Evidence for functional interaction between brassinosteroids and cadmium response in Arabidopsis thaliana

Journal of Experimental Botany

Volumn 63, Issue 3, 2012, Pages 1185-1200

  Villiers, Florent ^a,d   Jourdain, Agnés ^a   Bastien, Olivier ^a   Leonhardt, Nathalie ^b   Fujioka, Shozo ^c   Tichtincky, Gabrielle ^a   Parcy, Franois ^a   Bourguignon, Jacques ^a   Hugouvieux, Véronique ^a  

^a CNRS   (France)

^b IRFM   (France)

^c RIKEN   (Japan)

^d UNIVERSITY OF MARYLAND   (United States)

Author keywords

brassinosteroids; Cadmium; gene expression; transcriptional interaction

Indexed keywords

ARABIDOPSIS PROTEIN; BRASSINOSTEROID; CADMIUM; DIM1 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; BIOLOGY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SEEDLING; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BRASSINOSTEROIDS; CADMIUM; COMPUTATIONAL BIOLOGY; GENE EXPRESSION REGULATION, PLANT; PLANTS, GENETICALLY MODIFIED; SEEDLING;

ARABIDOPSIS THALIANA;

EID: 84856878555     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err335     Document Type: Article

References (71)

1. An C, Mou Z. 2011. Salicylic acid and its function in plant immunity. Journal of Integrative Plant Biology 53, 412-428.
2. Arteca JM, Arteca RN. 2001. Brassinosteroid-induced exaggerated growth in hydroponically grown Arabidopsis plants. Physiologia Plantarum 112, 104-112.
3. Asami T, Mizutani M, Fujioka S, et al. 2001. Selective interaction of triazole derivatives with DWF4, a cytochrome P450 monooxygenase of the brassinosteroid biosynthetic pathway, correlates with brassinosteroid deficiency in planta. Journal of Biological Chemistry 276, 25687-25691.
4. Asami T, Nakano T, Fujioka S. 2005. Plant brassinosteroid hormones. Vitamins and Hormones 72, 479-504.
5. Bari R, Jones JD. 2009. Role of plant hormones in plant defence responses. Plant Molecular Biology 69, 473-488.
6. Berger S. 2002. Jasmonate-related mutants of Arabidopsis as tools for studying stress signaling. Planta 214, 497-504.
7. Byrne C, Divekar SD, Storchan GB, Parodi DA, Martin MB. 2009. Cadmium: a metallohormone? Toxicology and Applied Pharmacology 238, 266-271.
8. Choe S, Dilkes BP, Fujioka S, Takatsuto S, Sakurai A, Feldmann KA. 1998. The DWF4 gene of Arabidopsis encodes a cytochrome P450 that mediates multiple 22alpha-hydroxylation steps in brassinosteroid biosynthesis. The Plant Cell 10, 231-243.
9. Choe S, Dilkes BP, Gregory BD, et al. 1999. The Arabidopsis dwarf1 mutant is defective in the conversion of 24-methylenecholesterol to campesterol in brassinosteroid biosynthesis. Plant Physiology 119, 897-907.
10. Clemens S. 2006a. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88, 1707-1719.
11. Clemens S. 2006b. Evolution and function of phytochelatin synthases. Journal of Plant Physiology 163, 319-332.
12. Clemens S, Kim EJ, Neumann D, Schroeder JI. 1999. Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. Embo Journal 18, 3325-3333.
13. Clouse SD, Sasse JM. 1998. Brassinosteroids: essential regulators of plant growth and development. Annual Review of Plant Physiology and Plant Molecular Biology 49, 427-451.
14. Cobbett C, Goldsbrough P. 2002. Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annual Review of Plant Biology 53, 159-182.
15. Cobbett CS. 2000. Phytochelatins and their roles in heavy metal detoxification. Plant Physiology 123, 825-832.
16. Cobbett CS, May MJ, Howden R, Rolls B. 1998. The glutathione-deficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in gamma-glutamylcysteine synthetase. The Plant Journal 16, 73-78.
17. Connolly EL, Fett JP, Guerinot ML. 2002. Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. The Plant Cell 14, 1347-1357.
18. Courbot M, Willems G, Motte P, Arvidsson S, Roosens N, Saumitou-Laprade P, Verbruggen N. 2007. A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiology 144, 1052-1065.
19. De Michele R, Vurro E, Rigo C, et al. 2009. Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiology 150, 217-228.
20. di Toppi LS, Gabbrielli R. 1999. Response to cadmium in higher plants. Environmental and Experimental Botany 41, 105-130.
21. Divi UK, Krishna P. 2009. Brassinosteroid: a biotechnological target for enhancing crop yield and stress tolerance. Nature Biotechnology 26, 131-136.
22. Ebbs S, Lau I, Ahner B, Kochian L. 2002. Phytochelatin synthesis is not responsible for Cd tolerance in the Zn/Cd hyperaccumulator Thlaspi caerulescens (J. & C. Presl). Planta 214, 635-640.
