The Solanum lycopersicum zinc finger2 cysteine-2/histidine-2 repressor-like transcription factor regulates development and tolerance to salinity in tomato and arabidopsis

Plant Physiology

Volumn 164, Issue 4, 2014, Pages 1967-1990

  Hichri, Imène ^a   Muhovski, Yordan ^b   Žižková, Eva ^c   Dobrev, Petre I ^c   Franco Zorrilla, Jose Manuel ^d   Solano, Roberto ^d   Lopez Vidriero, Irene ^d   Motyka, Vaclav ^c   Lutts, Stanley ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b WALLOON AGRICULTURAL RESEARCH CENTRE   (Belgium)

^c INSTITUTE OF EXPERIMENTAL BOTANY   (Czech Republic)

^d UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; PHYTOHORMONE; POLYAMINE; REPRESSOR PROTEIN; SODIUM CHLORIDE; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; CHEMISTRY; DNA MICROARRAY; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYDROPONICS; METABOLISM; MOLECULAR GENETICS; OSMOTIC PRESSURE; PHOTOSYNTHESIS; PHYSIOLOGY; SALINITY; SALT TOLERANCE; SIGNAL TRANSDUCTION; TOMATO; TRANSGENIC PLANT; UPREGULATION;

ABSCISIC ACID; AMINO ACID SEQUENCE; ARABIDOPSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; HYDROPONICS; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSMOTIC PRESSURE; PHOTOSYNTHESIS; PLANT GROWTH REGULATORS; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; POLYAMINES; REPRESSOR PROTEINS; SALINITY; SALT-TOLERANCE; SIGNAL TRANSDUCTION; SODIUM CHLORIDE; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 84898755305     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.225920     Document Type: Article

References (90)

