Epidermal restriction confers robustness to organ shapes

• Published in: Journal of integrative plant biology Vol. 62; no. 12; pp. 1853 - 1867
• Main Authors: Zhou, Lüwen, Du, Fei, Feng, Shiliang, Hu, Jinrong, Lü, Shouqin, Long, Mian, Jiao, Yuling
• Format: Journal Article
• Language: English
• Published: China (Republic : 1949- ) Wiley Subscription Services, Inc 01.12.2020; University of Chinese Academy of Sciences, Beijing 100049, China; Smart Materials and Advanced Structure Laboratory, School of Mechanical Engineering and Mechanics, Ningbo University, Ningbo 315211, China%State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China%Key Laboratory of Microgravity (National Microgravity Laboratory), Center of Biomechanics and Bioengineering, and Beijing Key Laboratory of Engineered Construction and Mechanobiology, Institute of Mechanics, Chinese Academy of Sciences, Beijing 100190, China; University of Chinese Academy of Sciences, Beijing 100049, China%State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China
• Subjects: Asymmetry; Computer applications; Organs; Questions; Robust control; Robustness
• ISSN: 1672-9072; 1744-7909
• DOI: 10.1111/jipb.12998

The shape of comparable tissues and organs is consistent among individuals of a given species, but how this consistency or robustness is achieved remains an open question. The interaction between morphogenetic factors determines organ formation and subsequent shaping, which is ultimately a mechanical process. Using a computational approach, we show that the epidermal layer is essential for the robustness of organ geometry control. Specifically, proper epidermal restriction allows organ asymmetry maintenance, and the tensile epidermal layer is sufficient to suppress local variability in growth, leading to shape robustness. The model explains the enhanced organ shape variations in epidermal mutant plants. In addition, differences in the patterns of epidermal restriction may underlie the initial establishment of organ asymmetry. Our results show that epidermal restriction can answer the longstanding question of how cellular growth noise is averaged to produce precise organ shapes, and the findings also shed light on organ asymmetry establishment. How organs maintain reproducible geometric shapes remains mysterious. A combination of computational and experimental approaches revealed that the epidermal layer is essential for the robustness of organ shape, as sufficient epidermal restriction not only suppresses local growth variability, but also maintains organ asymmetry.