Early transcriptional defense responses in arabidopsis cell suspension culture under high-light conditions

Plant Physiology

Volumn 156, Issue 3, 2011, Pages 1439-1456

  González Pérez, Sergio ^a   Gutiérrez, Jorge ^a   García García, Francisco ^b   Osuna, Daniel ^c   Dopazo, Joaquín ^b   Lorenzo, Óscar ^c   Revuelta, José L ^d   Arellano, Juan B ^a  

^a INSTITUTO DE RECURSOS NATURALES Y AGROBIOLOGÍA DE SALAMANCA   (Spain)

^b CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^c UNIVERSITY OF SALAMANCA   (Spain)

^d CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 79960035423     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.111.177766     Document Type: Article

References (98)

1. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824-827
2. Al-Shahrour F, Arbiza L, Dopazo H, Huerta J, Mínguez P, Montaner D, Dopazo J (2007) From genes to functional classes in the study of biological systems. BMC Bioinformatics 8: 114
3. Al-Shahrour F, Díaz-Uriarte R, Dopazo J (2004) FatiGO: a Web tool for finding significant associations of Gene Ontology terms with groups of genes. Bioinformatics 20: 578-580
4. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Physiol Plant Mol Biol 55: 373-399
5. Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II: inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113-134
6. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141: 391-396
7. Axelos M, Curie C, Mazzolini L, Bardet C, Lescure B (1992) A protocol for transient gene-expression in Arabidopsis thaliana protoplasts isolated from cell suspension cultures. Plant Physiol Biochem 30: 123-128
8. Bechtold U, Karpinski S, Mullineaux PM (2005) The influence of the light environment and photosynthesis on oxidative signalling responses in plant-biotrophic pathogen interactions. Plant Cell Environ 28: 1046-1055
9. Bell E, Takeda S, Dolan L (2009) Reactive oxygen species in growth and development. In LA del Ri{dotless} ́o, A Puppo, eds, Reactive Oxygen Species in Plant Signaling. Springer, Dordrecht, The Netherlands, pp 55-71
10. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Stat Methodol 57: 289-300
11. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29: 1165-1188
12. Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170: 489-504
13. Bolstad B, Irizarry R, Astrand M, Speed T (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193
14. Böttcher C, Pollmann S (2009) Plant oxylipins: plant responses to 12-oxophytodienoic acid are governed by its specific structural and functional properties. FEBS J 276: 4693-4704
15. Cassells AC, Curry RF (2001) Oxidative stress and physiological, epigenetic and genetic variability in plant tissue culture: implications for micropropagators and genetic engineers. Plant Cell Tissue Organ Cult 64: 145-157
16. Chini A, Fonseca S, Fernández G, Adie B, Chico JM, Lorenzo O, García- Casado G, López-Vidriero I, Lozano FM, Ponce MR, et al (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448: 666-671
17. Chomczynski P, Sacchi N (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat Protoc 1: 581-585
18. Cramer GR (2002) Response of abscisic acid mutants of Arabidopsis to salinity. Funct Plant Biol 29: 561-567
19. Danon A, Miersch O, Felix G, op den Camp RGL, Apel K (2005) Concurrent activation of cell death-regulating signaling pathways by singlet oxygen in Arabidopsis thaliana. Plant J 41: 68-80
20. Davletova S, Schlauch K, Coutu J, Mittler R (2005) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139: 847-856
21. DeMichele R, Vurro E, Rigo C, Costa A, Elviri L, Di Valentin M, Careri M, Zottini M, Sanitádi Toppi L, Lo Schiavo F (2009) Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol 150: 217-228
22. Doyle SM, Diamond M, McCabe PF (2010) Chloroplast and reactive oxygen species involvement in apoptotic-like programmed cell death in Arabidopsis suspension cultures. J Exp Bot 61: 473-482