1. Agarwal P, Arora R, Ray S, Singh AK, Singh VP, Takatsuji H, Kapoor S, Tyagi AK (2007) Genome-wide identification of C2H2 zinc-finger gene family in rice and their phylogeny and expression analysis. Plant Mol Biol 65: 467-485
2. Albacete A, Ghanem ME, Martínez-Andújar C, Acosta M, Sánchez-Bravo J, Martínez V, Lutts S, Dodd IC, Pérez-Alfocea F (2008) Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants. J Exp Bot 59: 4119-4131
3. Berger MF, Philippakis AA, Qureshi AM, He FS, Estep PW III, Bulyk ML (2006) Compact, universal DNA microarrays to comprehensively determine transcription-factor binding site specificities. Nat Biotechnol 24: 1429-1435
4. Borghesi E, González-Miret ML, Escudero-Gilete ML, Malorgio F, Heredia FJ, Meléndez-Martínez AJ (2011) Effects of salinity stress on carotenoids, anthocyanins, and color of diverse tomato genotypes. J Agric Food Chem 59: 11676-11682
5. Bradford KJ, Downie AB, Gee OH, Alvarado V, Yang H, Dahal P (2003) Abscisic acid and gibberellin differentially regulate expression of genes of the SNF1-related kinase complex in tomato seeds. Plant Physiol 132: 1560-1576
6. Buitink J, Thomas M, Gissot L, Leprince O (2004) Starvation, osmotic stress and desiccation tolerance lead to expression of different genes of the regulatory β and γ subunits of the SnRK1 complex in germinating seeds of Medicago truncatula. Plant Cell Environ 27: 55-67
7. Carillo P, Mastrolonardo G, Nacca F, Parisi D, Verlotta A, Fuggi A (2008) Nitrogen metabolism in durum wheat under salinity: accumulation of proline and glycine betaine. Funct Plant Biol 35: 412-426
8. Chen X, Han H, Jiang P, Nie L, Bao H, Fan P, Lv S, Feng J, Li Y (2011) Transformation of beta-lycopene cyclase genes from Salicornia europaea and Arabidopsis conferred salt tolerance in Arabidopsis and tobacco. Plant Cell Physiol 52: 909-921
9. Ciftci-Yilmaz S, Mittler R (2008) The zinc finger network of plants. Cell Mol Life Sci 65: 1150-1160
10. Ciftci-Yilmaz S, Morsy MR, Song L, Coutu A, Krizek BA, Lewis MW, Warren D, Cushman J, Connolly EL, Mittler R (2007) The EAR-motif of the Cys2/His2-type zinc finger protein Zat7 plays a key role in the defense response of Arabidopsis to salinity stress. J Biol Chem 282: 9260-9268
11. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
12. 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
13. Desikan R, Last K, Harrett-Williams R, Tagliavia C, Harter K, Hooley R, Hancock JT, Neill SJ (2006) Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. Plant J 47: 907-916
14. Dinkins R, Pflipsen C, Thompson A, Collins GB (2002) Ectopic expression of an Arabidopsis single zinc finger gene in tobacco results in dwarf plants. Plant Cell Physiol 43: 743-750
15. Djilianov DL, Dobrev PI, Moyankova DP, Vankova R, Georgieva DT, Gajdošová S, Motyka V (2013) Dynamics of endogenous phytohormones during desiccation and recovery of the resurrection plant species Haberlea rhodopensis. J Plant Growth Regul 32: 564-574
16. Dobrev PI, Kamínek M (2002) Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J Chromatogr A 950: 21-29
17. Dobrev PI, Vankova R (2012) Quantification of abscisic acid, cytokinin, and auxin content in salt-stressed plant tissues. In Shabala S, Cuin TA, eds, Plant Salt Tolerance: Methods and Protocols, Methods in Molecular Biology, Vol 913, Springer Science + Business Media, New York, pp 251-261
18. Dodd IC (2003) Hormonal interactions and stomatal responses. J Plant Growth Regul 22: 32-46
19. Ellul P, Garcia-Sogo B, Pineda B, Ríos G, Roig LA, Moreno V (2003) The ploidy level of transgenic plants in Agrobacterium-mediated transformation of tomato cotyledons (Lycopersicon esculentum Mill.) is genotype and procedure dependent [corrected]. Theor Appl Genet 106: 231-238
20. 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
21. Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14(Suppl): S15-S45
22. Fulton TM, Chunwongse J, Tanksley SD (1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol Biol Rep 13: 207-209
23. Gao H, Song A, Zhu X, Chen F, Jiang J, Chen Y, Sun Y, Shan H, Gu C, Li P, et al (2012) The heterologous expression in Arabidopsis of a chrysanthemum Cys2/His2 zinc finger protein gene confers salinity and drought tolerance. Planta 235: 979-993
24. Ghanem ME, Albacete A, Martínez-Andújar C, Acosta M, Romero-Aranda R, Dodd IC, Lutts S, Pérez-Alfocea F (2008) Hormonal changes during salinity-induced leaf senescence in tomato (Solanum lycopersicum L.). J Exp Bot 59: 3039-3050
25. Gibon Y, Sulpice R, Larher F (2000) Proline accumulation in canola leaf discs subjected to osmotic stress is related to the loss of chlorophylls and to the decrease of mitochondrial activity. Physiol Plant 110: 469-476
26. Gietz D, St Jean A, Woods RA, Schiestl RH (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res 20: 1425
27. Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 5: 26-33
28. Godoy M, Franco-Zorrilla JM, Pérez-Pérez J, Oliveros JC, Lorenzo O, Solano R (2011) Improved protein-binding microarrays for the identification of DNA-binding specificities of transcription factors. Plant J 66: 700-711
29. Gourcilleau D, Lenne C, Armenise C, Moulia B, Julien JL, Bronner G, Leblanc-Fournier N (2011) Phylogenetic study of plant Q-type C2H2 zinc finger proteins and expression analysis of poplar genes in response to osmotic, cold and mechanical stresses. DNA Res 18: 77-92
