Redox modulation of plant developmental regulators from the class I TCP transcription factor family

Plant Physiology

Volumn 162, Issue 3, 2013, Pages 1434-1447

  Viola, Ivana L ^a   Güttlein, Leandro N ^a   Gonzalez, Daniel H ^a  

^a UNIVERSIDAD NACIONAL DEL LITORAL   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; SACCHAROMYCES CEREVISIAE;

EID: 84879733323     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.216416     Document Type: Article

References (71)

1. Aggarwal P, Das Gupta M, Joseph AP, Chatterjee N, Srinivasan N, Nath U (2010) Identification of specific DNA binding residues in the TCP family of transcription factors in Arabidopsis. Plant Cell 22: 1174-1189.
2. Aguilar-Martínez JA, Poza-Carrión C, Cubas P (2007) Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19: 458-472.
3. Bick JA, Setterdahl AT, Knaff DB, Chen Y, Pitcher LH, Zilinskas BA, Leustek T (2001) Regulation of the plant 5'-adenylyl sulfate reductase by oxidative stress. Biochemistry 40: 9040-9048.
4. Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56: 187-220.
5. Cairns NG, Pasternak M, Wachter A, Cobbett CS, Meyer AJ (2006) Maturation of Arabidopsis seeds is dependent on glutathione biosynthesis within the embryo. Plant Physiol 141: 446-455.
6. Carol RJ, Dolan L (2006) The role of reactive oxygen species in cell growth: lessons from root hairs. J Exp Bot 57: 1829-1834.
7. Comelli RN, Gonzalez DH (2007) Conserved homeodomain cysteines confer redox sensitivity and influence the DNA binding properties of plant class III HD-Zip proteins. Arch Biochem Biophys 467: 41-47.
8. Cubas P, Lauter N, Doebley J, Coen E (1999) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18: 215-222.
9. Delaunay A, Isnard AD, Toledano MB (2000) H2O2 sensing through oxidation of the Yap1 transcription factor. EMBO J 19: 5157-5166.
10. Després C, Chubak C, Rochon A, Clark R, Bethune T, Desveaux D, Fobert PR (2003) The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/ leucine zipper transcription factor TGA1. Plant Cell 15: 2181-2191.
11. Dezar CA, Gago GM, Gonzalez DH, Chan RL (2005) Hahb-4, a sunflower homeobox-leucine zipper gene, is a developmental regulator and confers drought tolerance to Arabidopsis thaliana plants. Transgenic Res 14: 429-440.
12. Diaz Vivancos P, Wolff T, Markovic J, Pallardó FV, Foyer CH (2010) A nuclear glutathione cycle within the cell cycle. Biochem J 431: 169-178.
13. Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386: 485-488.
14. Ellenberger T, Fass D, Arnaud M, Harrison SC (1994) Crystal structure of transcription factor E47: E-box recognition by a basic region helix-loop-helix dimer. Genes Dev 8: 970-980.
15. Fairman R, Beran-Steed RK, Anthony-Cahill SJ, Lear JD, Stafford WF III, DeGrado WF, Benfield PA, Brenner SL (1993) Multiple oligomeric states regulate the DNA binding of helix-loop-helix peptides. Proc Natl Acad Sci USA 90: 10429-10433.
16. Ferré-D'Amaré AR, Pognonec P, Roeder RG, Burley SK (1994) Structure and function of the b/HLH/Z domain of USF. EMBO J 13: 180-189.
17. Fey V, Wagner R, Braütigam K, Wirtz M, Hell R, Dietzmann A, Leister D, Oelmüller R, Pfannschmidt T (2005) Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. J Biol Chem 280: 5318-5328.
18. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, et al (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422: 442-446.
19. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17: 1866-1875.
20. Giraud E, Ng S, Carrie C, Duncan O, Low J, Lee CP, Van Aken O, Millar AH, Murcha M, Whelan J (2010) TCP transcription factors link the regulation of genes encoding mitochondrial proteins with the circadian clock in Arabidopsis thaliana. Plant Cell 22: 3921-3934.
21. Gonzalez DH, Welchen E, Attallah CV, Comelli RN, Mufarrege EF (2007) Transcriptional coordination of the biogenesis of the oxidative phosphorylation machinery in plants. Plant J 51: 105-116.
22. Gordge MP, Hothersall JS, Noronha-Dutra AA (1998) Evidence for a cyclic GMP-independent mechanism in the anti-platelet action of S-nitrosoglutathione. Br J Pharmacol 124: 141-148.
23. Gupta R, Luan S (2003) Redox control of protein tyrosine phosphatases and mitogen-activated protein kinases in plants. Plant Physiol 132: 1149-1152.
