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TMK-based cell-surface auxin signalling activates cell-wall acidification

Wenwei Lin, Xiang Zhou, Wenxin Tang, Koji Takahashi, Xue Pan, Jiawei Dai, Hong Ren, Xiaoyue Zhu, Songqin Pan, Haiyan Zheng, William M. Gray, Tongda Xu, Toshinori Kinoshita and Zhenbiao Yang ()
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Wenwei Lin: Fujian Agriculture and Forestry University
Xiang Zhou: Fujian Agriculture and Forestry University
Wenxin Tang: Fujian Agriculture and Forestry University
Koji Takahashi: Nagoya University
Xue Pan: University of California
Jiawei Dai: Fujian Agriculture and Forestry University
Hong Ren: University of Minnesota
Xiaoyue Zhu: Fujian Agriculture and Forestry University
Songqin Pan: University of California
Haiyan Zheng: the State University of New Jersey
William M. Gray: University of Minnesota
Tongda Xu: Fujian Agriculture and Forestry University
Toshinori Kinoshita: Nagoya University
Zhenbiao Yang: Fujian Agriculture and Forestry University

Nature, 2021, vol. 599, issue 7884, 278-282

Abstract: Abstract The phytohormone auxin controls many processes in plants, at least in part through its regulation of cell expansion1. The acid growth hypothesis has been proposed to explain auxin-stimulated cell expansion for five decades, but the mechanism that underlies auxin-induced cell-wall acidification is poorly characterized. Auxin induces the phosphorylation and activation of the plasma membrane H+-ATPase that pumps protons into the apoplast2, yet how auxin activates its phosphorylation remains unclear. Here we show that the transmembrane kinase (TMK) auxin-signalling proteins interact with plasma membrane H+-ATPases, inducing their phosphorylation, and thereby promoting cell-wall acidification and hypocotyl cell elongation in Arabidopsis. Auxin induced interactions between TMKs and H+-ATPases in the plasma membrane within seconds, as well as TMK-dependent phosphorylation of the penultimate threonine residue on the H+-ATPases. Our genetic, biochemical and molecular evidence demonstrates that TMKs directly phosphorylate plasma membrane H+-ATPase and are required for auxin-induced H+-ATPase activation, apoplastic acidification and cell expansion. Thus, our findings reveal a crucial connection between auxin and plasma membrane H+-ATPase activation in regulating apoplastic pH changes and cell expansion through TMK-based cell surface auxin signalling.

Date: 2021
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DOI: 10.1038/s41586-021-03976-4

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