30. Hazarika P, Rajam MV (2011) Biotic and abiotic stress tolerance in transgenic tomatoes by constitutive expression of S-adenosylmethionine decarboxylase gene. Physiol Mol Biol Plants 17: 115-128
31. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125: 189-198
32. Hichri I, Heppel SC, Pillet J, Léon C, Czemmel S, Delrot S, Lauvergeat V, Bogs J (2010) The basic helix-loop-helix transcription factor MYC1 is involved in the regulation of the flavonoid biosynthesis pathway in grapevine. Mol Plant 3: 509-523
33. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27: 297-300
34. Hu X, Zhang Y, Shi Y, Zhang Z, Zou Z, Zhang H, Zhao J (2012) Effect of exogenous spermidine on polyamine content and metabolism in tomato exposed to salinity-alkalinity mixed stress. Plant Physiol Biochem 57: 200-209
35. Huang D, Wu W, Abrams SR, Cutler AJ (2008) The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors. J Exp Bot 59: 2991-3007
36. Huang J, Yang X, Wang MM, Tang HJ, Ding LY, Shen Y, Zhang HS (2007) A novel rice C2H2-type zinc finger protein lacking DLN-box/EAR-motif plays a role in salt tolerance. Biochim Biophys Acta 1769: 220-227
37. Jiang L, Pan LJ (2012) Identification and expression of C2H2 transcription factor genes in Carica papaya under abiotic and biotic stresses. Mol Biol Rep 39: 7105-7115
38. Jyothishwaran G, Kotresha D, Selvaraj T, Srideshikan SM, Rajvanshi PK, Jayabaskaran C (2007) A modified freeze-thaw method for efficient transformation of Agrobacterium tumefaciens. Curr Sci 93: 770-772
39. Kar RK (2011) Plant responses to water stress: role of reactive oxygen species. Plant Signal Behav 6: 1741-1745
40. Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7: 193-195
41. Kasinathan V, Wingler A (2004) Effect of reduced arginine decarboxylase activity on salt tolerance and on polyamine formation during salt stress in Arabidopsis thaliana. Physiol Plant 121: 101-107
42. Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45: 712-722
43. Kazan K (2006) Negative regulation of defence and stress genes by EARmotif-containing repressors. Trends Plant Sci 11: 109-112
44. Kiełbowicz-Matuk A (2012) Involvement of plant C(2)H(2)-type zinc finger transcription factors in stress responses. Plant Sci 185-186: 78-85
45. Kim SH, Hong JK, Lee SC, Sohn KH, Jung HW, Hwang BK (2004) CAZFP1, Cys2/His2-type zinc-finger transcription factor gene functions as a pathogen-induced early-defense gene in Capsicum annuum. Plant Mol Biol 55: 883-904
46. Kobayashi M, Horiuchi H, Fujita K, Takuhara Y, Suzuki S (2012) Characterization of grape C-repeat-binding factor 2 and B-box-type zinc finger protein in transgenic Arabidopsis plants under stress conditions. Mol Biol Rep 39: 7933-7939
47. Kodaira KS, Qin F, Tran LS, Maruyama K, Kidokoro S, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K (2011) Arabidopsis Cys2/His2 zinc-finger proteins AZF1 and AZF2 negatively regulate abscisic acidrepressive and auxin-inducible genes under abiotic stress conditions. Plant Physiol 157: 742-756
48. Koornneef M, Hanhart CJ, Hilhorst HW, Karssen CM (1989) In vivo inhibition of seed development and reserve protein accumulation in recombinants of abscisic acid biosynthesis and responsiveness mutants in Arabidopsis thaliana. Plant Physiol 90: 463-469
49. Kubo KI, Sakamoto A, Kobayashi A, Rybka Z, Kanno Y, Nakagawa H, Takatsuji H (1998) Cys2/His2 zinc-finger protein family of petunia: evolution and general mechanism of target-sequence recognition. Nucleic Acids Res 26: 608-615
50. Kulik A, Wawer I, Krzywinska E, Bucholc M, Dobrowolska G (2011) SnRK2 protein kinases-key regulators of plant response to abiotic stresses. OMICS 15: 859-872
51. Lefèvre I, Gratia E, Lutts S (2001) Discrimination between the ionic and osmotic components of salt stress in relation to free polyamine level in rice (Oryza sativa). Plant Sci 161: 943-952
52. Lin PC, Pomeranz MC, Jikumaru Y, Kang SG, Hah C, Fujioka S, Kamiya Y, Jang JC (2011) The Arabidopsis tandem zinc finger protein AtTZF1 affects ABA-and GA-mediated growth, stress and gene expression responses. Plant J 65: 253-268
53. Linkies A, Leubner-Metzger G (2012) Beyond gibberellins and abscisic acid: how ethylene and jasmonates control seed germination. Plant Cell Rep 31: 253-270
54. Lovelli S, Scopa A, Perniola M, Di Tommaso T, Sofo A (2012) Abscisic acid root and leaf concentration in relation to biomass partitioning in salinized tomato plants. J Plant Physiol 169: 226-233
55. Mangeon A, Junqueira RM, Sachetto-Martins G (2010) Functional diversity of the plant glycine-rich proteins superfamily. Plant Signal Behav 5: 99-104
56. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51: 659-668
57. Mishra G, Zhang W, Deng F, Zhao J, Wang X (2006) A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis. Science 312: 264-266
58. 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
59. Mittova V, Tal M, Volokita M, Guy M (2002) Salt stress induces upregulation of an efficient chloroplast antioxidant system in the salttolerant wild tomato species Lycopersicon pennellii but not in the cultivated species. Physiol Plant 115: 393-400
60. Mitsuya Y, Takahashi Y, Uehara Y, Berberich T, Miyazaki A, Takahashi H, Kusano T (2007) Identification of a novel Cys2/His2-type zinc-finger protein as a component of a spermine-signaling pathway in tobacco. J Plant Physiol 164: 785-793