24. Heine GF, Hernandez JM, Grotewold E (2004) Two cysteines in plant R2R3. MYB domains participate in REDOX-dependent DNA binding. J Biol Chem 279: 37878-37885.
25. Hervé C, Dabos P, Bardet C, Jauneau A, Auriac MC, Ramboer A, Lacout F, Tremousaygue D (2009) In vivo interference with AtTCP20 function induces severe plant growth alterations and deregulates the expression of many genes important for development. Plant Physiol 149: 1462-1477.
26. Hicks LM, Cahoon RE, Bonner ER, Rivard RS, Sheffield J, Jez JM (2007) Thiol-based regulation of redox-active glutamate-cysteine ligase from Arabidopsis thaliana. Plant Cell 19: 2653-2661.
27. Hull GA, Devic M (1995) The beta-glucuronidase (gus) reporter gene system. Gene fusions: spectrophotometric, fluorometric, and histochemical detection. In H Jones, ed, Methods in Plant Molecular Biology: Plant Gene Transfer and Expression Protocols. Humana Press, Totowa, NJ, pp 125-141.
28. Jiang K, Schwarzer C, Lally E, Zhang S, Ruzin S, Machen T, Remington SJ, Feldman L (2006) Expression and characterization of a redox-sensing green fluorescent protein (reduction-oxidation-sensitive green fluorescent protein) in Arabidopsis. Plant Physiol 141: 397-403.
29. Kieffer M, Master V, Waites R, Davies B (2011) TCP14 and TCP15 affect internode length and leaf shape in Arabidopsis. Plant J 68: 147-158.
30. Kosugi S, Ohashi Y (2002) DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J 30: 337-348.
31. Koyama T, Furutani M, Tasaka M, Ohme-Takagi M (2007) TCP transcription factors control the morphology of shoot lateral organs via negative regulation of the expression of boundary-specific genes in Arabidopsis. Plant Cell 19: 473-484.
32. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
33. Lee J, Godon C, Lagniel G, Spector D, Garín J, Labarre J, Toledano MB (1999) Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast. J Biol Chem 274: 16040-16046.
34. Li C, Potuschak T, Colón-Carmona A, Gutiérrez RA, Doerner P (2005) Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proc Natl Acad Sci USA 102: 12978-12983.
35. Li JF, Park E, von Arnim AG, Nebenführ A (2009) The FAST technique: a simplified Agrobacterium-based transformation method for transient gene expression analysis in seedlings of Arabidopsis and other plant species. Plant Methods 5: 6.
36. Li ZY, Li B, Dong AW (2012) The Arabidopsis transcription factor AtTCP15 regulates endoreduplication by modulating expression of key cell-cycle genes. Mol Plant 5: 270-280.
37. Lindermayr C, Sell S, Müller B, Leister D, Durner J (2010) Redox regulation of the NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. Plant Cell 22: 2894-2907.
38. Luo D, Carpenter R, Vincent C, Copsey L, Coen E (1996) Origin of floral asymmetry in Antirrhinum. Nature 383: 794-799.
39. Martín-Trillo M, Cubas P (2010) TCP genes: a family snapshot ten years later. Trends Plant Sci 15: 31-39.
40. May M, Vernoux T, Leaver C, Van Montagu M, Inze D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49: 649-667.
41. Meinhard M, Rodriguez PL, Grill E (2002) The sensitivity of ABI2 to hydrogen peroxide links the abscisic acid-response regulator to redox signalling. Planta 214: 775-782.
42. Meyer AJ (2008) The integration of glutathione homeostasis and redox signaling. J Plant Physiol 165: 1390-1403.
43. Meyer AJ, Brach T, Marty L, Kreye S, Rouhier N, Jacquot JP, Hell R (2007) Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J 52: 973-986.
44. Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113: 935-944.
45. Mulrooney SB (1997) Application of a single-plasmid vector for mutagenesis and high-level expression of thioredoxin reductase and its use to examine flavin cofactor incorporation. Protein Expr Purif 9: 372-378.
46. Nag A, King S, Jack T (2009) miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proc Natl Acad Sci USA 106: 22534-22539.
47. Nath U, Crawford BC, Carpenter R, Coen E (2003) Genetic control of surface curvature. Science 299: 1404-1407.
48. Navaud O, Dabos P, Carnus E, Tremousaygue D, Hervé C (2007) TCP transcription factors predate the emergence of land plants. J Mol Evol 65: 23-33.
49. Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53: 1283-1304.
50. Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425: 257-263.
