Enhanced tolerance to freezing in tobacco and tomato overexpressing transcription factor TERF2/LeERF2 is modulated by ethylene biosynthesis

Plant Molecular Biology

Volumn 73, Issue 3, 2010, Pages 241-249

  Zhang, Zhijin ^a,b,c   Huang, Rongfeng ^a,b,c  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b National Key Facility of Crop Gene Resources and Genetic Improvement   (China)

^c INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

ERF protein TERF2 LeERF2; Ethylene biosynthesis; Tobacco; Tolerance to freezing; Transcriptional regulation

Indexed keywords

LYCOPERSICON ESCULENTUM; NICOTIANA TABACUM;

1 AMINOCYCLOPROPANECARBOXYLIC ACID; 1-AMINOCYCLOPROPANE-1-CARBOXYLIC ACID; AMINO ACID; COMPLEMENTARY DNA; ETHYLENE; ETHYLENE DERIVATIVE; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

ADAPTATION; ARTICLE; BIOSYNTHESIS; DRUG EFFECT; FREEZING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEEDLING; SIGNAL TRANSDUCTION; TOBACCO; TOMATO; TRANSGENIC PLANT;

ADAPTATION, PHYSIOLOGICAL; AMINO ACIDS, CYCLIC; DNA, ANTISENSE; ETHYLENES; FREEZING; GENE EXPRESSION REGULATION, PLANT; LYCOPERSICON ESCULENTUM; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEEDLING; SIGNAL TRANSDUCTION; TOBACCO; TRANSCRIPTION FACTORS;

EID: 77953092166     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-010-9609-4     Document Type: Article

References (55)

1. Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of Arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell 9: 1859-1868.
2. 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. doi: 10. 1105/tpc. 108. 058941.
3. Aharoni A, Dixit S, Jetter R, Thoenes E, van Arkel G, Pereira A (2004) The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell 16: 2463-2480. doi: 10. 1105/tpc. 104. 022897.
4. Andriankaja A, Boisson-Dernier A, Frances L, Sauviac L, Jauneau A, Barker DG, de Carvalho-Niebel F (2007) AP2-ERF transcription factors mediate Nod factor dependent Mt ENOD11 activation in root hairs via a novel cis-regulatory motif. Plant Cell 19: 2866-2885. doi: 10. 1105/tpc. 107. 052944.
5. Berrocal-Lobo M, Molina A, Solano R (2002) Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J 29: 23-32.
6. Cao WH, Liu J, He XJ, Mu RL, Zhou HL, Chen SY, Zhang JS (2007) Modulation of ethylene responses affects plant salt-stress responses. Plant Physiol 143: 707-719. doi: 10. 1104/pp. 106. 094292.
7. Chakravarthy S, Tuori RP, D'Ascenzo MD, Fobert PR, Despres C, Martin GB (2003) The tomato transcription factor Pti4 regulates defense-related gene expression via GCC box and non-GCC box cis elements. Plant Cell 15: 3033-3050. doi: 10. 1105/tpc. 017574.
8. Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12: 444-451. doi: 10. 1016/j. tplants. 2007. 07. 002.
9. Ciardi JA, Deikman J, Orzolek MD (1997) Increased ethylene synthesis enhances chilling tolerance in tomato. Physiol Plant 101: 333-340.
10. Feng JX, Liu D, Pan Y, Gong W, Ma LG, Luo JC, Deng XW, Zhu YX (2005) An annotation update via cDNA sequence analysis and comprehensive profiling of developmental, hormonal or environmental responsiveness of the Arabidopsis AP2/EREBP transcription factor gene family. Plant Mol Biol 59: 853-868. doi: 10. 1007/s11103-005-1511-0.
11. Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to CBF cold response pathway. Plant Cell 14: 1675-1690. doi: 10. 1105/tpc. 003483.
12. Fukao T, Xu K, Ronald PC, Bailey-Serres J (2006) A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18: 2021-2034. doi: 10. 1105/tpc. 106. 043000.
13. Gao S, Zhang H, Tian Y, Li F, Zhang Z, Lu X, Chen X, Huang R (2008) Expression of TERF1 in rice regulates expression of stress-responsive genes and enhances tolerance to drought and high-salinity. Plant Cell Rep 27: 1787-1795. doi: 10. 1007/s00299-008-0602-1.
14. Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124: 1854-1865.
15. Gonzalez-Aguilar GA, Fortiz J, Cruz R, Baez R, Wang CY (2000) Methyl jasmonate reduces chilling injury and maintains postharvest quality of mango fruit. J Agric Food Chem 48: 515-519.
16. Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7: 465-471. doi: 10. 1016/j. pbi. 2004. 04. 007.
17. Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol 130: 639-648. doi: 10. 1104/pp. 006478.
18. Huang Z, Zhang Z, Zhang X, Zhang H, Huang D, Huang R (2004) Tomato TERF1 modulates ethylene response and enhances osmotic stress tolerance by activating expression of downstream genes. FEBS Lett 573: 110-116.
19. Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47: 141-153. doi: 10. 1093/pcp/pci230.
20. Jaglo KR, Kleff S, Amundsen KL, Zhang X, Haake V, Zhang JZ, Deits T, Thomashow MF (2001) Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol 127: 910-917. doi: 10. 1104/pp. 010548.
21. Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) ArabidopsisCBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280: 104-106.
22. Karaba A, Dixit S, Greco R, Aharoni A, Trijatmiko KR, Marsch-Martinez N, Krishnan A, Nataraja KN, Udayakumar M, Pereira A (2007) Improvement of water use efficiency in rice by expression of HARDY, an Arabidopsis drought and salt tolerance gene. Proc Natl Acad Sci USA 104: 15270-15275. doi: 10. 1073/pnas. 0707294104.
23. Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2004) A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought- and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol 45: 346-350.
24. Kendrick MD, Chang C (2008) Ethylene signaling: new levels of complexity and regulation. Curr Opin Plant Biol 11: 479-485. doi: 10. 1016/j. pbi. 2008. 06. 011.
25. Khan AA, Huang XL (1998) Synergistic enhancement of ethylene production and germination with kinetin and 1-aminocyclopropane-1-carboxylic acid in lettuce seeds exposed to salinity stress. Plant Physiol 87: 847-852.
26. Kim CY, Liu Y, Thorne ET, Yang H, Fukushige H, Gassmann W, Hildebrand D, Sharp RE, Zhang S (2003) Activation of a stress-responsive mitogen-activated protein kinase cascade induces the biosynthesis of ethylene in plants. Plant Cell 15: 2707-2718. doi: 10. 1105/tpc. 011411.