61. Mizoguchi T, Wright L, Fujiwara S, Cremer F, Lee K, Onouchi H, Mouradov A, Fowler S, Kamada H, Putterill J, et al (2005) Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 17: 2255-2270
62. Nakai K, Horton P (1999) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24: 34-36
63. Nakashima K, Yamaguchi-Shinozaki K (2013) ABA signaling in stressresponse and seed development. Plant Cell Rep 32: 959-970
64. Neily MH, Matsukura C, Maucourt M, Bernillon S, Deborde C, Moing A, Yin YG, Saito T, Mori K, Asamizu E, et al (2011) Enhanced polyamine accumulation alters carotenoid metabolism at the transcriptional level in tomato fruit overexpressing spermidine synthase. J Plant Physiol 168: 242-252
65. Ohta M, Matsui K, Hiratsu K, Shinshi H, Ohme-Takagi M (2001) Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. Plant Cell 13: 1959-1968
66. Ouyang B, Yang T, Li H, Zhang L, Zhang Y, Zhang J, Fei Z, Ye Z (2007) Identification of early salt stress response genes in tomato root by suppression subtractive hybridization and microarray analysis. J Exp Bot 58: 507-520
67. Pabo CO, Peisach E, Grant RA (2001) Design and selection of novel Cys2His2 zinc finger proteins. Annu Rev Biochem 70: 313-340
68. Penfield S, Hall A (2009) A role for multiple circadian clock genes in the response to signals that break seed dormancy in Arabidopsis. Plant Cell 21: 1722-1732
69. Putterill J, Robson F, Lee K, Simon R, Coupland G (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80: 847-857
70. Quinet M, Vromman D, Clippe A, Bertin P, Lequeux H, Dufey I, Lutts S, Lefèvre I (2012) Combined transcriptomic and physiological approaches reveal strong differences between short-and long-term response of rice (Oryza sativa) to iron toxicity. Plant Cell Environ 35: 1837-1859
71. 2)-type zinc-finger protein gene family under water stress. Gene 248: 23-32
72. Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol 136: 2734-2746
73. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, et al (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31: 279-292
74. Shpak ED, Berthiaume CT, Hill EJ, Torii KU (2004) Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation. Development 131: 1491-1501
75. Solanke AU, Sharma MK, Tyagi AK, Sharma AK (2009) Characterization and phylogenetic analysis of environmental stress-responsive SAP gene family encoding A20/AN1 zinc finger proteins in tomato. Mol Genet Genomics 282: 153-164
76. Sturaro M, Vernieri P, Castiglioni P, Binelli G, Gavazzi G (1996) The rea (red embryonic axis) phenotype describes a new mutation affecting the response of maize embryos to abscisic acid and osmotic stress. J Exp Bot 47: 755-762
77. Subramanian C, Woo J, Cai X, Xu X, Servick S, Johnson CH, Nebenführ A, von Arnim AG (2006) A suite of tools and application notes for in vivo protein interaction assays using bioluminescence resonance energy transfer (BRET). Plant J 48: 138-152
78. Sun SJ, Guo SQ, Yang X, Bao YM, Tang HJ, Sun H, Huang J, Zhang HS (2010) Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice. J Exp Bot 61: 2807-2818
79. Takatsuji H, Matsumoto T (1996) Target-sequence recognition by separatetype Cys2/His2 zinc finger proteins in plants. J Biol Chem 271: 23368-23373
80. Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2005) Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol 138: 2337-2343
81. Tian ZD, Zhang Y, Liu J, Xie CH (2010) Novel potato C2H2-type zinc finger protein gene, StZFP1, which responds to biotic and abiotic stress, plays a role in salt tolerance. Plant Biol (Stuttg) 12: 689-697
82. Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635-641
83. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RTPCR data by geometric averaging of multiple internal control genes. Genome Biol 3: Research0034.1-Research0034.11
84. Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Close TJ (2007) Large-scale expression profiling and physiological characterization of jasmonic acid-mediated adaptation of barley to salinity stress. Plant Cell Environ 30: 410-421
85. Wang RS, Pandey S, Li S, Gookin TE, Zhao Z, Albert R, Assmann SM (2011) Common and unique elements of the ABA-regulated transcriptome of Arabidopsis guard cells. BMC Genomics 12: 216
86. Xing HT, Guo P, Xia XL, Yin WL (2011) PdERECTA, a leucine-rich repeat receptor-like kinase of poplar, confers enhanced water use efficiency in Arabidopsis. Planta 234: 229-241
87. Xu DQ, Huang J, Guo SQ, Yang X, Bao YM, Tang HJ, Zhang HS (2008) Overexpression of a TFIIIA-type zinc finger protein gene ZFP252 enhances drought and salt tolerance in rice (Oryza sativa L.). FEBS Lett 582: 1037-1043
88. Yan J, Tsuichihara N, Etoh T, Iwai S (2007) Reactive oxygen species and nitric oxide are involved in ABA inhibition of stomatal opening. Plant Cell Environ 30: 1320-1325
89. Zhang H, Han B, Wang T, Chen S, Li H, Zhang Y, Dai S (2012) Mechanisms of plant salt response: insights from proteomics. J Proteome Res 11: 49-67
90. Zhang X, Guo XP, Lei CL, Chen Z, Lin Q, Wang J, Wu FQ, Wang J, Wan J (2011) Overexpression of SlCZFP1, a novel TFIIIA-type zinc finger protein from tomato, confers enhanced cold tolerance in transgenic Arabidopsis and rice. Plant Mol Biol Rep 29: 185-196