Canalization of Auxin Flow by Aux/IAA-ARF-dependent Feedback Regulation of PIN Polarity

Overview

Journal Genes Dev

Specialty Molecular Biology

Date 2006 Oct 18

PMID 17043314

Citations 179

Authors

Michael Sauer

Jozef Balla

Christian Luschnig

Justyna Wisniewska

Vilem Reinohl

Jiri Friml

Eva Benkova

Affiliations

Soon will be listed here.

Abstract

Plant development is characterized by a profound ability to regenerate and form tissues with new axes of polarity. An unsolved question concerns how the position within a tissue and cues from neighboring cells are integrated to specify the polarity of individual cells. The canalization hypothesis proposes a feedback effect of the phytohormone auxin on the directionality of intercellular auxin flow as a means to polarize tissues. Here we identify a cellular and molecular mechanism for canalization. Local auxin application, wounding, or auxin accumulation during de novo organ formation lead to rearrangements in the subcellular polar localization of PIN auxin transport components. This auxin effect on PIN polarity is cell-specific, does not depend on PIN transcription, and involves the Aux/IAA-ARF (indole-3-acetic acid-auxin response factor) signaling pathway. Our data suggest that auxin acts as polarizing cue, which links individual cell polarity with tissue and organ polarity through control of PIN polar targeting. This feedback regulation provides a conceptual framework for polarization during multiple regenerative and patterning processes in plants.

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References

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

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

Vieten A, Vanneste S, Wisniewska J, Benkova E, Benjamins R, Beeckman T . Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development. 2005; 132(20):4521-31. DOI: 10.1242/dev.02027. View

Heisler M, Ohno C, Das P, Sieber P, Reddy G, Long J . Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol. 2005; 15(21):1899-911. DOI: 10.1016/j.cub.2005.09.052. View

Xu J, Hofhuis H, Heidstra R, Sauer M, Friml J, Scheres B . A molecular framework for plant regeneration. Science. 2006; 311(5759):385-8. DOI: 10.1126/science.1121790. View

Jonsson H, Heisler M, Shapiro B, Meyerowitz E, Mjolsness E . An auxin-driven polarized transport model for phyllotaxis. Proc Natl Acad Sci U S A. 2006; 103(5):1633-8. PMC: 1326488. DOI: 10.1073/pnas.0509839103. View

Smith R, Guyomarch S, Mandel T, Reinhardt D, Kuhlemeier C, Prusinkiewicz P . A plausible model of phyllotaxis. Proc Natl Acad Sci U S A. 2006; 103(5):1301-6. PMC: 1345713. DOI: 10.1073/pnas.0510457103. View

Barbier de Reuille P, Bohn-Courseau I, Ljung K, Morin H, Carraro N, Godin C . Computer simulations reveal properties of the cell-cell signaling network at the shoot apex in Arabidopsis. Proc Natl Acad Sci U S A. 2006; 103(5):1627-32. PMC: 1360567. DOI: 10.1073/pnas.0510130103. View

Abas L, Benjamins R, Malenica N, Paciorek T, Wisniewska J, Wirniewska J . Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol. 2006; 8(3):249-56. DOI: 10.1038/ncb1369. View

10.

Parry G, Estelle M . Auxin receptors: a new role for F-box proteins. Curr Opin Cell Biol. 2006; 18(2):152-6. DOI: 10.1016/j.ceb.2006.02.001. View

11.

Scarpella E, Marcos D, Friml J, Berleth T . Control of leaf vascular patterning by polar auxin transport. Genes Dev. 2006; 20(8):1015-27. PMC: 1472298. DOI: 10.1101/gad.1402406. View

12.

Petrasek J, Mravec J, Bouchard R, Blakeslee J, Abas M, Seifertova D . PIN proteins perform a rate-limiting function in cellular auxin efflux. Science. 2006; 312(5775):914-8. DOI: 10.1126/science.1123542. View

13.

Wisniewska J, Xu J, Seifertova D, Brewer P, Ruzicka K, Blilou I . Polar PIN localization directs auxin flow in plants. Science. 2006; 312(5775):883. DOI: 10.1126/science.1121356. View

14.

Benjamins R, Quint A, Weijers D, Hooykaas P, Offringa R . The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development. 2001; 128(20):4057-67. DOI: 10.1242/dev.128.20.4057. View

15.

Christensen S, Dagenais N, Chory J, Weigel D . Regulation of auxin response by the protein kinase PINOID. Cell. 2000; 100(4):469-78. DOI: 10.1016/s0092-8674(00)80682-0. View

16.

Reinhardt D, Mandel T, Kuhlemeier C . Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell. 2000; 12(4):507-18. PMC: 139849. DOI: 10.1105/tpc.12.4.507. View

17.

Koizumi K, Sugiyama M, Fukuda H . A series of novel mutants of Arabidopsis thaliana that are defective in the formation of continuous vascular network: calling the auxin signal flow canalization hypothesis into question. Development. 2000; 127(15):3197-204. DOI: 10.1242/dev.127.15.3197. View

18.

Sieberer T, Seifert G, Hauser M, GRISAFI P, Fink G, Luschnig C . Post-transcriptional control of the Arabidopsis auxin efflux carrier EIR1 requires AXR1. Curr Biol. 2001; 10(24):1595-8. DOI: 10.1016/s0960-9822(00)00861-7. View

19.

Morris D . Transmembrane auxin carrier systems--dynamic regulators of polar auxin transport. Plant Growth Regul. 2002; 32(2-3):161-72. DOI: 10.1023/a:1010701527848. View

20.

Fukaki H, Tameda S, Masuda H, Tasaka M . Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J. 2002; 29(2):153-68. DOI: 10.1046/j.0960-7412.2001.01201.x. View