The heat shock factor A4A confers salt tolerance and is regulated by oxidative stress and the mitogen-activated protein kinases MPK3 and MPK6

Plant Physiology

Volumn 165, Issue 1, 2014, Pages 319-334

  Pérez Salamó, Imma ^a   Papdi, Csaba ^a,b   Rigó, Gábor ^a   Zsigmond, Laura ^a,c   Vilela, Belmiro ^d   Lumbreras, Victoria ^d   Nagy, István ^a   Horváth, Balázs ^a   Domoki, Mónika ^a   Darula, Zsuzsa ^a   Medzihradszky, Katalin ^a   Bögre, László ^b   Koncz, Csaba ^a,e   Szabados, László ^a  

^a INSTITUTE OF BIOCHEMISTRY   (Hungary)

^b UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY OF SZEGED   (Hungary)

^d CENTRE FOR RESEARCH IN AGRICULTURAL GENOMICS CRAG   (Spain)

^e MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; ATMPK3 PROTEIN, ARABIDOPSIS; BACTERIAL DNA; ESTRADIOL; HSFA4A PROTEIN, ARABIDOPSIS; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MPK6 PROTEIN, ARABIDOPSIS; PROTEIN BINDING; SODIUM CHLORIDE; T-DNA; TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ARABIDOPSIS; CELL CULTURE; CELL NUCLEUS; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETIC TRANSFORMATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PHOSPHORYLATION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT GENE; PROTEIN MULTIMERIZATION; SALINITY; SALT TOLERANCE; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL NUCLEUS; CELLS, CULTURED; DNA, BACTERIAL; ESTRADIOL; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHOSPHORYLATION; PLANTS, GENETICALLY MODIFIED; PROTEIN BINDING; PROTEIN MULTIMERIZATION; SALINITY; SALT-TOLERANCE; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFORMATION, GENETIC;

EID: 84899875638     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.237891     Document Type: Article

References (91)

1. Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P (2008) The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20: 2117-2129
2. Ahn SG, Thiele DJ (2003) Redox regulation of mammalian heat shock factor 1 is essential for Hsp gene activation and protection from stress. Genes Dev 17: 516-528
3. Akerfelt M, Morimoto RI, Sistonen L (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol 11: 545-555
4. Anckar J, Sistonen L (2011) Regulation of HSF1 function in the heat stress response: implications in aging and disease. Annu Rev Biochem 80: 1089-1115
5. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415: 977-983
6. Baniwal SK, Bharti K, Chan KY, Fauth M, Ganguli A, Kotak S, Mishra SK, Nover L, Port M, Scharf KD, et al (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J Biosci 29: 471-487
7. Baniwal SK, Chan KY, Scharf KD, Nover L (2007) Role of heat stress transcription factor HsfA5 as specific repressor of HsfA4. J Biol Chem 282: 3605-3613
8. Banti V, Mafessoni F, Loreti E, Alpi A, Perata P (2010) The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiol 152: 1471-1483
9. Bartels S, Anderson JC, González Besteiro MA, Carreri A, Hirt H, Buchala A, Métraux JP, Peck SC, Ulm R (2009) MAP kinase phosphatase1 and protein tyrosine phosphatase1 are repressors of salicylic acid synthesis and SNC1-mediated responses in Arabidopsis. Plant Cell 21: 2884-2897
10. Chan-Schaminet KY, Baniwal SK, Bublak D, Nover L, Scharf KD (2009) Specific interaction between tomato HsfA1 and HsfA2 creates heterooligomeric superactivator complexes for synergistic activation of heat stress gene expression. J Biol Chem 284: 20848-20857
11. Chang R, Jang CJ, Branco-Price C, Nghiem P, Bailey-Serres J (2012) Transient MPK6 activation in response to oxygen deprivation and reoxygenation is mediated by mitochondria and aids seedling survival in Arabidopsis. Plant Mol Biol 78: 109-122
12. Chaouch S, Queval G, Vanderauwera S, Mhamdi A, Vandorpe M, Langlois-Meurinne M, Van Breusegem F, Saindrenan P, Noctor G (2010) Peroxisomal hydrogen peroxide is coupled to biotic defense responses by ISOCHORISMATE SYNTHASE1 in a daylength-related manner. Plant Physiol 153: 1692-1705
13. Chen YC, Tsai SH, Shen SC, Lin JK, Lee WR (2001) Alternative activation of extracellular signal-regulated protein kinases in curcumin and arsenite-induced HSP70 gene expression in human colorectal carcinoma cells. Eur J Cell Biol 80: 213-221
14. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159
15. Chu B, Soncin F, Price BD, Stevenson MA, Calderwood SK (1996) Sequential phosphorylation by mitogen-activated protein kinase and glycogen synthase kinase 3 represses transcriptional activation by heat shock factor-1. J Biol Chem 271: 30847-30857
16. Czarnecka-Verner E, Pan S, Salem T, Gurley WB (2004) Plant class B HSFs inhibit transcription and exhibit affinity for TFIIB and TBP. Plant Mol Biol 56: 57-75
17. Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005a) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17: 268-281
18. Davletova S, Schlauch K, Coutu J, Mittler R (2005b) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139: 847-856
19. Dephoure N, Gould KL, Gygi SP, Kellogg DR (2013) Mapping and analysis of phosphorylation sites: a quick guide for cell biologists. Mol Biol Cell 24: 535-542
20. Devaiah BN, Nagarajan VK, Raghothama KG (2007) Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiol 145: 147-159
21. Dóczi R, Okrész L, Romero AE, Paccanaro A, Bögre L (2012) Exploring the evolutionary path of plant MAPK networks. Trends Plant Sci 17: 518-525
22. Droillard M, Boudsocq M, Barbier-Brygoo H, Laurière C (2002) Different protein kinase families are activated by osmotic stresses in Arabidopsis thaliana cell suspensions. Involvement of the MAP kinases AtMPK3 and AtMPK6. FEBS Lett 527: 43-50
23. Evrard A, Kumar M, Lecourieux D, Lucks J, von Koskull-Döring P, Hirt H (2013) Regulation of the heat stress response in Arabidopsis by MPK6-targeted phosphorylation of the heat stress factor HsfA2. PeerJ 1: e59
24. Fohgrub U, Kempken F (2012) Molecular analysis of fungal gene expression upon interkingdom competition with insects. Methods Mol Biol 944: 279-286
25. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17: 1866-1875
26. Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, Apel K, Inzé D, Mittler R, Van Breusegem F (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 141: 436-445
27. Hashikawa N, Sakurai H (2004) Phosphorylation of the yeast heat shock transcription factor is implicated in gene-specific activation dependent on the architecture of the heat shock element. Mol Cell Biol 24: 3648-3659
28. Huang GT, Ma SL, Bai LP, Zhang L, Ma H, Jia P, Liu J, Zhong M, Guo ZF (2012) Signal transduction during cold, salt, and drought stresses in plants. Mol Biol Rep 39: 969-987
29. James P, Halladay J, Craig EA (1996) Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144: 1425-1436
30. Jefferson RA, Kavanagh TA, BevanMW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901-3907
31. Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D'Angelo C, Bornberg-Bauer E, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50: 347-363
