Cell surface- and Rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis

Tongda Xu, Mingzhang Wen, Shingo Nagawa, Ying Fu, Jin Gui Chen, Ming Jing Wu, Catherine Perrot-Rechenmann, Jiří Friml, Alan M. Jones, Zhenbiao Yang

Research output: Contribution to journalArticlepeer-review

385 Scopus citations

Abstract

Auxin is a multifunctional hormone essential for plant development and pattern formation. A nuclear auxin-signaling system controlling auxin-induced gene expression is well established, but cytoplasmic auxin signaling, as in its coordination of cell polarization, is unexplored. We found a cytoplasmic auxin-signaling mechanism that modulates the interdigitated growth of Arabidopsis leaf epidermal pavement cells (PCs), which develop interdigitated lobes and indentations to form a puzzle-piece shape in a two-dimensional plane. PC interdigitation is compromised in leaves deficient in either auxin biosynthesis or its export mediated by PINFORMED 1 localized at the lobe tip. Auxin coordinately activates two Rho GTPases, ROP2 and ROP6, which promote the formation of complementary lobes and indentations, respectively. Activation of these ROPs by auxin occurs within 30 s and depends on AUXIN-BINDING PROTEIN 1. These findings reveal Rho GTPase-based auxin-signaling mechanisms, which modulate the spatial coordination of cell expansion across a field of cells.

Original languageEnglish
Pages (from-to)99-110
Number of pages12
JournalCell
Volume143
Issue number1
DOIs
StatePublished - Oct 2010
Externally publishedYes

Funding

We are grateful to Veronica Grieneisen, Ben Scheres, Athanasius F. M. Marée, Paulien Hogeweg, Xuemei Chen, and G. Venugopala Reddy for their stimulating discussion and critical comments on this manuscript; and to Xinping Cui for her assistance with the statistical analysis. We are grateful to Tom Guilfoyle and Yunde Zhao for their generous supply of Arabidopsis mutant lines used in this work. This work is supported by grants from the U.S. National Institute of General Medical Sciences to Z.Y. (GM081451) and to A.M.J. (GM065989), by the National Science Foundation to A.M.J. (MCB-0718202) and the Department of Energy to A.M.J. (DE-FG02-05ER15671) and to Z.Y. (DE-FG02-04ER15555) and by the Research Foundation-Flanders (Odysseus) to J.F.

Keywords

  • Devbio
  • Signaling

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