PtrABF of Poncirus trifoliata functions in dehydration tolerance by reducing stomatal density and maintaining reactive oxygen species homeostasis

Journal of Experimental Botany

Volumn 66, Issue 19, 2015, Pages 5911-5927

  Zhang, Qinghua ^a   Wang, Min ^a   Hu, Jianbing ^a   Wang, Wei ^a   Fu, Xingzheng ^a   Liu, Ji Hong ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

ABRE; Antioxidant enzyme; Arginine decarboxylase; Polyamine; Polyamine oxidase; Poncirus trifoliata; ROS; Stomatal development

Indexed keywords

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; PLANT PROTEIN; REACTIVE OXYGEN METABOLITE;

ADAPTATION; DROUGHT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOMEOSTASIS; METABOLISM; PHYSIOLOGY; PLANT STOMA; TRANSGENIC PLANT; TRIFOLIATE ORANGE;

ADAPTATION, PHYSIOLOGICAL; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; DROUGHTS; GENE EXPRESSION REGULATION, PLANT; HOMEOSTASIS; PLANT PROTEINS; PLANT STOMATA; PLANTS, GENETICALLY MODIFIED; PONCIRUS; REACTIVE OXYGEN SPECIES;

EID: 84942250330     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv301     Document Type: Article

References (63)