51. Pasternak M, Lim B, Wirtz M, Hell R, Cobbett CS, Meyer AJ (2008) Restricting glutathione biosynthesis to the cytosol is sufficient for normal plant development. Plant J 53: 999-1012.
52. Pei ZM, Murata Y, Benning G, Thomine S, Klüsener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406: 731-734.
53. Pellny TK, Locato V, Vivancos PD, Markovic J, De Gara L, Pallardó FV, Foyer CH (2009) Pyridine nucleotide cycling and control of intracellular redox state in relation to poly (ADP-ribose) polymerase activity and nuclear localization of glutathione during exponential growth of Arabidopsis cells in culture. Mol Plant 2: 442-456.
54. Potters G, Pasternak TP, Guisez Y, Jansen MAK (2009) Different stresses, similar morphogenic responses: integrating a plethora of pathways. Plant Cell Environ 32: 158-169.
55. Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MAK (2007) Stressinduced morphogenic responses: growing out of trouble? Trends Plant Sci 12: 98-105.
56. Printen JA, Sprague GF Jr (1994) Protein-protein interactions in the yeast pheromone response pathway: Ste5p interacts with all members of the MAP kinase cascade. Genetics 138: 609-619.
57. Pruneda-Paz JL, Breton G, Para A, Kay SA (2009) A functional genomics approach reveals CHE as a component of the Arabidopsis circadian clock. Science 323: 1481-1485.
58. Reynolds A, Lundblad V, Dorris D, Keavency M (1997) Yeast vectors and assays for expression of cloned genes. In F Ausubel, R Brent, RE Kingston, DD Moore, JG Seidman, JA Smith, K Struhl, eds, Current Protocols in Molecular Biology. Greene Publishing and Wiley-Interscience, New York, pp 13.6.1-13.6.6.
59. Rouhier N, Lemaire SD, Jacquot JP (2008) The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annu Rev Plant Biol 59: 143-166.
60. Sedmak JJ, Grossberg SE (1977) A rapid, sensitive, and versatile assay for protein using Coomassie Brilliant Blue G250. Anal Biochem 79: 544-552.
61. Serpa V, Vernal J, Lamattina L, Grotewold E, Cassia R, Terenzi H (2007) Inhibition of AtMYB2. DNA-binding by nitric oxide involves cysteine S-nitrosylation. Biochem Biophys Res Commun 361: 1048-1053.
62. Shaikhali J, Heiber I, Seidel T, Ströher E, Hiltscher H, Birkmann S, Dietz KJ, Baier M (2008) The redox-sensitive transcription factor Rap2.4a controls nuclear expression of 2-Cys peroxiredoxin A and other chloroplast antioxidant enzymes. BMC Plant Biol 8: 48.
63. Shaikhali J, Norén L, de Dios Barajas-López J, Srivastava V, König J, Sauer UH, Wingsle G, Dietz KJ, Strand Å (2012) Redox-mediated mechanisms regulate DNA binding activity of the G-group of basic region leucine zipper (bZIP) transcription factors in Arabidopsis. J Biol Chem 287: 27510-27525.
64. Shimizu T, Toumoto A, Ihara K, Shimizu M, Kyogoku Y, Ogawa N, Oshima Y, Hakoshima T (1997) Crystal structure of PHO4 bHLH domain-DNA complex: flanking base recognition. EMBO J 16: 4689-4697.
65. Silver J, Limjoco T, Feinstone S (1995) Site-specific mutagenesis using the polymerase chain reaction. In MA Innis, DH Gelfand, JJ Sninsky, eds, PCR Strategies. Academic Press, San Diego, pp 179-188.
66. Spinelli SV, Martin AP, Viola IL, Gonzalez DH, Palatnik JF (2011) A mechanistic link between STM and CUC1 during Arabidopsis development. Plant Physiol 156: 1894-1904.
67. Starovasnik MA, Blackwell TK, Laue TM, Weintraub H, Klevit RE (1992) Folding topology of the disulfide-bonded dimeric DNA-binding domain of the myogenic determination factor MyoD. Biochemistry 31: 9891-9903.
68. Steiner E, Efroni I, Gopalraj M, Saathoff K, Tseng TS, Kieffer M, Eshed Y, Olszewski N, Weiss D (2012) The ArabidopsisO-linked N-acetylglucosamine transferase SPINDLY interacts with class I TCPs to facilitate cytokinin responses in leaves and flowers. Plant Cell 24: 96-108.
69. Takada S, Hibara K, Ishida T, Tasaka M (2001) The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 128: 1127-1135.
70. Takeda T, Amano K, Ohto MA, Nakamura K, Sato S, Kato T, Tabata S, Ueguchi C (2006) RNA interference of the Arabidopsis putative transcription factor TCP16 gene results in abortion of early pollen development. Plant Mol Biol 61: 165-177.
71. Tatematsu K, Nakabayashi K, Kamiya Y, Nambara E (2008) Transcription factor AtTCP14 regulates embryonic growth potential during seed germination in Arabidopsis thaliana. Plant J 53: 42-52