Brassinosteroid coordinates cell layer interactions in plants via cell wall and tissue mechanics

Author:

Kelly-Bellow Robert1ORCID,Lee Karen1ORCID,Kennaway Richard1ORCID,Barclay J. Elaine1ORCID,Whibley Annabel1ORCID,Bushell Claire1ORCID,Spooner Jamie1,Yu Man1,Brett Paul2ORCID,Kular Baldeep2ORCID,Cheng Shujing3ORCID,Chu Jinfang34ORCID,Xu Ting5,Lane Brendan6ORCID,Fitzsimons James7ORCID,Xue Yongbiao5ORCID,Smith Richard S.6ORCID,Whitewoods Christopher D.17ORCID,Coen Enrico1ORCID

Affiliation:

1. Department of Cell and Developmental Biology, John Innes Centre, Norwich NR4 7UH, UK.

2. Department of Biochemistry and Metabolism, John Innes Centre, Norwich NR4 7UH, UK.

3. National Centre for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.

4. College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing 100039, China.

5. State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.

6. Department of Computational and Systems Biology, John Innes Centre, Norwich NR4 7UH, UK.

7. Sainsbury Laboratory, University of Cambridge, Cambridge CB2 1LR, UK.

Abstract

Growth coordination between cell layers is essential for development of most multicellular organisms. Coordination may be mediated by molecular signaling and/or mechanical connectivity between cells, but how genes modify mechanical interactions between layers is unknown. Here we show that genes driving brassinosteroid synthesis promote growth of internal tissue, at least in part, by reducing mechanical epidermal constraint. We identified a brassinosteroid-deficient dwarf mutant in the aquatic plant Utricularia gibba with twisted internal tissue, likely caused by mechanical constraint from a slow-growing epidermis. We tested this hypothesis by showing that a brassinosteroid mutant in Arabidopsis enhances epidermal crack formation, indicative of increased tissue stress. We propose that by remodeling cell walls, brassinosteroids reduce epidermal constraint, showing how genes can control growth coordination between layers by means of mechanics.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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