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, Zhenbiao Yang

Research output: Contribution to journalArticlepeer-review

16 Scopus citations

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.

Original languageEnglish (US)
Pages (from-to)278-282
Number of pages5
JournalNature
Volume599
Issue number7884
DOIs
StatePublished - Nov 11 2021

Bibliographical note

Funding Information:
Acknowledgemacents We thank the members of the Yang laboratory for discussion and comments on this work; J. Leung (Department of Institute Jean-Pierre Bourgin, INRA) for ost2-2D seeds; K. Iba (Kyushu University) for 35S::GFP-AHA1 seeds; C. Grefen (University of Tubingen) for FRET analyses 2in1 binary vectors; and L. Shan (University of Texas A&M) for protoplast transient expression vectors. This work was in part supported by an NIH grant (GM100130) to Z.Y.; K.T. (20K06685) and T.K. (20H05687 and 20H05910) were funded by MEXT/ JSPS KAKENHI. W.M.G. was funded by NIH (GM067203). H.Z. was funded by NIH (S10OD016400).

Publisher Copyright:
© 2021, The Author(s).

PubMed: MeSH publication types

  • Journal Article
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

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