A Complex Interplay of Three R2R3 MYB Transcription Factors Determines the Profile of Aliphatic Glucosinolates in Arabidopsis

Overview

Journal Plant Physiol

Specialty Physiology

Date 2010 Mar 30

PMID 20348214

Citations 101

Authors

Ida Elken Sonderby

Meike Burow

Heather C Rowe

Daniel J Kliebenstein

Barbara Ann Halkier

Affiliations

Soon will be listed here.

Abstract

While R2R3 MYB transcription factors are a large gene family of transcription factors within plants, comprehensive functional data in planta are still scarce. A model for studying R2R3 MYB control of metabolic networks is the glucosinolates (GLSs), secondary metabolites that control plant resistance against insects and pathogens and carry cancer-preventive properties. Three related members of the R2R3 MYB transcription factor family within Arabidopsis (Arabidopsis thaliana), MYB28, MYB29, and MYB76, are the commonly defined regulators of aliphatic GLS biosynthesis. We utilized new genotypes and systems analysis techniques to test the existing regulatory model in which MYB28 is the dominant regulator, MYB29 plays a minor rheostat role, and MYB76 is largely uninvolved. We unequivocally show that MYB76 is not dependent on MYB28 and MYB29 for induction of aliphatic GLSs and that MYB76 plays a role in determining the spatial distribution of aliphatic GLSs within the leaf, pointing at a potential role of MYB76 in transport regulation. Transcriptional profiling of knockout mutants revealed that GLS metabolite levels are uncoupled from the level of transcript accumulation for aliphatic GLS biosynthetic genes. This uncoupling of chemotypes from biosynthetic transcripts suggests revising our view of the regulation of GLS metabolism from a simple linear transcription factor-promoter model to a more modular system in which transcription factors cause similar chemotypes via nonoverlapping regulatory patterns. Similar regulatory networks might exist in other secondary pathways.

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References

Chen S, Glawischnig E, Jorgensen K, Naur P, JOrgensen B, Olsen C . CYP79F1 and CYP79F2 have distinct functions in the biosynthesis of aliphatic glucosinolates in Arabidopsis. Plant J. 2003; 33(5):923-37. DOI: 10.1046/j.1365-313x.2003.01679.x. View

Gigolashvili T, Yatusevich R, Rollwitz I, Humphry M, Gershenzon J, Flugge U . The plastidic bile acid transporter 5 is required for the biosynthesis of methionine-derived glucosinolates in Arabidopsis thaliana. Plant Cell. 2009; 21(6):1813-29. PMC: 2714935. DOI: 10.1105/tpc.109.066399. View

Levy M, Wang Q, Kaspi R, Parrella M, Abel S . Arabidopsis IQD1, a novel calmodulin-binding nuclear protein, stimulates glucosinolate accumulation and plant defense. Plant J. 2005; 43(1):79-96. DOI: 10.1111/j.1365-313X.2005.02435.x. View

Maruyama-Nakashita A, Nakamura Y, Tohge T, Saito K, Takahashi H . Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell. 2006; 18(11):3235-51. PMC: 1693955. DOI: 10.1105/tpc.106.046458. View

Irizarry R, Hobbs B, Collin F, Beazer-Barclay Y, Antonellis K, Scherf U . Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003; 4(2):249-64. DOI: 10.1093/biostatistics/4.2.249. View

Schuster J, Binder S . The mitochondrial branched-chain aminotransferase (AtBCAT-1) is capable to initiate degradation of leucine, isoleucine and valine in almost all tissues in Arabidopsis thaliana. Plant Mol Biol. 2005; 57(2):241-54. DOI: 10.1007/s11103-004-7533-1. View

Sawada Y, Toyooka K, Kuwahara A, Sakata A, Nagano M, Saito K . Arabidopsis bile acid:sodium symporter family protein 5 is involved in methionine-derived glucosinolate biosynthesis. Plant Cell Physiol. 2009; 50(9):1579-86. PMC: 2739670. DOI: 10.1093/pcp/pcp110. View

Hirai M, Sugiyama K, Sawada Y, Tohge T, Obayashi T, Suzuki A . Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc Natl Acad Sci U S A. 2007; 104(15):6478-83. PMC: 1849962. DOI: 10.1073/pnas.0611629104. View

Falk K, Tokuhisa J, Gershenzon J . The effect of sulfur nutrition on plant glucosinolate content: physiology and molecular mechanisms. Plant Biol (Stuttg). 2007; 9(5):573-81. DOI: 10.1055/s-2007-965431. View

10.

Brown P, Tokuhisa J, Reichelt M, Gershenzon J . Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry. 2003; 62(3):471-81. DOI: 10.1016/s0031-9422(02)00549-6. View

11.

Bednarek P, Pislewska-Bednarek M, Svatos A, Schneider B, Doubsky J, Mansurova M . A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science. 2008; 323(5910):101-6. DOI: 10.1126/science.1163732. View

12.

Kliebenstein D, Lambrix V, Reichelt M, Gershenzon J, Mitchell-Olds T . Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate-dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. Plant Cell. 2001; 13(3):681-93. PMC: 135509. DOI: 10.1105/tpc.13.3.681. View

13.

Dare A, Schaffer R, Lin-Wang K, Allan A, Hellens R . Identification of a cis-regulatory element by transient analysis of co-ordinately regulated genes. Plant Methods. 2008; 4:17. PMC: 2491621. DOI: 10.1186/1746-4811-4-17. View

14.

Gigolashvili T, Engqvist M, Yatusevich R, Muller C, Flugge U . HAG2/MYB76 and HAG3/MYB29 exert a specific and coordinated control on the regulation of aliphatic glucosinolate biosynthesis in Arabidopsis thaliana. New Phytol. 2007; 177(3):627-642. DOI: 10.1111/j.1469-8137.2007.02295.x. View

15.

Juge N, Mithen R, Traka M . Molecular basis for chemoprevention by sulforaphane: a comprehensive review. Cell Mol Life Sci. 2007; 64(9):1105-27. PMC: 11136334. DOI: 10.1007/s00018-007-6484-5. View

16.

Grotewold E . Transcription factors for predictive plant metabolic engineering: are we there yet?. Curr Opin Biotechnol. 2008; 19(2):138-44. DOI: 10.1016/j.copbio.2008.02.002. View

17.

Halkier B, Gershenzon J . Biology and biochemistry of glucosinolates. Annu Rev Plant Biol. 2006; 57:303-33. DOI: 10.1146/annurev.arplant.57.032905.105228. View

18.

Reintanz B, Lehnen M, Reichelt M, Gershenzon J, Kowalczyk M, Sandberg G . Bus, a bushy Arabidopsis CYP79F1 knockout mutant with abolished synthesis of short-chain aliphatic glucosinolates. Plant Cell. 2001; 13(2):351-67. PMC: 102247. DOI: 10.1105/tpc.13.2.351. View

19.

Beekwilder J, van Leeuwen W, van Dam N, Bertossi M, Grandi V, Mizzi L . The impact of the absence of aliphatic glucosinolates on insect herbivory in Arabidopsis. PLoS One. 2008; 3(4):e2068. PMC: 2323576. DOI: 10.1371/journal.pone.0002068. View

20.

Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K . Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J. 2007; 50(4):660-77. PMC: 1976380. DOI: 10.1111/j.1365-313X.2007.03078.x. View