1. Alcázar R, Bitrián M, Bartels D, Koncz C, Altabella T, Tiburcio AF. 2011. Polyamine metabolic canalization in response to drought stress in Arabidopsis and the resurrection plant Craterostigma plantagineum. Plant Signaling and Behavior 6, 243-250.
2. Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF. 2010. Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231, 1237-1249.
3. An Z, Jing W, Liu Y, Zhang W. 2008. Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba. Journal of Experimental Botany 59, 815-825.
4. Casson SA, Hetherington AM. 2010. Environmental regulation of stomata development. Current Opinion in Plant Biology 13, 90-95.
5. Choi H, Hong JH, Ha JO, Kang JY, Kim SY. 2000. ABFs, a family of ABA-responsive element binding factors. Journal of Biological Chemistry 275, 1723-1730.
6. Cominelli E, Galbiati M, Tonelli C. 2010. Transcription factors controlling stomatal movements and drought tolerance. Transcription 1, 41-45.
7. Cuevas JC, López-Cobollo R, Alcázar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A. 2008. Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiology 148, 1094-1105.
8. Danquah A, de Zelicout A, Colcombet J, Hirt H. 2014. The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnology Advance 32, 40-52.
9. Fu XZ, Khan, EU, Hu SS, Fan QJ, Liu JH. 2011. Overexpression of the betaine aldehyde dehydrogenase gene from Atriplex hortensis enhances salt tolerance in the transgenic trifoliate orange (Poncirus trifoliata (L. ) Raf. ). Environmental and Experimental Botany 74, 106-113.
10. Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K. 2005. AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. The Plant Cell 17, 3470-3488.
11. Fujita Y, Yoshida T, Yamaguchi-Shinozaki K. 2013. Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiologia Plantarum 147, 15-27.
12. Hossain MA, Lee Y, Cho JI, Ahn CH, Lee SK, Jeon JS, Kang H, Lee CH, An G, Park PB. 2010. The bZIP transcription factor OsABF1 is an ABA responsive element binding factor that enhances abiotic stress signaling in rice. Plant Molecular Biology 72, 557-566.
13. Hsieh TH, Li CW, Su RC, Cheng CP, Sanjaya, Tsai YC, Chan MT. 2010. A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta 231, 1459-1473.
14. Huang SH, Yu CW, Lin CH. 2005. Hydrogen peroxide functions as a stress signal in plants. Botanical Bulletin of Academia Sinica 46, 1-10.
15. Huang XS, Liu JH, Chen XJ. 2010. Overexpression of PtrABF gene, a bZIP transcription factor isolated from Poncirus trifoliata, enhances dehydration and drought tolerance in tobacco via scavenging ROS and modulating expression of stress-responsive genes. BMC Plant Biology 10, 230.
16. Huang XS, Wang W, Zhang Q, Liu JH. 2013. A basic helix-loop-helix transcription factor PtrbHLH, of Poncirus trifoliata confers cold tolerance and modulates peroxidase-mediated scavenging of hydrogen peroxide. Plant Physiology 162, 1178-1194.
17. Jang SJ, Wi SJ, Choi YJ, An G, Park KY. 2012. Increased polyamine biosynthesis enhances stress tolerance by preventing the accumulation of reactive oxygen species: T-DNA mutational analysis of Oryza sativa lysine decarboxylase-like protein1. Molecules and Cells 34, 251-262.
18. Kanaoka MM, Pillitteri LJ, Fujii H, Yoshida Y, Bogenschutz NL, Takabayashi J, Zhu JK, Torii KU. 2008. SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation. The Plant Cell 20, 1775-1785.
19. 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 and Cell Physiology 45, 712-722.
20. Kang JY, Choi HI, Im MY, Kim SY. 2002. Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. The Plant Cell 14, 343-357.
21. Kim JB, Kang JY, Kim SY. 2004a. Over-expression of a transcription factor regulating ABA-responsive gene expression confers multiple stress tolerance. Plant Biotechnology Journal 2, 459-466.
22. Kim S, Kang JY, Cho DI, Park JH, Kim SY. 2004b. ABF2, an ABREbinding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. The Plant Journal 40, 75-87.
23. Kim SY. 2006. The role of ABF family bZIP class transcription factors in stress response. Physiologia Plantarum 126, 519-527.
24. Kusano T, Berberich T, Tateda C, Takahashi Y. 2008. Polyamines: essential factors for growth and survival. Planta 228, 367-381.
25. Liu JH, Kitashiba H, Wang J, Ban Y, Moriguchi T. 2007. Polyamines and their ability to provide environmental stress tolerance to plants. Plant Biotechnology 24, 117-126.
26. Liu, JH, Moriguchi T. 2007. Changes in free polyamine titers and expression of polyamine biosynthetic genes during growth of peach in vitro callus. Plant Cell Reports 26, 125-131.
27. Liu JH, Peng T, Dai WS. 2014. Critical cis-acting elements and interacting transcription factors: key players associated with abiotic stress responses in plants. Plant Molecular Biology Reporter 32, 303-317.
28. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-C(T) method. Methods 25, 402-408.
29. Luo X, Bai X, Sun X, et al. 2013. Expression of wild soybean WRKY20 in Arabidopsis enhances drought tolerance and regulates ABA signaling. Journal of Experimental Botany 64, 2155-2169.
30. Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill A. 2009. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324, 1064-1068.
31. MacAlister CA, Ohashi-Ito K, Bergmann DC. 2007. Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. Nature 445, 537-540.
32. Mehrotra R, Bhalothia P, Bansal P, Basantani MK, Bharti V, Mehrotra S. 2014. Abscisic acid and abiotic stress tolerance-different tiers of regulation. Journal of Plant Physiology 171, 486-496.
33. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R. 2010. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell and Environment 33, 453-467.
34. Minocha R, Majumdar R, Minocha SC. 2014. Polyamines and abiotic stress in plants: a complex relationship. Frontiers in Plant Science 5, 175.
35. Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA. 2008a. Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. The Plant Cell 20, 1708-1724.
36. Moschou PN, Sanmartin M, Andriopoulou AH, Rojo E, Sanchez-Serrano JJ, Roubelakis-Angelakis KA. 2008b. Bridging the gap between plant and mammalian polyamine catabolism: a novel peroxisomal polyamine oxidase responsible for a full back-conversion pathway in Arabidopsis. Plant Physiology 147, 1845-1857.
37. Muñiz García MN, Giammaria V, Grandellis C, Téllez-Iñón MT, Ulloa RM, Capiati DA. 2012. Characterization of StABF1, a stressresponsive bZIP transcription factor from Solanum tuberosum L. that is phosphorylated by StCDPK2 in vitro. Planta 235, 761-778.
38. Nakashima K, Yamaguchi-Shinozaki K. 2013. ABA signaling in stressresponse and seed development. Plant Cell Reports 32, 959-970.
39. Nilson SE, Assmann SM. 2007. The control of transpiration. Insights from Arabidopsis. Plant Physiology 143, 19-27.
40. Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, Kim M, Kim YK, Nahm BH, Kim JK. 2005. Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiology 138, 341-351.
41. Olvera-Carrillo Y, Reyes JL, Covarrubias AA. 2011. Late embryogenesis abundant proteins: versatile players in the plant adaptation to water limiting environments. Plant Signaling and Behavior 6, 586-589.
42. Orellana S, Yañez M, Espinoza A, Verdugo I, González E, Lara SR, Casaretto JA. 2010. The transcription factor SlAREB1 confers drought, salt stress tolerance and regulates biotic and abiotic stress-related genes in tomato. Plant, Cell and Environment 33, 2191-2208.
43. Park SY, Fung P, Nishimura N, et al. 2009. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324, 1068-1071.
44. Pillitteri LJ, Sloan DB, Bogenschutz NL, Torii KU. 2007. Termination of asymmetric cell division and differentiation of stomata. Nature 445, 501-505.
45. Pogány M, von Rad U, Grün S, Dongó A, Pintye A, Simoneau P, Bahnweg G, Kiss L, Barna B, Durner J. 2009. Dual roles of reactive oxygen species and NADPH oxidase RBOHD in an Arabidopsis-Alternaria pathosystem. Plant Physiology 151, 1459-1475.
46. Shi H, Chan Z. 2014. Improvement of plant abiotic stress tolerance through modulation of the polyamine pathway. Journal of Integrative Plant Biology 56, 114-121.
47. Shi J, Fu XZ, Peng T, Huang XS, Fan QJ, Liu JH. 2010. Spermine pretreatment confers dehydration tolerance of citrus in vitro plants via modulation of antioxidative capacity and stomatal response. Tree Physiology 30, 914-922.
48. Shi Y, Ding Y, Yang S. 2015. Cold signal transduction and its interplay with phytohormones during cold acclimation. Plant and Cell Physiology 56, 7-15.
49. Shinozaki K, Yamaguchi-Shinozaki K. 2007. Gene networks involved in drought stress response and tolerance. Journal of Experimental Botany 58, 221-227.
50. Tiburcio AF, Altabella T, Bitrián M, Alcázar R. 2014. The roles of polyamines during the lifespan of plants: from development to stress. Planta 240, 1-18.
51. Uno Y, Furuhata 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. Proceedings of the National Academy of Sciences, USA 97, 11632-11637.
52. Van Houtte H, Vandesteene L, López-Galvis L, et al. 2013. Overexpression of the trehalase gene AtTRE1 leads to increased drought stress tolerance in arabidopsis and is involved in abscisic acid-induced stomatal closure. Plant Physiology 161, 1158-1171.
53. Vanjildorj E, Bae TW, Riu KZ, Kim SY, Lee HY. 2005. Overexpression of Arabidopsis ABF3 gene enhances tolerance to drought and cold in transgenic lettuce (Lactuca sativa). Plant Cell, Tissue and Organ Culture 83, 41-50.
54. Vanjildorj E, Bae TW, Riu KZ, Yun PY, Park SY, Lee CH, Kim SY, Lee HY. 2006. Transgenic Agrostis mongolica Roshev. with enhanced tolerance to drought and heat stresses obtained from Agrobacterium-mediated transformation. Plant Cell, Tissue and Organ Culture 87, 109-120.
55. Walter M, Chaban C, Schütze K, et al. 2004. Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. The Plant Journal 40, 428-438.
56. Wang J, Sun PP, Chen CL, Wang Y, Fu XZ, Liu JH. 2011. An arginine decarboxylase gene PtADC from Poncirus trifoliata confers abiotic stress tolerance and promotes primary root growth in Arabidopsis. Journal of Experimental Botany 62, 2899-2914.
57. Wen XP, Ban Y, Inoue H, Matsuda N, Moriguchi T. 2010. Spermidine levels are implicated in heavy metal tolerance in a spermidine synthase overexpressing transgenic European pear by exerting antioxidant activities. Transgenic Research 19, 91-103.
58. Xian LH, Sun PP, Wu J, Hu SS, Liu JH. 2014. Molecular cloning and characterization of CrNCED1, a gene encoding 9-cis-epoxicarotenoid dioxygenase in Citrus reshni, with functions in tolerance to multiple abiotic stresses. Planta 239, 61-77.
59. Xie C, Zhang R, Qu Y, Miao Z, Zhang Y, Shen X, Wang T, Dong J. 2012. Overexpression of MtCAS31 enhances drought tolerance in transgenic Arabidopsis by reducing stomatal density. New Phytologist 195, 124-135.
60. Yáñez M, Cáceres S, Orellana S, Bastías A, Verdugo I, Ruiz-Lara S, Casaretto JA. 2009. An abiotic stress-responsive bZIP transcription factor from wild and cultivated tomatoes regulates stress-related genes. Plant Cell Reports 28, 1497-1507.
61. Yoshida T, Fujita Y, Maruyama K, Mogami J, Todaka D, Shinozaki K, Yamaguchi-Shinozaki K. 2015. Four Arabidopsis AREB/ABF transcription factors function predominantly in gene expression downstream of SnRK2 kinases in abscisic acid signalling in response to osmotic stress. Plant, Cell and Environment 38, 35-49.
62. Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. 2010. AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABREdependent ABA signaling involved in drought stress tolerance and require ABA for full activation. The Plant Journal 61, 672-685.
63. Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song CP. 2001. Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiology 126, 1438-1448.