23. Fagioni M, D'Amici GM, Timperio AM, Zolla L. 2009. Proteomic analysis of multiprotein complexes in the thylakoid membrane upon cadmium treatment. Journal of Proteome Research 8, 310-326.
24. Fujioka S, Takatsuto S, Yoshida S. 2002. An early C-22 oxidation branch in the brassinosteroid biosynthetic pathway. Plant Physiology 130, 930-939.
25. Gill SS, Tuteja N. 2010. Polyamines and abiotic stress tolerance in plants. Plant Signaling and Behavior 5, 26-33.
26. Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S. 2002. Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiology 130, 1319-1334.
27. Gosti F, Bertauche N, Vartanian N, Giraudat J. 1995. Abscisic acid-dependent and-independent regulation of gene expression by progressive drought in Arabidopsis thaliana. Molecular and General Genetics 246, 10-18.
28. Ha SB, Smith AP, Howden R, Dietrich WM, Bugg S, O'Connell MJ, Goldsbrough PB, Cobbett CS. 1999. Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. The Plant Cell 11, 1153-1164.
29. Hayat S, Ali B, Hasan SA, Ahmad A. 2007. Brassinosteroid enhanced the level of antioxidants under cadmium stress in Brassica juncea. Environmental and Experimental Botany 60, 33-41.
30. Hayat S, Hasan SA, Hayat Q, Ahmad A. 2010. Brassinosteroids protect Lycopersicon esculentum from cadmium toxicity applied as shotgun approach. Protoplasma 239, 3-14.
31. Hasan SA, Hayat S, Ahmad A. 2011. Brassinosteroids protect photosynthetic machinery against the cadmium induced oxidative stress in two tomato cultivars. Chemosphere (in press).
32. He JX, Gendron JM, Sun Y, Gampala SS, Gendron N, Sun CQ, Wang ZY. 2005. BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307, 1634-1638.
33. Herbette S, Taconnat L, Hugouvieux V, et al. 2006. Genome-wide transcriptome profiling of the early cadmium response of Arabidopsis roots and shoots. Biochimie 88, 1751-1765.
34. Howden R, Goldsbrough PB, Andersen CR, Cobbett CS. 1995. Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. Plant Physiology 107, 1059-1066.
35. Hugouvieux V, Dutilleul C, Jourdain A, Reynaud F, Lopez V, Bourguignon J. 2009. Arabidopsis putative selenium-binding protein1 expression is tightly linked to cellular sulfur demand and can reduce sensitivity to stresses requiring glutathione for tolerance. Plant Physiology 151, 768-781.
36. Ishihara T, Kobayashi E, Okubo Y, Suwazono Y, Kido T, Nishijyo M, Nakagawa H, Nogawa K. 2001. Association between cadmium concentration in rice and mortality in the Jinzu River basin, Japan. Toxicology 163, 23-28.
37. Kagale S, Divi UK, Krochko JE, Keller WA, Krishna P. 2007. Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta 225, 353-364.
38. Kim HB, Kwon M, Ryu H, Fujioka S, Takatsuto S, Yoshida S, An CS, Lee I, Hwang I, Choe S. 2006. The regulation of DWARF4 expression is likely a critical mechanism in maintaining the homeostasis of bioactive brassinosteroids in Arabidopsis. Plant Physiology 140, 548-557.
39. Kim TW, Wang ZY. 2010. Brassinosteroid signal transduction from receptor kinases to transcription factors. Annual Review of Plant Biology 61, 681-704.
40. Klahre U, Noguchi T, Fujioka S, Takatsuto S, Yokota T, Nomura T, Yoshida S, Chua NH. 1998. The Arabidopsis DIMINUTO/DWARF1 gene encodes a protein involved in steroid synthesis. The Plant Cell 10, 1677-1690.
41. Krishna P. 2003. Brassinosteroid-mediated stress responses. Journal of Plant Growth Regulation 22, 289-297.
42. Li J, Chory J. 1997. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90, 929-938.
43. Makandar R, Nalam V, Chaturvedi R, Jeannotte R, Sparks AA, Shah J. 2010. Involvement of salicylate and jasmonate signaling pathways in Arabidopsis interaction with Fusarium graminearum. Molecular Plant-Microbe Interactions 23, 861-870.
44. Manly BF. 1997. Randomization, bootstrap and Monte Carlo methods in biology, 2nd edn. New-York: Chapman & Hall/CRC Press.
45. Mathur J, Molnar G, Fujioka S, et al. 1998. Transcription of the Arabidopsis CPD gene, encoding a steroidogenic cytochrome P450, is negatively controlled by brassinosteroids. The Plant Journal 14, 593-602.
46. Mussig C, Fischer S, Altmann T. 2002. Brassinosteroid-regulated gene expression. Plant Physiology 129, 1241-1251.
47. Papoyan A, Kochian LV. 2004. Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiology 136, 3814-3823.
48. Perfus-Barbeoch L, Leonhardt N, Vavasseur A, Forestier C. 2002. Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. The Plant Journal 32, 539-548.
