Oil palm EgCBF3 conferred stress tolerance in transgenic tomato plants through modulation of the ethylene signaling pathway

Journal of Plant Physiology

Volumn 202, Issue , 2016, Pages 107-120

  Ebrahimi, Mortaza ^a,b   Abdullah, Siti Nor Akmar ^a   Abdul Aziz, Maheran ^a   Namasivayam, Parameswari ^a  

^a UNIVERSITY PUTRA MALAYSIA   (Malaysia)

^b AGRICULTURAL BIOTECHNOLOGY RESEARCH INSTITUTE OF IRAN ABRII   (Iran)

Author keywords

AP2 ERF; EgCBF3; Ethylene; Oil palm; Overexpression; Transgenic tomato

Indexed keywords

ETHYLENE; ETHYLENE DERIVATIVE; PALM OIL; PLANT PROTEIN; SODIUM CHLORIDE; VEGETABLE OIL;

ADAPTATION; ARECACEAE; BIOSYNTHESIS; COLD; DROUGHT; DRUG EFFECTS; FLOWER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT GENE; PLANT LEAF; PLANT ROOT; REPRODUCIBILITY; SIGNAL TRANSDUCTION; TOMATO; TRANSGENIC PLANT;

ADAPTATION, PHYSIOLOGICAL; ARECACEAE; BIOSYNTHETIC PATHWAYS; COLD TEMPERATURE; DROUGHTS; ETHYLENES; FLOWERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; LYCOPERSICON ESCULENTUM; PLANT LEAVES; PLANT OILS; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL;

EID: 84982854179     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2016.07.001     Document Type: Article

References (83)