23. Durrant WE, Dong X (2004) Systemic acquired resistance (2004). Annu Rev Phytopathol 42: 185-209
24. Flors C, Fryer MJ, Waring J, Reeder B, Bechtold U, Mullineaux PM, Nonell S, Wilson MT, Baker NR (2006) Imaging the production of singlet oxygen in vivo using a new fluorescent sensor, Singlet Oxygen Sensor Green. J Exp Bot 57: 1725-1734
25. Foyer CH, Noctor G (2005a) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28: 1056-1071
26. Foyer CH, Noctor G (2005b) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17: 1866-1875
27. Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR (2003) Control of ascorbate peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. Plant J 33: 691-705
28. Fufezan C, Rutherford AW, Krieger-Liszkay A (2002) Singlet oxygen production in herbicide-treated photosystem II. FEBS Lett 532: 407-410
29. Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, Apel K, Inze D, Mittler R, van Breusegem F (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 141: 436-445
30. Galvez-Valdivieso G, Fryer MJ, Lawson T, Slattery K, Truman W, Smirnoff N, Asami T, Davies WJ, Jones AM, Baker NR, et al (2009) The high light response in Arabidopsis involves ABA signaling between vascular and bundle sheath cells. Plant Cell 21: 2143-2162
31. Galvez-Valdivieso G, Mullineaux PM (2010) The role of reactive oxygen species in signalling from chloroplasts to the nucleus. Physiol Plant 138: 430-439
32. Gao M, Wang X, Wang D, Xu F, Ding X, Zhang Z, Bi D, Cheng YT, Chen S, Li X, et al (2009) Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host Microbe 6: 34-44
33. Gechev TS, van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays 28: 1091-1101
34. Gollmer A, Arnbjerg J, Blaikie FH, Pedersen BW, Breitenbach T, Daasbjerg K, Glasius M, Ogilby PR (2011) Singlet oxygen sensor green(): photochemical behavior in solution and in a mammalian cell. Photochem Photobiol 87: 671-679
35. Halliwell B (2006) Reactive species and antioxidants: redox biology is a fundamental theme of aerobic life. Plant Physiol 141: 312-322
36. Hayward A, Stirnberg P, Beveridge C, Leyser O (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151: 400-412
37. Hideg E, Spetea C, Vass I (1995) Superoxide radicals are not the main promoters of acceptor-side-induced photoinhibitory damage in spinach thylakoids. Photosynth Res 46: 399-407
38. Hideg E, Vass I (1995) Singlet oxygen is not produced in photosystem I under photoinhibitory conditions. Photochem Photobiol 62: 949-952
39. Hruz T, Laule O, Szabo G, Wessendrop F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinformatics 2008: 420747
40. Huffaker A, Pearce G, Ryan CA (2006) An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc Natl Acad Sci USA 103: 10098-10103
41. Huibers RP, de Jong M, Dekter RW, Van den Ackerveken G (2009) Disease-specific expression of host genes during downy mildew infection of Arabidopsis. Mol Plant Microbe Interact 22: 1104-1115
42. Humphrey AJ, Beale MH (2006) Strigol: biogenesis and physiological activity. Phytochemistry 67: 636-640
43. Ishitani M, Xiong L, Stevenson B, Zhu JK (1997) Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis thaliana: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways. Plant Cell 9: 1935-1949
44. Jakab G, Manrique A, Zimmerli L, Metraux JP, Mauch-Mani B (2003) Molecular characterization of a novel lipase-like pathogen-inducible gene family of Arabidopsis. Plant Physiol 132: 2230-2239
45. Johnson MP, Zia A, Horton P, Ruban AV (2010) Effect of xanthophylls composition on the chlorophyll excited state lifetime in plant leaves and isolated LHCII. Chem Phys 373: 23-32
46. Johnson RA, Wichern DW (1998) Applied Multivariate Statistical Analysis, Ed 2. Prentice Hall, Upper Saddle River, NJ
47. Jouannea JP, Peaudlen C (1967) Growth and synthesis of proteins in cell suspensions of a kinetin dependent tobacco. Physiol Plant 20: 834-850