32. Kim J, Nueda A, Meng YH, Dynan WS, Mivechi NF (1997) Analysis of the phosphorylation of human heat shock transcription factor-1 by MAP kinase family members. J Cell Biochem 67: 43-54
33. Kim SH, Woo DH, Kim JM, Lee SY, Chung WS, Moon YH (2011) Arabidopsis MKK4 mediates osmotic-stress response via its regulation of MPK3 activity. Biochem Biophys Res Commun 412: 150-154
34. Kortstee AJ, Khan SA, Helderman C, Trindade LM, Wu Y, Visser RG, Brendolise C, Allan A, Schouten HJ, Jacobsen E (2011) Anthocyanin production as a potential visual selection marker during plant transformation. Transgenic Res 20: 1253-1264
35. Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10: 310-316
36. Kotak S, Port M, Ganguli A, Bicker F, von Koskull-Döring P (2004) Characterization of C-terminal domains of Arabidopsis heat stress transcription factors (Hsfs) and identification of a new signature combination of plant class A Hsfs with AHA and NES motifs essential for activator function and intracellular localization. Plant J 39: 98-112
37. Kytridis VP, Manetas Y (2006) Mesophyll versus epidermal anthocyanins as potential in vivo antioxidants: evidence linking the putative antioxidant role to the proximity of oxy-radical source. J Exp Bot 57: 2203-2210
38. Larsen MR, Thingholm TE, Jensen ON, Roepstorff P, Jørgensen TJ (2005) Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol Cell Proteomics 4: 873-886
39. Li C, Chen Q, Gao X, Qi B, Chen N, Xu S, Chen J, Wang X (2005) AtHsfA2 modulates expression of stress responsive genes and enhances tolerance to heat and oxidative stress in Arabidopsis. Sci China C Life Sci 48: 540-550
40. Li G, Meng X, Wang R, Mao G, Han L, Liu Y, Zhang S (2012) Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genet 8: e1002767
41. Li M, Doll J, Weckermann K, Oecking C, Berendzen KW, Schöffl F (2010) Detection of in vivo interactions between Arabidopsis class A-HSFs, using a novel BiFC fragment, and identification of novel class B-HSF interacting proteins. Eur J Cell Biol 89: 126-132
42. Libault M, Wan J, Czechowski T, Udvardi M, Stacey G (2007) Identification of 118 Arabidopsis transcription factor and 30 ubiquitin-ligase genes responding to chitin, a plant-defense elicitor. Mol Plant Microbe Interact 20: 900-911
43. Link V, Sinha AK, Vashista P, Hofmann MG, Proels RK, Ehness R, Roitsch T (2002) A heat-activated MAP kinase in tomato: a possible regulator of the heat stress response. FEBS Lett 531: 179-183
44. Liu HC, Liao HT, Charng YY (2011) The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. Plant Cell Environ 34: 738-751
45. Liu XM, Kim KE, Kim KC, Nguyen XC, Han HJ, Jung MS, Kim HS, Kim SH, Park HC, Yun DJ, et al (2010) Cadmium activates Arabidopsis MPK3 and MPK6 via accumulation of reactive oxygen species. Phytochemistry 71: 614-618
46. Liu XM, Nguyen XC, Kim KE, Han HJ, Yoo J, Lee K, Kim MC, Yun DJ, Chung WS (2013) Phosphorylation of the zinc finger transcriptional regulator ZAT6 by MPK6 regulates Arabidopsis seed germination under salt and osmotic stress. Biochem Biophys Res Commun 430: 1054-1059
47. Lumbreras V, Vilela B, Irar S, Solé M, Capellades M, Valls M, Coca M, Pagès M (2010) MAPK phosphatase MKP2 mediates disease responses in Arabidopsis and functionally interacts with MPK3 and MPK6. Plant J 63: 1017-1030
48. Mathur J, Koncz C, Szabados L (1995) A simple method for isolation, liquid culture, transformation and regeneration of Arabidopsis thaliana protoplasts. Plant Cell Rep 14: 221-226
49. Miller G, Mittler R (2006) Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann Bot (Lond) 98: 279-288
50. 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
51. Mishra SK, Tripp J, Winkelhaus S, Tschiersch B, Theres K, Nover L, Scharf KD (2002) In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev 16: 1555-1567
52. 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
53. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628
54. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbatespecific peroxidase in spinach chloroplasts. Plant Cell Physiol 22: 867-880
55. Nguyen XC, Hoang MH, Kim HS, Lee K, Liu XM, Kim SH, Bahk S, Park HC, Chung WS (2012a) Phosphorylation of the transcriptional regulator MYB44 by mitogen activated protein kinase regulates Arabidopsis seed germination. Biochem Biophys Res Commun 423: 703-708
56. Nguyen XC, Kim SH, Lee K, Kim KE, Liu XM, Han HJ, Hoang MH, Lee SW, Hong JC, Moon YH, et al (2012b) Identification of a C2H2-type zinc finger transcription factor (ZAT10) from Arabidopsis as a substrate of MAP kinase. Plant Cell Rep 31: 737-745
57. Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka S (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J 48: 535-547
58. Nover L, Bharti K, Döring P, Mishra SK, Ganguli A, Scharf KD (2001) Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones 6: 177-189
59. Ogawa D, Yamaguchi K, Nishiuchi T (2007) High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased themotolerance but also salt/osmotic stress tolerance and enhanced callus growth. J Exp Bot 58: 3373-3383
