Abstract
Plants use programmed cell death (PCD) as a tool in their growth and development. PCD is also involved in defense against different kinds of stresses including pathogen attack. In both types of PCD, reactive oxygen species (ROS) play an important role. ROS is not only a toxic by-product but also acts as signaling molecule that can trigger defense mechanisms in plant. Earlier transcriptome studies indicated the activation of ROS responsive and/or generating genes. Eight genes were selected with a potential role in ROS-induced PCD pathway and one of them, encoding the zinc finger protein ZAT11 (Zinc Arabidopsis thaliana11) exhibited an altered cell death phenotype. Two independent zat11 mutants in a loh2 (LAG one homologue2) genetic background showed enhanced tolerance to paraquat-induced oxidative stress and PCD; whereas, these double mutants exhibited cell death triggered by Alternaria alternata f. sp. lycopersici-toxin (AAL-toxin) or 3-aminotriazole (AT). This indicates that ZAT11 is involved in an intricate oxidative stress-induced PCD network, and the final outcome depends on ZAT11 interactions with other players specific for the particular types of oxidative stress.
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References
Brandwagt BF, Mesbah LA, Takken FLW, Laurent PL, Kneppers TJA, Hille J, Nijkamp HJJ (2000) A longevity assurance gene homolog of tomato mediates resistance to Alternaria alternata f. sp lycopersici toxins and fumonisin B1. Proc Natl Acad Sci USA 97:4961–4966
Chaves I, Regalado AP, Chen M, Ricardo CP, Showalter AM (2002) Programmed cell death induced by (β-D-galactosyl)3 Yariv reagent in Nicotiana tabacum BY-2 suspension-cultured cells. Physiol Plant 116:548–553
Chen YF, Li LQ, Xu Q, Kong YH, Wang H, Wu WH (2009) The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis. Plant Cell 21:3554–3566
Coimbra S, Costa M, Jones B, Mendes MA, Pereira LG (2009) Pollen grain development is compromised in Arabidopsis agp6 agp11 null mutants. J Exp Bot 60:3133–3142
Coll NS, Epple P, Dangl JL (2011) Programmed cell death in the plant immune system. Cell Death Differ 18:1247–1256
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
Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143:1789–1801
Englbrecht CC, Schoof H, Böhm S (2004) Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 5:39
Fujibe T, Saji H, Arakawa K (2004) A methyl viologen-resistant mutant of Arabidopsis, which is allelic to ozone-sensitive rcd1, is tolerant to supplemental ultraviolet-B irradiation. Plant Physiol 134:275–285
Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Mittler R, Breusegem FV, Shulaev V, Apel K, Inze D (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 141:436–445
Gaspar YM, Nam J, Schultz CJ, Lee LY, Gilson PR, Gelvin SB, Bacic A (2004) Characterization of the Arabidopsis lysine-rich arabinogalactan protein AtAGP17 mutant (rat1) that results in a decreased efficiency of Agrobacterium transformation. Plant Physiol 135:2162–2171
Gechev TS, Hille J (2005) Hydrogen peroxide as a signal controlling plant programmed cell death. J Cell Biol 168:17–20
Gechev T, Gadjev I, Van Breusegem F, Inze D, Dukiandjiev S, Toneva V, Minkov I (2002) Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes. Cell Mol Life Sci 59:708–714
Gechev TS, Gadjev IZ, Hille J (2004) An extensive microarray analysis of AAL-toxin-induced cell death in Arabidopsis thaliana brings new insights into the complexity of programmed cell death in plants. Cell Mol Life Sci 61:1185–1197
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
Gechev TS, Ferwerda MA, Mehterov N, Laloi C, Qureshi MK, Hille J (2008) Arabidopsis AAL-toxin-resistant mutant atr1 shows enhanced tolerance to programmed cell death induced by reactive oxygen species. Biochem Biophys Res Commun 375:639–644
Gunawardena AH (2008) Programmed cell death and tissue remodelling in plants. J Exp Bot 59:445–451
Guo Y, Cai Z, Gan S (2004) Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ 27:521–549
Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322
Huang XY, Chao DY, Gao JP, Zhu MZ, Shi M, Lin HX (2009) A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev 23:1805–1817
Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and b in n, n-dimethylformamide and 80 % acetone. Plant Physiol 77:483–485
Ito J, Fukuda H (2002) ZEN1 is a key enzyme in the degradation of nuclear DNA during programmed cell death of tracheary elements. Plant Cell 14:3201–3211
Jiang Y, Deyholos MK (2009) Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol 69:91–105
Kalde M, Barth M, Somssich IE, Lippok B (2003) Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways. Mol Plant Microbe Interact 16:295–305
Kasajima I, Ide Y, Yokota Hirai M, Fujiwara T (2010) WRKY6 is involved in the response to boron deficiency in Arabidopsis thaliana. Physiol Plant 139:80–92
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
McLellan H, Gilroy EM, Yun BW, Birch PR, Loake GJ (2009) Functional redundancy in the Arabidopsis Cathepsin B gene family contributes to basal defence, the hypersensitive response and senescence. New Phytol 183:408–418
Mehterov N, Balazadeh S, Hille J, Toneva V, Mueller-Roeber B, Gechev T (2012) Oxidative stress provokes distinct transcriptional responses in the stress-tolerant atr7 and stress-sensitive loh2 Arabidopsis thaliana mutants as revealed by multi-parallel quantitative real-time PCR analysis of ROS marker and antioxidant genes. Plant Physiol Biochem 59:20–29
Mittler R, Kim Y, Song L, Coutu J, Coutu A, Ciftci-Yilmaz S, Lee H, Stevenson B, Zhu JK (2006) Gain- and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. FEBS Lett 580:6537–6542
Motose H, Sugiyama M, Fukuda H (2004) A proteoglycan mediates inductive interaction during plant vascular development. Nature 429:873–878
Qureshi MK, Radeva V, Genkov T, Minkov I, Hille J, Gechev TS (2011) Isolation and characterization of Arabidopsis mutants with enhanced tolerance to oxidative stress. Acta Physiol Plant 33:375–382
Rizhsky L, Davletova S, Liang H, Mittler R (2004) The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J Biol Chem 279:11736–11743
Robatzek S, Somssich IE (2002) Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev 16:1139–1149
Spassieva SD, Markham JE, Hille J (2002) The plant disease resistance gene Asc-1 prevents disruption of sphingolipid metabolism during AAL-toxin-induced programmed cell death. Plant J 32:561–572
Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8:397–403
Van Breusegem F, Dat J (2006) Reactive oxygen species in plant cell death. Plant Physiol 141:384–390
Wagner D, Przybyla D, Op den Camp R, Kim C, Landgraf F, Lee KP, Würsch M, Laloi C, Nater M, Hideg E, Apel K (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306:1183–1185
Wang YH (2008) How effective is T-DNA insertional mutagenesis in Arabidopsis? J Biochem Tech 1:11–20
Wang L, Pei Z, Tian Y, He C (2005) OsLSD1, a rice zinc finger protein, regulates programmed cell death and callus differentiation. Mol Plant Microbe Interact 18:375–384
Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, Inzé D, Van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C-3 plants. EMBO J 16:4806–4816
Yun BW, Feechan A, Yin M, Saidi NB, Le Bihan T, Yu M, Moore JW, Kang JG, Kwon E, Spoel SH, Pallas JA, Loake GJ (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478:264–268
Zimmermann P, Heinlein C, Orendi G, Zentgraf U (2006) Senescence-specific regulation of catalases in Arabidopsis thaliana (L.) Heynh. Plant Cell Environ 29:1049–1060
Acknowledgments
Authors acknowledge Veselin Petrov for critically reading the manuscript. MK Qureshi wishes to thank the Higher Education Commission (HEC) of Pakistan for financial support of part of this project. Part of this project was also financially supported by EC FP7 (project BioSupport, 245588).
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Communicated by J.-H. Liu.
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Qureshi, M.K., Sujeeth, N., Gechev, T.S. et al. The zinc finger protein ZAT11 modulates paraquat-induced programmed cell death in Arabidopsis thaliana . Acta Physiol Plant 35, 1863–1871 (2013). https://doi.org/10.1007/s11738-013-1224-y
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DOI: https://doi.org/10.1007/s11738-013-1224-y