48. Keren N, Berg A, van Kan PJM, Levanon H, Ohad I (1997) Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: the role of back electron flow. Proc Natl Acad Sci USA 94: 1579-1584
49. Khandelwal A, Elvitigala T, Ghosh B, Quatrano RS (2008) Arabidopsis transcriptome reveals control circuits regulating redox homeostasis and the role of an AP2 transcription factor. Plant Physiol 148: 2050-2058
50. Kim CH, Meskauskiene R, Apel K, Laloi C (2008) No single way to understand singlet oxygen signalling in plants. EMBO Rep 9: 435-439
51. Koltai H, LekKala SP, Bhattacharya C, Mayzlish-Gati E, Resnick N, Wininger S, Dor E, Yoneyama K, Yoneyama K, Hershenhorn J, et al (2010) A tomato strigolactone-impaired mutant displays aberrant shoot morphology and plant interactions. J Exp Bot 61: 1739-1749
52. Koornneef M, Dellaert LWM, van der Veen JH (1982) EMS- and radiationinduced mutation frequencies at individual loci in Arabidopsis thaliana (L.) Heynh. Mutat Res 93: 109-123
53. Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res 98:551-564
54. Laloi C, Stachowiak M, Pers-Kamczyc E, Warzych E, Murgia I, Apel K(2007) Cross-talk between singlet oxygen- and hydrogen peroxidedependent suspension of stress responses in Arabidopsis thaliana. Proc Natl Acad Sci USA 104: 672-677
55. Larkindale J, Hall JD, Knight MR, Vierling E (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 138: 882-897
56. Lebkuecher JG, Haldeman KA, Harris CE, Holz SL, Joudah SA, Minton DA (1999) Development of photosystem II activity during irradiance of etiolated Helianthus (Asteraceae) seedlings. Am J Bot 86: 1087-1092
57. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCT method. Methods 25: 402-408
58. Lokstein H, Tian L, Polle JEW, DellaPenna D (2002) Xanthophyll biosynthetic mutants of Arabidopsis thaliana: altered nonphotochemical quenching of chlorophyll fluorescence is due to changes in photosystem II antenna size and stability. Biochim Biophys Acta 1553: 309-319
59. Lorenzo O, Piqueras R, Sánchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15: 165-178
60. Lu PL, Chen NZ, An R, Su Z, Qi BS, Ren F, Chen J, Wang XC (2007) A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis. Plant Mol Biol 63: 289-305
61. Mayzlish-Gati E, LekKala SP, Resnick N, Wininger S, Bhattacharya C, Lemcoff JH, Kapulnik Y, Koltai H (2010) Strigolactones are positive regulators of light-harvesting genes in tomato. J Exp Bot 61: 3129-3136
62. Menges M, Hennig L, Gruissem W, Murray JAH (2003) Genome-wide gene expression in an Arabidopsis cell suspension. Plant Mol Biol 53: 423-442
63. Meskauskiene R, Nater M, Goslings D, Kessler F, op den Camp R, Apel K (2001) FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 98: 12826-12831
64. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15: 809-834
65. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33: 453-467
66. Mishra NP, Francke C, van Gorkom HJ, Ghanotakis DF (1994) Destructive role of singlet oxygen during aerobic illumination of the photosystem II core complex. Biochim Biophys Acta 1186: 81-90
67. Mittler R, Vanderauwera S, Gollery M, van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490-498
68. Miyao M, Ikeuchi M, Yamamoto N, Ono T (1995) Specific degradation of the D1 protein of photosystem II by treatment with hydrogen peroxide in darkness: implications for the mechanism of degradation of the D1 protein under illumination. Biochemistry 34: 10019-10026
69. Mullineaux PM, Baker NR (2010) Oxidative stress: antagonistic signaling for acclimation or cell death? Plant Physiol 154: 521-525
70. Nakano T, Suzuki K, Ohtsuki N, Tsujimoto Y, Fujimura T, Shinshi H (2006) Identification of genes of the plant-specific transcription-factor families cooperatively regulated by ethylene and jasmonate in Arabidopsis thaliana. J Plant Res 119: 407-413
71. Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50: 333-359
72. Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10: 1121-1134
