Uniform Auxin Triggers the Rho GTPase-dependent Formation of Interdigitation Patterns in Pavement Cells

Overview

Journal Small GTPases

Specialties Biochemistry
Cell Biology

Date 2011 Dec 7

PMID 22145096

Citations 14

Authors

Tongda Xu

Shingo Nagawa

Zhenbiao Yang

Affiliations

Soon will be listed here.

Abstract

The investigation of Rho-family GTPases has uncovered mechanisms for spatiotemporal control of cellular processes such as cell polarization, movement, morphogenesis and cell division. Now Rho GTPase plays another leading role in the discovery of a new signaling mechanism for auxin, a multifunctional hormone that regulates pattern formation in plants. Arabidopsis leaf epidermal pavement cells (PCs) develop the puzzle-piece cell shape with interlocking lobes and indentations via interdigitated cellular growth.1 Through the ABP1 (Auxin Binding Protein 1) cell surface receptor, auxin coordinately activates 2 mutually exclusive Rho GTPase signaling pathways that are activated in the complementary lobing and indenting sides of adjacent cells: the ROP2 pathway for lobe formation and the ROP6 pathway for promoting indentation. This new signaling mechanism also involves ROP2-dependent polar accumulation of PIN1 in the plasma membrane, a member of the PIN auxin efflux carrier family that is critical for the formation of various developmental patterns including the PC interdigitation pattern. This Rho-dependent auxin signaling mechanism explains how interdigitated cellular growth is coordinated. In this extra view, we propose that the same mechanism can also explain how a uniform auxin signal initiates the formation of the interdigitated pattern.

Citing Articles

Mechano-chemical regulation of complex cell shape formation: Epidermal pavement cells-A case study.

van Spoordonk R, Schneider R, Sampathkumar A Quant Plant Biol. 2023; 4:e5.

PMID: 37251797 PMC: 10225270. DOI: 10.1017/qpb.2023.4.

Auxin and Target of Rapamycin Spatiotemporally Regulate Root Organogenesis.

Xie X, Wang Y, Datla R, Ren M Int J Mol Sci. 2021; 22(21).

PMID: 34768785 PMC: 8583787. DOI: 10.3390/ijms222111357.

Auxin-induced actin cytoskeleton rearrangements require AUX1.

Arieti R, Staiger C New Phytol. 2019; 226(2):441-459.

PMID: 31859367 PMC: 7154765. DOI: 10.1111/nph.16382.

Calcium: The Missing Link in Auxin Action.

Vanneste S, Friml J Plants (Basel). 2016; 2(4):650-75.

PMID: 27137397 PMC: 4844386. DOI: 10.3390/plants2040650.

Pavement cells: a model system for non-transcriptional auxin signalling and crosstalks.

Chen J, Wang F, Zheng S, Xu T, Yang Z J Exp Bot. 2015; 66(16):4957-70.

PMID: 26047974 PMC: 4598803. DOI: 10.1093/jxb/erv266.

References

Thiel G, Blatt M, Fricker M, White I, Millner P . Modulation of K+ channels in Vicia stomatal guard cells by peptide homologs to the auxin-binding protein C terminus. Proc Natl Acad Sci U S A. 1993; 90(24):11493-7. PMC: 48010. DOI: 10.1073/pnas.90.24.11493. View

Hertel R, Thomson K, Russo V . In-vitro auxin binding to particulate cell fractions from corn coleoptiles. Planta. 2014; 107(4):325-40. DOI: 10.1007/BF00386394. View

Chapman E, Estelle M . Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet. 2009; 43:265-85. DOI: 10.1146/annurev-genet-102108-134148. View

Calderon-Villalobos L, Tan X, Zheng N, Estelle M . Auxin perception--structural insights. Cold Spring Harb Perspect Biol. 2010; 2(7):a005546. PMC: 2890193. DOI: 10.1101/cshperspect.a005546. View

Hazak O, Bloch D, Poraty L, Sternberg H, Zhang J, Friml J . A rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution. PLoS Biol. 2010; 8(1):e1000282. PMC: 2808208. DOI: 10.1371/journal.pbio.1000282. View