1. AbuQamar, S., Luo, H., Laluk, K., Mickelbart, M.V., Mengiste, T., Crosstalk between biotic and abiotic stress responses in tomato is mediated by the AIM1 transcription factor. Plant J. 58 (2009), 347–360.
2. Achard, P., Gong, F., Cheminant, S., Alioua, M., Hedden, P., Genschik, P., 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 (2008), 2117–2129.
3. Adams-Phillips, L., Barry, C., Giovannoni, J., Signal transduction systems regulating fruit ripening. Trends Plant Sci. 9 (2004), 331–338.
4. Barry, C.S., Giovannoni, J.J., Ethylene and fruit ripening. J. Plant Growth Regul. 26 (2007), 143–159.
5. Barry, C.S., Llop-Tous, M.I., Grierson, D., The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato. Plant Physiol. 123 (2000), 979–986.
6. Bleecker, A.B., Kende, H., Ethylene: a gaseous signal molecule in plants. Annu. Rev. Cell Dev. Biol. 16 (2000), 1–18.
7. Caffagni, A., Pecchioni, N., Francia, E., Pagani, D., Milc, J., Candidate gene expression profiling in two contrasting tomato cultivars under chilling stress. Biol. Plant. 58 (2014), 283–295.
8. Ciardi, J.A., Deikman, J., Orzolek, M.D., Increased ethylene synthesis enhances chilling tolerance in tomato. Physiol. Plant. 101 (1997), 333–340.
9. Constabel, C.P., Bergey, D.R., Ryan, C.A., Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc. Natl. Acad. Sci. 92 (1995), 407–411.
10. Curtis, M.D., Grossniklaus, U., A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133 (2003), 462–469, 10.1104/pp.103.027979.
11. Druege, U., Ethylene and plant responses to abiotic stress. Ethylene Action in Plants, 2006, Springer, 81–118.
12. Ebrahimi, M., Abdullah, S.N.A., Aziz, M.A., Namasivayam, P., A novel CBF that regulates abiotic stress response and the ripening process in oil palm (Elaeis guineensis) fruits. Tree Genet. Genomes 11 (2015), 1–16.
13. Eck, J., Kirk, D., Walmsley, A., Tomato (Lycopersicum esculentum). Wang, K., (eds.) Agrobacterium Protocols SE – 39, Methods in Molecular Biology, 2006, Humana Press, 459–474, 10.1385/1-59745-130-4:459.
14. Florina, F., Giancarla, V., Cerasela, P., Sofia, P., The effect of salt stress on chlorophyll content in several Romanian tomato varieties. J. Hortic. For. Biotechnol. 17:1 (2013), 363–367.
15. Fontes, P.C.R., de Araujo, C., Use of a chlorophyll meter and plant visual aspect for nitrogen management in tomato fertigation. J Appl. Hortic. 8:1 (2006), 8–11.
16. Fowler, S., Thomashow, M.F., Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14 (2002), 1675–1690.
17. Gilmour, S.J., Zarka, D.G., Stockinger, E.J., Salazar, M.P., Houghton, J.M., Thomashow, M.F., Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold‐induced COR gene expression. Plant J. 16 (1998), 433–442.
18. Gilmour, S.J., Sebolt, A.M., Salazar, M.P., Everard, J.D., Thomashow, M.F., Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol. 124 (2000), 1854–1865.
19. Gilmour, S.J., Fowler, S.G., Thomashow, M.F., Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol. Biol. 54 (2004), 767–781.
20. Gopal, J., Iwama, K., In vitro screening of potato against water-stress mediated through sorbitol and polyethylene glycol. Plant Cell Rep. 26 (2007), 693–700.
21. Griffith, M., Yaish, M.W.F., Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci. 9 (2004), 399–405.
22. Gutha, L.R., Reddy, A.R., Rice DREB1B promoter shows distinct stress-specific responses, and the overexpression of cDNA in tobacco confers improved abiotic and biotic stress tolerance. Plant Mol. Biol. 68 (2008), 533–555.
23. Hon, W.-C., Griffith, M., Mlynarz, A., Kwok, Y.C., Yang, D.S.C., Antifreeze proteins in winter rye are similar to pathogenesis-related proteins. Plant Physiol. 109 (1995), 879–889.
24. Hsieh, T.-H., Lee, J., Charng, Y., Chan, M.-T., Tomato plants ectopically expressing Arabidopsis CBF1 show enhanced resistance to water deficit stress. Plant Physiol. 130 (2002), 618–626.
25. Hua, J., From freezing to scorching, transcriptional responses to temperature variations in plants. Curr. Opin. Plant Biol. 12 (2009), 568–573.
26. Jaglo-Ottosen, K.R., Gilmour, S.J., Zarka, D.G., Schabenberger, O., Thomashow, M.F., Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280 (1998), 104–106.
27. Jan, N., Andrabi, K.I., Cold resistance in plants: a mystery unresolved. Electron. J. Biotechnol. 12 (2009), 14–15.
28. Joo, S., Kim, W.T., A gaseous plant hormone ethylene: the signaling pathway. J. Plant Biol. 50 (2007), 109–116.
29. Kang, H., Saltveit, M.E., Activity of enzymatic antioxidant defense systems in chilled and heat shocked cucumber seedling radicles. Physiol. Plant. 113 (2001), 548–556.
30. Kasuga, M., Liu, Q., Miura, S., Yamaguchi-Shinozaki, K., Shinozaki, K., Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat. Biotechnol. 17 (1999), 287–291.
31. Lata, C., Prasad, M., Role of DREBs in regulation of abiotic stress responses in plants. J. Exp. Bot. 6 (2011), 1–18.