73. Ochsenbein C, Przybyla D, Danon A, Landgraf F, Gobel C, Imboden A, Feussner I, Apel K (2006) The role of EDS1 (enhanced disease susceptibility) during singlet oxygen-mediated stress responses of Arabidopsis. Plant J 47: 445-456
74. op den Camp RG, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Göbel C, Feussner I, et al (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15: 2320-2332
75. Oswald O, Martin T, Dominy PJ, Graham IA (2001) Plastid redox state and sugars: interactive regulators of nuclear-encoded photosynthetic gene expression. Proc Natl Acad Sci USA 98: 2047-2052
76. Piñas-Fernández A, Strand A (2008) Retrograde signaling and plant stress: plastid signals initiate cellular stress responses. Curr Opin Plant Biol 11: 509-513
77. Pogson BJ, Niyogi KK, Bjorkman O, DellaPenna D (1998) Altered xanthophylls compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants. Proc Natl Acad Sci USA 95: 13324-13329
78. Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975: 384-394
79. Przybyla D, Gobel C, Imboden A, Hamberg M, Feussner I, Apel K (2008) Enzymatic, but not non-enzymatic, 1O2-mediated peroxidation of polyunsaturated fatty acids forms part of the EXECUTER1-dependent stress response program in the flu mutant of Arabidopsis thaliana. Plant J 54: 236-248
80. Quinn GP, Keough MJ (2002) Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge, UK
81. Rhee SG, Chang T-S, Jeong W, Kang D (2010) Methods for detection and measurement of hydrogen peroxide inside and outside of cells. Mol Cells 29: 539-549
82. Rinalducci S, Pedersen JZ, Zolla L (2004) Formation of radicals from singlet oxygen produced during photoinhibition of isolated light-harvesting proteins of photosystem II. Biochim Biophys Acta 1608: 63-73
83. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, et al (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34: 374-378
84. Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi- Shinozaki K (2006) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103: 18822-18827
85. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76-85
86. Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article 3
87. Sorefan K, Booker J, Haurogne K, Goussot M, Bainbridge K, Foo E, Chatfield S, Ward S, Beveridge C, Rameau C, et al (2003) MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev 17: 1469-1474
88. Takahashi Y, Hansson O, Mathis P, Satoh K (1987) Primary radical pair in the photosystem II reaction center. Biochim Biophys Acta 893: 49-59
89. Triantaphylidés C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signalling. Trends Plant Sci 14: 219-228
90. Triantaphylidés C, Krischke M, Hoeberichts FA, Ksas B, Gresser G, Havaux M, van Breusegem F, Mueller MJ (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol 148: 960-968
91. Ülker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7: 491-498
92. van Breusegem F, Bailey-Serres J, Mittler R (2008) Unraveling the tapestry of networks involving reactive oxygen species in plants. Plant Physiol 147: 978-984
93. Vass I, Cser K (2009) Janus-faced charge recombinations in photosystem II photoinhibition. Trends Plant Sci 14: 200-205
94. Wang GD, Long YC, Thomma BPHJ, de Wit PJGM, Angenent GC, Fiers M (2010) Functional analyses of the CLAVATA2-like proteins and their domains that contribute to CLAVATA2 specificity. Plant Physiol 152: 320-331
95. Wang KLC, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14: S131-S151
96. Wu YR, Deng ZY, Lai JB, Zhang YY, Yang CP, Yin BJ, Zhao QZ, Zhang L, Li Y, Yang CW, et al (2009) Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses. Cell Res 19: 1279-1290
97. Xiong L, Gong Z, Rock C, Subramanian S, Guo Y, Xu W, Galbraith D, Zhu JK (2001) Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Dev Cell 6: 771-781
98. Zeier J, Pink B, Mueller MJ, Berger S (2004) Light conditions influence specific defence responses in incompatible plant-pathogen interactions: uncoupling systemic resistance from salicylic acid and PR-1 accumulation. Planta 219: 673-683