27. Kizis D, Lumbreras V, Pagès M (2001) Role of AP2/EREBP transcription factors in gene regulation during abiotic stress. FEBS Lett 498: 187-189.
28. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10: 1391-1406.
29. Ludwig AA, Saitoh H, Felix G, Freymark G, Miersch O, Wasternack C, Boller T, Jones JD, Romeis T (2005) Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proc Natl Acad Sci USA 102: 10736-10741. doi: 10. 1073/pnas. 0502954102.
30. Middleton PH, Jakab J, Penmetsa RV, Starker CG, Doll J, Kaló P, Prabhu R, Marsh JF, Mitra RM, Kereszt A, Dudas B, VandenBosch K, Long SR, Cook DR, Kiss GB, Oldroyd GE (2007) An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. Plant Cell 19: 1221-1234. doi: 10. 1105/tpc. 106. 048264.
31. Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140: 411-432. doi: 10. 1104/pp. 105. 073783.
32. Novillo F, Medina J, Salinas J (2007) Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon. Proc Natl Acad Sci USA 104: 21002-21007. doi: 10. 1073/pnas. 0705639105.
33. Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7: 173-182.
34. Park JM, Park CJ, Lee SB, Ham BK, Shin R, Paek KH (2001) Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell 13: 1035-1046.
35. Sasaki K, Mitsuhara I, Seo S, Ito H, Matsui H, Ohashi Y (2007) Two novel AP2/ERF domain proteins interact with cis-element VWRE for wound-induced expression of the tobacco tpoxN1 gene. Plant J 50: 1079-1092. doi: 10. 1111/j. 1365-313X. 2007. 03111. x.
36. Sessa G, Meller Y, Fluhr R (1995) A GCC element and a G-box motif participate in ethylene-induced expression of the PRB-1b gene. Plant Mol Biol 28: 145-153.
37. Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6: 410-417.
38. Singh K, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5: 430-436.
39. Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ethylene-insensitive3 and ethyleneresponse-factor1. Genes Dev 12: 3703-3714.
40. Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94: 1035-1040.
41. Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of Arabidopsis stress inducible NAC transcription factors that bind to a drought responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16: 2481-2498. doi: 10. 1105/tpc. 104. 022699.
42. Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97: 11632-11637. doi: 10. 1073/pnas. 190309197.
43. van der Fits L, Memelink J (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289: 295-297.
44. van der Fits L, Memelink J (2001) The jasmonate-inducible AP2/ERF-domain transcription factor ORCA3 activates gene expression via interaction with a jasmonate-responsive promoter element. Plant J 25: 43-53.
45. Vogel JT, Zarka DG, van Buskirk HA, Fowler SG, Thomashow MF (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41: 195-211. doi: 10. 1111/j. 1365-313X. 2004. 02288. x.
46. Wu L, Zhang Z, Zhang H, Wang XC, Huang R (2008) Transcriptional modulation of ethylene response factor protein JERF3 in the oxidative stress response enhances tolerance of tobacco seedlings to salt, drought, and freezing. Plant Physiol 148: 1953-1963. doi: 10. 1104/pp. 108. 126813.
47. Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442: 705-708. doi: 10. 1038/nature04920.
48. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57: 781-803. doi: 10. 1146/annurev. arplant. 57. 032905. 105444.
49. Yi SY, Kim JH, Joung YH, Lee S, Kim WT, Yu SH, Choi D (2004) The pepper transcription factor CaPF1 confers pathogen and freezing tolerance in Arabidopsis. Plant Physiol 136: 2862-2874. doi: 10. 1104/pp. 104. 042903.
50. Yu XM, Griffith M, Wiseman SB (2001) Ethylene induces antifreeze activity in winter rye leaves. Plant Physiol 126: 1232-1240.
51. Zhang JY, Broeckling CD, Blancaflor EB, Sledge MK, Sumner LW, Wang ZY (2005a) Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). Plant J 42: 689-707. doi: 10. 1111/j. 1365-313X. 2005. 02405. x.
52. Zhang X, Zhang Z, Chen J, Chen Q, Wang XC, Huang R (2005b) Expressing TERF1 in tobacco enhances drought tolerance and abscisic acid sensitivity during seedling development. Planta 222: 494-501. doi: 10. 1007/s00425-005-1564-y.
53. Zhang Z, Zhang H, Quan R, Wang XC, Huang R (2009) Transcriptional regulation of ethylene response factor LeERF2 in the expression of ethylene biosynthesis genes controls ethylene production in tomato and tobacco. Plant Physiol 150: 365-377. doi: 10. 1104/pp. 109. 135830.
54. Zhao D, Shen L, Fan B, Yu M, Zheng Y, Lv S, Sheng J (2009) Ethylene and cold participate in the regulation of LeCBF1 gene expression in postharvest tomato fruits. FEBS Lett 583: 3329-3334. doi: 10. 1016/j. febslet. 2009. 09. 029.
55. Zhou J, Tang X, Martin GB (1997) The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO J 16: 3207-3218. doi: 10. 1093/emboj/16. 11. 3207.