32. Li, H., Guo, H., Molecular basis of the ethylene signaling and response pathway in Arabidopsis. J. Plant Growth Regul. 26 (2007), 106–117.
33. Li, C.-W., Su, R.-C., Cheng, C.-P., You, S.-J., Hsieh, T.-H., Chao, T.-C., Chan, M.-T., Tomato RAV transcription factor is a pivotal modulator involved in the AP2/EREBP-mediated defense pathway. Plant Physiol. 156 (2011), 213–227.
34. Lissarre, M., Ohta, M., Sato, A., Miura, K., Cold-responsive gene regulation during cold acclimation in plants. Plant Signal. Behav. 5 (2010), 948–952.
35. Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K., Shinozaki, K., 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 (1998), 1391–1406.
36. Liu, J.-J., Sturrock, R., Ekramoddoullah, A.K.M., The superfamily of thaumatin-like proteins: its origin, evolution, and expression towards biological function. Plant Cell Rep. 29 (2010), 419–436.
37. Ma, B., Yin, C.-C., He, S.-J., Lu, X., Zhang, W.-K., Lu, T.-G., Chen, S.-Y., Zhang, J.-S., Ethylene-induced inhibition of root growth requires abscisic acid function in rice (Oryza sativa L.) seedlings. PLoS Genet., 2014.
38. Maruyama, H., Koyama, R., Oi, T., Yagi, M., Takeda, M., Kanechi, M., Inagaki, N., Uno, Y., In vitro evaluation of osmotic stress tolerance using a novel root recovery assay. Plant Cell Tissue Organ Cult. 95 (2008), 101–106.
39. Matsui, A., Ishida, J., Morosawa, T., Mochizuki, Y., Kaminuma, E., Endo, T.A., Okamoto, M., Nambara, E., Nakajima, M., Kawashima, M., Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol. 49 (2008), 1135–1149.
40. Medina, J., Catalá, R., Salinas, J., The CBFs: three Arabidopsis transcription factors to cold acclimate. Plant Sci. 180 (2011), 3–11.
41. Meyer, K., Keil, M., Naldrett, M.J., A leucine-rich repeat protein of carrot that exhibits antifreeze activity. FEBS Lett. 447 (1999), 171–178.
42. Miura, K., Furumoto, T., Cold signaling and cold response in plants. Int. J. Mol. Sci. 14 (2013), 5312–5337.
43. Moffatt, B., Ewart, V., Eastman, A., Cold comfort: plant antifreeze proteins. Physiol. Plant. 126 (2006), 5–16.
44. Monneveux, P., Ramírez, D.A., Pino, M.-T., Drought tolerance in potato (S. tuberosum L.): can we learn from drought tolerance research in cereals?. Plant Sci. 205 (2013), 76–86.
45. Narváez-Vásquez, J., Tu, C.-J., Park, S.-Y., Walling, L.L., Targeting and localization of wound-inducible leucine aminopeptidase A in tomato leaves. Planta 227 (2008), 341–351.
46. Nitsch, L.M.C., Oplaat, C., Feron, R., Ma, Q., Wolters-Arts, M., Hedden, P., Mariani, C., Vriezen, W.H., Abscisic acid levels in tomato ovaries are regulated by LeNCED1 and SlCYP707A1. Planta 229 (2009), 1335–1346.
47. Novillo, F., Alonso, J.M., Ecker, J.R., Salinas, J., CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 3985–3990.
48. Novillo, F., Medina, J., Salinas, J., 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. U. S. A. 104 (2007), 21002–21007.
49. Pech, J.-C., Latché, A., Bouzayen, M., Ethylene biosynthesis. Davies, P., (eds.) Plant Hormones SE – 6, 2010, Springer, Netherlands, 115–136, 10.1007/978-1-4020-2686-7_6.
50. Ramankutty, N., Evan, A.T., Monfreda, C., Foley, J.A., Farming the planet: 1. Geographic distribution of global agricultural lands in the year 2000. Global Biogeochem. Cycles, 22, 2008.
51. Sairam, R.K., Rao, K.V., Srivastava, G.C., Differential response of wheat genotypes to long-term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sci. 163 (2002), 1037–1046.
52. Sharabi-Schwager, M., Lers, A., Samach, A., Guy, C.L., Porat, R., Overexpression of the CBF2 transcriptional activator in Arabidopsis delays leaf senescence and extends plant longevity. J. Exp. Bot. 61 (2010), 261–273.
53. Sharabi-Schwager, M., Samach, A., Porat, R., Overexpression of the CBF2 transcriptional activator in Arabidopsis counteracts hormone activation of leaf senescence. Plant Signal. Behav. 5 (2010), 296–299.
54. Sharabi‐Schwager, M., Samach, A., Porat, R., Overexpression of the CBF2 transcriptional activator in Arabidopsis suppresses the responsiveness of leaf tissue to the stress hormone ethylene. Plant Biol. 12 (2010), 630–638.
55. Sharp, R.E., LeNoble, M.E., ABA, ethylene and the control of shoot and root growth under water stress. J. Exp. Bot. 53 (2002), 33–37.
56. Sharp, R.E., Interaction with ethylene: changing views on the role of abscisic acid in root and shoot growth responses to water stress. Plant. Cell Environ. 25 (2002), 211–222.
57. Shi, Y., Tian, S., Hou, L., Huang, X., Zhang, X., Guo, H., Yang, S., Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis. Plant Cell Online 24 (2012), 2578–2595.
58. Smart, R.E., Bingham, G.E., Rapid estimates of relative water content. Plant Physiol. 53 (1974), 258–260.
59. Spollen, W.G., LeNoble, M.E., Samuels, T.D., Bernstein, N., Sharp, R.E., Abscisic acid accumulation maintains maize primary root elongation at low water potentials by restricting ethylene production. Plant Physiol. 122 (2000), 967–976.
