The Modified Flavonol Glycosylation Profile in the Arabidopsis Rol1 Mutants Results in Alterations in Plant Growth and Cell Shape Formation

Overview

Journal Plant Cell

Publisher Oxford University Press

Specialties Biology
Cell Biology

Date 2008 Jun 24

PMID 18567791

Citations 43

Authors

Christoph Ringli

Laurent Bigler

Benjamin M Kuhn

Ruth-Maria Leiber

Anouck Diet

Diana Santelia

Beat Frey

Stephan Pollmann

Markus Klein

Affiliations

Soon will be listed here.

Abstract

Flavonoids are secondary metabolites known to modulate plant growth and development. A primary function of flavonols, a subgroup of flavonoids, is thought to be the modification of auxin fluxes in the plant. Flavonols in the cell are glycosylated, and the repressor of lrx1 (rol1) mutants of Arabidopsis thaliana, affected in rhamnose biosynthesis, have a modified flavonol glycosylation profile. A detailed analysis of the rol1-2 allele revealed hyponastic growth, aberrant pavement cell and stomatal morphology in cotyledons, and defective trichome formation. Blocking flavonoid biosynthesis suppresses the rol1-2 shoot phenotype, suggesting that it is induced by the modified flavonol profile. The hyponastic cotyledons of rol1-2 are likely to be the result of a flavonol-induced increase in auxin concentration. By contrast, the pavement cell, stomata, and trichome formation phenotypes appear not to be induced by the modified auxin distribution. Together, these results suggest that changes in the composition of flavonols can have a tremendous impact on plant development through both auxin-induced and auxin-independent processes.

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References

Mathur J, Mathur N, Kernebeck B, Hulskamp M . Mutations in actin-related proteins 2 and 3 affect cell shape development in Arabidopsis. Plant Cell. 2003; 15(7):1632-45. PMC: 165406. DOI: 10.1105/tpc.011676. View

Diet A, Link B, Seifert G, Schellenberg B, Wagner U, Pauly M . The Arabidopsis root hair cell wall formation mutant lrx1 is suppressed by mutations in the RHM1 gene encoding a UDP-L-rhamnose synthase. Plant Cell. 2006; 18(7):1630-41. PMC: 1488927. DOI: 10.1105/tpc.105.038653. View

Peer W, Bandyopadhyay A, Blakeslee J, Makam S, Chen R, Masson P . Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. Plant Cell. 2004; 16(7):1898-911. PMC: 514169. DOI: 10.1105/tpc.021501. View

Murphy A, Hoogner K, Peer W, Taiz L . Identification, purification, and molecular cloning of N-1-naphthylphthalmic acid-binding plasma membrane-associated aminopeptidases from Arabidopsis. Plant Physiol. 2002; 128(3):935-50. PMC: 152206. DOI: 10.1104/pp.010519. View

Laxmi A, Paul L, Raychaudhuri A, Peters J, Khurana J . Arabidopsis cytokinin-resistant mutant, cnr1, displays altered auxin responses and sugar sensitivity. Plant Mol Biol. 2006; 62(3):409-25. DOI: 10.1007/s11103-006-9032-z. View

Frank M, Cartwright H, Smith L . Three Brick genes have distinct functions in a common pathway promoting polarized cell division and cell morphogenesis in the maize leaf epidermis. Development. 2002; 130(4):753-62. DOI: 10.1242/dev.00290. View

Shirley B, Kubasek W, Storz G, Bruggemann E, Koornneef M, Ausubel F . Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. Plant J. 1995; 8(5):659-71. DOI: 10.1046/j.1365-313x.1995.08050659.x. View

Debeaujon I, Nesi N, Perez P, Devic M, Grandjean O, Caboche M . Proanthocyanidin-accumulating cells in Arabidopsis testa: regulation of differentiation and role in seed development. Plant Cell. 2003; 15(11):2514-31. PMC: 280558. DOI: 10.1105/tpc.014043. View

Ridley B, ONeill M, Mohnen D . Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry. 2001; 57(6):929-67. DOI: 10.1016/s0031-9422(01)00113-3. View

10.

Ulmasov T, Murfett J, Hagen G, Guilfoyle T . Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell. 1997; 9(11):1963-71. PMC: 157050. DOI: 10.1105/tpc.9.11.1963. View

11.

Baumberger N, Ringli C, Keller B . The chimeric leucine-rich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana. Genes Dev. 2001; 15(9):1128-39. PMC: 312681. DOI: 10.1101/gad.200201. View

12.

Williamson R, Burn J, Birch R, Baskin T, Arioli T, Betzner A . Morphology of rsw1, a cellulose-deficient mutant of Arabidopsis thaliana. Protoplasma. 2001; 215(1-4):116-27. DOI: 10.1007/BF01280308. View

13.

Watahiki M, Yamamoto K . The massugu1 mutation of Arabidopsis identified with failure of auxin-induced growth curvature of hypocotyl confers auxin insensitivity to hypocotyl and leaf. Plant Physiol. 1997; 115(2):419-26. PMC: 158499. DOI: 10.1104/pp.115.2.419. View

14.

Kerhoas L, Aouak D, Cingoz A, Routaboul J, Lepiniec L, Einhorn J . Structural characterization of the major flavonoid glycosides from Arabidopsis thaliana seeds. J Agric Food Chem. 2006; 54(18):6603-12. DOI: 10.1021/jf061043n. View

15.

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

16.

Mo Y, Nagel C, Taylor L . Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. Proc Natl Acad Sci U S A. 1992; 89(15):7213-7. PMC: 49676. DOI: 10.1073/pnas.89.15.7213. View

17.

Lepiniec L, Debeaujon I, Routaboul J, Baudry A, Pourcel L, Nesi N . Genetics and biochemistry of seed flavonoids. Annu Rev Plant Biol. 2006; 57:405-30. DOI: 10.1146/annurev.arplant.57.032905.105252. View

18.

Chary S, Hicks G, Choi Y, Carter D, Raikhel N . Trehalose-6-phosphate synthase/phosphatase regulates cell shape and plant architecture in Arabidopsis. Plant Physiol. 2007; 146(1):97-107. PMC: 2230562. DOI: 10.1104/pp.107.107441. View

19.

Smith L . Cytoskeletal control of plant cell shape: getting the fine points. Curr Opin Plant Biol. 2002; 6(1):63-73. DOI: 10.1016/s1369-5266(02)00012-2. View

20.

Carpita N, Gibeaut D . Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J. 1993; 3(1):1-30. DOI: 10.1111/j.1365-313x.1993.tb00007.x. View