60. Op den Camp RG, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Gobel 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
61. Palágyi A, Terecskei K, Adám E, Kevei E, Kircher S, Mérai Z, Schäfer E, Nagy F, Kozma-Bognár L (2010) Functional analysis of amino-terminal domains of the photoreceptor phytochrome B. Plant Physiol 153: 1834-1845
62. Panchuk II, Volkov RA, Schöffl F (2002) Heat stress-and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol 129: 838-853
63. Papdi C, Abrahám E, Joseph MP, Popescu C, Koncz C, Szabados L (2008) Functional identification of Arabidopsis stress regulatory genes using the controlled cDNA overexpression system. Plant Physiol 147: 528-542
64. Papdi C, Leung J, Joseph MP, Salamó IP, Szabados L (2010) Genetic screens to identify plant stress genes. Methods Mol Biol 639: 121-139
65. Pelham HR (1982) A regulatory upstream promoter element in the Drosophila hsp 70 heat-shock gene. Cell 30: 517-528
66. Peng X, Hu Y, Tang X, Zhou P, Deng X, Wang H, Guo Z (2012) Constitutive expression of rice WRKY30 gene increases the endogenous jasmonic acid accumulation, PR gene expression and resistance to fungal pathogens in rice. Planta 236: 1485-1498
67. Pucciariello C, Banti V, Perata P (2012) ROS signaling as common element in low oxygen and heat stresses. Plant Physiol Biochem 59: 3-10
68. Rasmussen MW, Roux M, Petersen M, Mundy J (2012) MAP kinase cascades in Arabidopsis innate immunity. Front Plant Sci 3: 169
69. Rigó G, Papdi C, Szabados L (2012) Transformation using controlled cDNA overexpression system. Methods Mol Biol 913: 277-290
70. 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
71. Scarpeci TE, Zanor MI, Carrillo N, Mueller-Roeber B, Valle EM (2008) Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: a focus on rapidly induced genes. Plant Mol Biol 66: 361-378
72. Scharf KD, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim Biophys Acta 1819: 104-119
73. Shim D, Hwang JU, Lee J, Lee S, Choi Y, An G, Martinoia E, Lee Y (2009) Orthologs of the class A4 heat shock transcription factor HsfA4a confer cadmium tolerance in wheat and rice. Plant Cell 21: 4031-4043
74. Smekalova V, Doskocilova A, Komis G, Samaj J (2013) Crosstalk between secondary messengers, hormones and MAPK modules during abiotic stress signalling in plants. Biotechnol Adv 32: 2-11
75. Steffens NO, Galuschka C, Schindler M, Bülow L, Hehl R (2005) AthaMap web tools for database-assisted identification of combinatorial cis-regulatory elements and the display of highly conserved transcription factor binding sites in Arabidopsis thaliana. Nucleic Acids Res 33: W397-W402
76. StrausMR, Rietz S, Ver Loren van Themaat E, BartschM, Parker JE (2010) Salicylic acid antagonism of EDS1-driven cell death is important for immune and oxidative stress responses in Arabidopsis. Plant J 62: 628-640
77. Sun W, Bernard C, van de Cotte B, Van Montagu M, Verbruggen N (2001) At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J 27: 407-415
78. Suri SS, Dhindsa RS (2008) A heat-activated MAP kinase (HAMK) as a mediator of heat shock response in tobacco cells. Plant Cell Environ 31: 218-226
79. Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35: 259-270
80. Teige M, Scheikl E, Eulgem T, Dóczi R, Ichimura K, Shinozaki K, Dangl JL, Hirt H (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15: 141-152
81. Toufighi K, Brady SM, Austin R, Ly E, Provart NJ (2005) The Botany Array Resource: e-northerns, expression angling, and promoter analyses. Plant J 43: 153-163
82. Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu JK (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45: 523-539
83. Volkov RA, Panchuk II, Mullineaux PM, Schöffl F (2006) Heat stressinduced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol Biol 61: 733-746
84. von Koskull-Döring P, Scharf KD, Nover L (2007) The diversity of plant heat stress transcription factors. Trends Plant Sci 12: 452-457
85. Wing D, Koncz C, Schell J (1989) Conserved function in Nicotiana tabacum of a single Drosophila hsp70 promoter heat shock element when fused to a minimal T-DNA promoter. Mol Gen Genet 219: 9-16
86. Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2: e718
87. Yamanouchi U, Yano M, Lin H, Ashikari M, Yamada K (2002) A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. Proc Natl Acad Sci USA 99: 7530-7535
88. Yoshida T, Sakuma Y, Todaka D, Maruyama K, Qin F, Mizoi J, Kidokoro S, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K (2008) Functional analysis of an Arabidopsis heat-shock transcription factor HsfA3 in the transcriptional cascade downstream of the DREB2A stress-regulatory system. Biochem Biophys Res Commun 368: 515-521
89. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136: 2621-2632
90. Zsigmond L, Rigó G, Szarka A, Székely G, Otvös K, Darula Z, Medzihradszky KF, Koncz C, Koncz Z, Szabados L (2008) Arabidopsis PPR40 connects abiotic stress responses to mitochondrial electron transport. Plant Physiol 146: 1721-1737
91. Zsigmond L, Szepesi A, Tari I, Rigó G, Király A, Szabados L (2012) Overexpression of the mitochondrial PPR40 gene improves salt tolerance in Arabidopsis. Plant Sci 182: 87-93