60. Stockinger, E.J., Gilmour, S.J., Thomashow, M.F., 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. U. S. A. 94 (1997), 1035–1040.
61. Thompson, A.J., Jackson, A.C., Parker, R.A., Morpeth, D.R., Burbidge, A., Taylor, I.B., Abscisic acid biosynthesis in tomato: regulation of zeaxanthin epoxidase and 9-cis-epoxycarotenoid dioxygenase mRNAs by light/dark cycles, water stress and abscisic acid. Plant Mol. Biol. 42 (2000), 833–845.
62. Thompson, A.J., Jackson, A.C., Symonds, R.C., Mulholland, B.J., Dadswell, A.R., Blake, P.S., Burbidge, A., Taylor, I.B., Ectopic expression of a tomato 9‐cis‐epoxycarotenoid dioxygenase gene causes over‐production of abscisic acid. Plant J. 23 (2000), 363–374.
63. Tornero, P., Gadea, J., Conejero, V., Vera, P., Two PR-1 genes from tomato are differentially regulated and reveal a novel mode of expression for a pathogenesis-related gene during the hypersensitive response and development. Mol. Plant—Microbe Interact. 10 (1997), 624–634.
64. Umezawa, T., Fujita, M., Fujita, Y., Yamaguchi-Shinozaki, K., Shinozaki, K., Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr. Opin. Biotechnol. 17 (2006), 113–122.
65. Van Kan, J.A.L., Cozijnsen, T., Danhash, N., De Wit, P.J.G.M., Induction of tomato stress protein mRNAs by ethephon, 2,6-dichloroisonicotinic acid and salicylate. Plant Mol. Biol. 27 (1995), 1205–1213.
66. van Loon, L.C., Geraats, B.P.J., Linthorst, H.J.M., Ethylene as a modulator of disease resistance in plants. Trends Plant Sci. 11 (2006), 184–191.
67. Van Zhong, G., Burns, J.K., Profiling ethylene-regulated gene expression in Arabidopsis thaliana by microarray analysis. Plant Mol. Biol. 53 (2003), 117–131.
68. Walling, L.L., Recycling or regulation? The role of amino-terminal modifying enzymes. Curr. Opin. Plant Biol. 9 (2006), 227–233.
69. Weigel, D., The APETALA2 domain is related to a novel type of DNA binding domain. Plant Cell, 7, 1995, 388.
70. Worrall, D., Elias, L., Ashford, D., Smallwood, M., Sidebottom, C., Lillford, P., Telford, J., Holt, C., Bowles, D., A carrot leucine-rich-repeat protein that inhibits ice recrystallization. Science 282 (1998), 115–117.
71. Xiong, Y., Fei, S.-Z., Functional and phylogenetic analysis of a DREB/CBF-like gene in perennial ryegrass (Lolium perenne L.). Planta 224 (2006), 878–888.
72. Xu, F., Liu, Z., Xie, H., Zhu, J., Zhang, J., Kraus, J., Blaschnig, T., Nehls, R., Wang, H., Increased drought tolerance through the suppression of ESKMO1 gene and overexpression of CBF-related genes in Arabidopsis. PLoS One, 9(9), 2014, e106509.
73. Yamaguchi-Shinozaki, K., Shinozaki, K., A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6 (1994), 251–264.
74. Yang, Y., Li, R., Qi, M., In vivo analysis of plant promoters and transcription factors by agroinfiltration of tobacco leaves. Plant J. 22 (2000), 543–551.
75. Zeller, G., Henz, S.R., Widmer, C.K., Sachsenberg, T., Rätsch, G., Weigel, D., Laubinger, S., Stress‐induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. Plant J. 58 (2009), 1068–1082.
76. Zhang, Z., Huang, R., Enhanced tolerance to freezing in tobacco and tomato overexpressing transcription factor TERF2/LeERF2 is modulated by ethylene biosynthesis. Plant Mol. Biol. 73 (2010), 241–249.
77. Zhang, X., Fowler, S.G., Cheng, H., Lou, Y., Rhee, S.Y., Stockinger, E.J., Thomashow, M.F., Freezing‐sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing‐tolerant Arabidopsis. Plant J. 39 (2004), 905–919.
78. Zhang, H., Zhang, D., Chen, J., Yang, Y., Huang, Z., Huang, D., Wang, X.-C., Huang, R., Tomato stress-responsive factor TSRF1 interacts with ethylene responsive element GCC box and regulates pathogen resistance to Ralstonia solanacearum. Plant Mol. Biol. 55 (2004), 825–834.
79. Zhang, M., Yuan, B., Leng, P., The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. J. Exp. Bot. 60 (2009), 1579–1588.
80. Zhang, Z., Zhang, H., Quan, R., Wang, X.-C., Huang, R., Transcriptional regulation of the ethylene response factor LeERF2 in the expression of ethylene biosynthesis genes controls ethylene production in tomato and tobacco. Plant Physiol. 150 (2009), 365–377.
81. Zhang, L., Li, Z., Li, J., Wang, A., Ectopic overexpression of SsCBF1, a CRT/DRE-binding factor from the nightshade plant Solanum lycopersicoides, confers freezing and salt tolerance in transgenic Arabidopsis. PLoS One, 8, 2013, e61810.
82. Zhao, M., Liu, W., Xia, X., Wang, T., Zhang, W., Cold acclimation‐induced freezing tolerance of Medicago truncatula seedlings is negatively regulated by ethylene. Physiol. Plant. 152 (2014), 115–129.
83. Zhou, M., Xu, M., Wu, L., Shen, C., Ma, H., Lin, J., CbCBF from Capsella bursa-pastoris enhances cold tolerance and restrains growth in nicotiana tabacum by antagonizing with gibberellin and affecting cell cycle signaling. Plant Mol. Biol. 85 (2014), 259–275.