2017; Zuniga, 2015). We lack information on the growth of morphogenetically important domains at the margin and base of developing leaves, and cell-level fate maps for leaf primordia do not exist. It remains unclear how local growth regulation at the margin integrates with global patterns of growth, proliferation, and differentiation to produce divergent leaf forms (Bar and Ori, 2014; Bilsborough et al, 2011; Alvarez et al, 2016; Donnelly et al, 1999; Fox et al, 2018; Kuchen et al, 2012; Poethig, 1987). Current evidence indicates that growth polarity is vital for leaf geometry, yet the degree to which this polarity is a local or global feature of organ development and how it

Methods

Results

Discussion

Conclusion