49. Pietrini F, Iannelli MA, Pasqualini S, Massacci A. 2003. Interaction of cadmium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis (Cav.) Trin. ex steudel. Plant Physiology 133, 829-837.
50. Rodriguez-Serrano M, Romero-Puertas MC, Pazmino DM, Testillano PS, Risueno MC, Del Rio LA, Sandalio LM. 2009. Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiology 150, 229-243.
51. Romanyuk ND, Rigden DJ, Vatamaniuk OK, Lang A, Cahoon RE, Jez JM, Rea PA. 2006. Mutagenic definition of a papain-like catalytic triad, sufficiency of the N-terminal domain for single-site core catalytic enzyme acylation, and C-terminal domain for augmentative metal activation of a eukaryotic phytochelatin synthase. Plant Physiology 141, 858-869.
52. Salt DE, Rauser WE. 1995. MgATP-dependent transport of phytochelatins across the tonoplast of oat roots. Plant Physiology 107, 1293-1301.
53. Sarry JE, Kuhn L, Ducruix C, et al. 2006. The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics 6, 2180-2198.
54. Sauge-Merle S, Cuine S, Carrier P, Lecomte-Pradines C, Luu DT, Peltier G. 2003. Enhanced toxic metal accumulation in engineered bacterial cells expressing Arabidopsis thaliana phytochelatin synthase. Applied Environmental Microbiology 69, 490-494.
55. Schaaf G, Honsbein A, Meda AR, Kirchner S, Wipf D, von Wiren N. 2006. AtIREG2 encodes a tonoplast transport protein involved in iron-dependent nickel detoxification in Arabidopsis thaliana roots. Journal of Biological Chemistry 281, 25532-25540.
56. Steffens JC, Hunt DF, Williams BG. 1986. Accumulation of non-protein metal-binding polypeptides (c-glutamyl-cysteinyl)n-glycine in selected cadmium-resistant tomato cells. Journal of Biological Chemistry 261, 13879-13882.
57. Sun Y, Fan XY, Cao DM, et al. 2010. Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Developmental Cell 19, 765-777.
58. Tamaoki M, Freeman JL, Pilon-Smits EA. 2008. Cooperative ethylene and jasmonic acid signaling regulates selenite resistance in Arabidopsis. Plant Physiology 146, 1219-1230.
59. Tanaka K, Asami T, Yoshida S, Nakamura Y, Matsuo T, Okamoto S. 2005. Brassinosteroid homeostasis in Arabidopsis is ensured by feedback expressions of multiple genes involved in its metabolism. Plant Physiology 138, 1117-1125.
60. Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI. 2000. Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proceedings of the National Academy of Sciences, USA 97, 4991-4996.
61. Vatamaniuk OK, Mari S, Lu YP, Rea PA. 1999. AtPCS1, a phytochelatin synthase from Arabidopsis: isolation and in vitro reconstitution. Proceedings of the National Academy of Sciences, USA 96, 7110-7115.
62. Vatamaniuk OK, Mari S, Lu YP, Rea PA. 2000. Mechanism of heavy metal ion activation of phytochelatin (PC) synthase: blocked thiols are sufficient for PC synthase-catalyzed transpeptidation of glutathione and related thiol peptides. Journal of Biological Chemistry 275, 31451-31459.
63. Verkleij JAC, Van Hoof NALM, Chardonnens AN, Koevoets PLM, Hakvoort H, ten Bookum WM, Schat H, Ernst WHO. 2001. Mechansims of heavy metal resistance in Silene vulgaris. In: Plant nutrition. Netherlands: Springer, 446-447.
64. Vijayan P, Shockey J, Levesque CA, Cook RJ, Browse J. 1998. A role for jasmonate in pathogen defense of Arabidopsis. Proceedings of the National Academy of Sciences, USA 95, 7209-7214.
65. Vogeli-Lange R, Wagner GJ. 1990. Subcellular localization of cadmium and cadmium-binding peptides in tobacco leaves: implication of a transport function for cadmium-binding peptides. Plant Physiology 92, 1086-1093.
66. Weber M, Trampczynska A, Clemens S. 2006. Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2+-hypertolerant facultative metallophyte Arabidopsis halleri. Plant, Cell and Environment 29, 950-963.
67. Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Asami T, Chen Z, Yu JQ. 2009. Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiology 150, 801-814.
68. Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. 2010. AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. The Plant Journal 61, 672-685.
69. Yu X, Li L, Zola J, et al. 2011. A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. The Plant Journal 65, 634-646.
70. Yusuf M, Fariduddin Q, Hayat S, Hasan SA, Ahmad A. 2011. Protective response of 28-homobrassinolide in cultivars of Triticum aestivum with different levels of nickel. Archives of Environmental Contamination and Toxicology 60, 68-76.
71. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W. 2004. GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiology 136, 2621-2632.