Differential growth dynamics control aerial organ geometry

How gene activities and biomechanics together direct organ shapes is poorly understood. Plant leaf and floral organs develop from highly similar initial structures and share similar gene expression patterns, yet they gain drastically different shapes later-flat and bilateral leaf primordia and radially symmetric floral primordia, respectively. We analyzed cellular growth patterns and gene expression in young leaves and flowers of Arabidopsis thaliana and found significant differences in cell growth rates, which correlate with convergence sites of phytohormone auxin that require polar auxin transport. In leaf primordia, the PRESSED-FLOWER-expressing middle domain grows faster than adjacent adaxial domain and coincides with auxin convergence. In contrast, in floral primordia, the LEAFY-expressing domain shows accelerated growth rates and pronounced auxin convergence. This distinct cell growth dynamics between leaf and flower requires changes in levels of cell-wall pectin de-methyl-esterification and mechanical properties of the cell wall. Data-driven computer model simulations at organ and cellular levels demonstrate that growth differences are central to obtaining distinct organ shape, corroborating in planta observations. Together, our study provides a mechanistic basis for the establishment of early aerial organ symmetries through local modulation of differential growth patterns with auxin and biomechanics.
We thank Jie Cheng and Hongzhi Kong for advice on GPT simulation, Fei Du and Baocai Zhang for advice on immunostaining, Marcus Heisler, Chun-Ming Liu, Elliot Meyerowitz, G. Venu Reddy, and Yan Xiong for materials, and Yanbao Tian for assistance with SEM. Y.J. was supported by K.C. Wong Education Foundation, and NSFC grants 32230010 and 31825002. Y.W. was supported by NSFC grants 32270345 and 31871245, National Key R&D Program of China grant 2019YFA0903902, and Fundamental Research Funds for the Central Universities. K.W. was supported by the Programa de Atraccion de Talento 2017 (Comunidad de Madrid, 2017-T1/BIO-5654 to K.W.), and Programa Estatal de Generacion del Conocimiento y Fortalecimiento Cientıfico y Tecnologico del Sistema de I+D+I 2019 (PGC2018-093387-A-I00) from MICIU. D.A. was funded by the Ministerio de Universidades of Spain FPU19/04729 fellowship. This work has been performed in the frame of the initiative “Centre of Excellence for Plant-Environment Interactions (CEPEI)” between the Centre for Plant Biotechnology and Genomics (CBGP, UPM-INIA/CSIC) and the Institute of Genetics and Developmental Biology (IGDB) and the Plant Stress Centre (PSC) of the Chinese Academy of Science (CAS). CEPEI initiative has been financially supported by the "Severo Ochoa Programme for Centres of Excellence in R&D” from the Agencia Estatal de Investigación of Spain (grants SEV-2016-0672 [2017–2021] and CEX2020-000999-S [2022–2025] to the CBGP). Conceptualization, Y.J. and Y.W.; methodology, Y.X. Z.P. D.A. Y.J. Y.W. and K.W.; software, D.A. and Z.P.; formal analysis, Y.X. Z.P. D.A. S.L. and M.L.; investigation, Y.X. Z.P. and D.A.; data curation, Z.P. and D.A.; writing – original draft, Y.J. Y.X. K.W. D.A. and Z.P.; writing – review & editing, Z.P. Y.J. Y.W. Y.X. K.W. and D.A.; funding acquisition, Y.J. K.W. and Y.W. The authors declare no competing interests.