Shimomura S . Identification of a glycosylphosphatidylinositol-anchored plasma membrane protein interacting with the C-terminus of auxin-binding protein 1: a photoaffinity crosslinking study. Plant Mol Biol. 2006; 60(5):663-77. DOI: 10.1007/s11103-005-5471-1. View

Xu J, Wang F, Van Keymeulen A, Herzmark P, Straight A, Kelly K . Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell. 2003; 114(2):201-14. DOI: 10.1016/s0092-8674(03)00555-5. View

Wartlick O, Kicheva A, Gonzalez-Gaitan M . Morphogen gradient formation. Cold Spring Harb Perspect Biol. 2010; 1(3):a001255. PMC: 2773637. DOI: 10.1101/cshperspect.a001255. View

Badescu G, Napier R . Receptors for auxin: will it all end in TIRs?. Trends Plant Sci. 2006; 11(5):217-23. DOI: 10.1016/j.tplants.2006.03.001. View

10.

Tromas A, Braun N, Muller P, Khodus T, Paponov I, Palme K . The AUXIN BINDING PROTEIN 1 is required for differential auxin responses mediating root growth. PLoS One. 2009; 4(9):e6648. PMC: 2744284. DOI: 10.1371/journal.pone.0006648. View

11.

Chen J, Ullah H, Young J, Sussman M, Jones A . ABP1 is required for organized cell elongation and division in Arabidopsis embryogenesis. Genes Dev. 2001; 15(7):902-11. PMC: 312669. DOI: 10.1101/gad.866201. View

12.

Li L, Xu J, Xu Z, Xue H . Brassinosteroids stimulate plant tropisms through modulation of polar auxin transport in Brassica and Arabidopsis. Plant Cell. 2005; 17(10):2738-53. PMC: 1242269. DOI: 10.1105/tpc.105.034397. View

13.

Jones A, Herman E . KDEL-Containing Auxin-Binding Protein Is Secreted to the Plasma Membrane and Cell Wall. Plant Physiol. 1993; 101(2):595-606. PMC: 160609. DOI: 10.1104/pp.101.2.595. View

14.

Fu Y, Gu Y, Zheng Z, Wasteneys G, Yang Z . Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell. 2005; 120(5):687-700. DOI: 10.1016/j.cell.2004.12.026. View

15.

Paciorek T, Zazimalova E, Ruthardt N, Petrasek J, Stierhof Y, Kleine-Vehn J . Auxin inhibits endocytosis and promotes its own efflux from cells. Nature. 2005; 435(7046):1251-6. DOI: 10.1038/nature03633. View

16.

Yamagami M, Haga K, Napier R, Iino M . Two distinct signaling pathways participate in auxin-induced swelling of pea epidermal protoplasts. Plant Physiol. 2004; 134(2):735-47. PMC: 344549. DOI: 10.1104/pp.103.031294. View

17.

Wu H, Hazak O, Cheung A, Yalovsky S . RAC/ROP GTPases and auxin signaling. Plant Cell. 2011; 23(4):1208-18. PMC: 3101531. DOI: 10.1105/tpc.111.083907. View

18.

Braun N, Wyrzykowska J, Muller P, David K, Couch D, Perrot-Rechenmann C . Conditional repression of AUXIN BINDING PROTEIN1 reveals that it coordinates cell division and cell expansion during postembryonic shoot development in Arabidopsis and tobacco. Plant Cell. 2008; 20(10):2746-62. PMC: 2590743. DOI: 10.1105/tpc.108.059048. View

19.

Bauly J, Sealy I, Macdonald H, Brearley J, Droge S, Hillmer S . Overexpression of auxin-binding protein enhances the sensitivity of guard cells to auxin. Plant Physiol. 2000; 124(3):1229-38. PMC: 59221. DOI: 10.1104/pp.124.3.1229. View

20.

Reinhardt D . Phyllotaxis--a new chapter in an old tale about beauty and magic numbers. Curr Opin Plant Biol. 2005; 8(5):487-93. DOI: 10.1016/j.pbi.2005.07.012. View