Molecular cloning and characterization of CrNCED1, a gene encoding 9-cis-epoxycarotenoid dioxygenase in Citrus reshni, with functions in tolerance to multiple abiotic stresses

Planta

Volumn 239, Issue 1, 2014, Pages 61-77

  Xian, Lihong ^a   Sun, Peipei ^a   Hu, Shuangshuang ^a   Wu, Juan ^a   Liu, Ji Hong ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

9 Cis epoxycarotenoid dioxygenase; Abiotic stress; Abscisic acid; Antioxidant defense; Citrus reshni; Osmotic adjustment; Reactive oxygen species

Indexed keywords

9 CIS EPOXY CAROTENOID DIOXYGENASE; 9-CIS-EPOXY-CAROTENOID DIOXYGENASE; ABSCISIC ACID; DIOXYGENASE; REACTIVE OXYGEN METABOLITE; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CITRUS; DROUGHT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; OXIDATIVE STRESS; PHYLOGENY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROMOTER REGION; SALT TOLERANCE; TOBACCO; TRANSGENIC PLANT;

ABSCISIC ACID; AMINO ACID SEQUENCE; CITRUS; CLONING, MOLECULAR; DIOXYGENASES; DROUGHTS; GENE EXPRESSION REGULATION, PLANT; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; PHYLOGENY; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; REACTIVE OXYGEN SPECIES; SALT-TOLERANCE; STRESS, PHYSIOLOGICAL; TOBACCO;

EID: 84891608688     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-013-1963-4     Document Type: Article

References (62)

1. Agusti J, Zapater M, Iglesias DJ, Cercos M, Tadeo FR, Talon M (2007) Differential expression of putative 9-cis-epoxycarotenoid dioxygenases and abscisic acid accumulation in water stressed vegetative and reproductive tissues of citrus. Plant Sci 172: 85-94.
2. Arc E, Sechet J, Corbineau F, Rajjou L, Marion-Poll A (2013) ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination. Frontiers Plant Sci 4: 63.
3. Aswath CR, Kim SH, Mo SY, Kim DH (2005) Transgenic plants of creeping bent grass harboring the stress inducible gene, 9-cis-epoxycarotenoid dioxygenase, are highly tolerant to drought and NaCl stress. Plant Growth Regul 47: 129-139.
4. Berli FJ, Moreno D, Piccoli P, Hespanhol-Viana L, Silva MF, Bressan-Smith R, Cavagnaro JB, Bottini R (2010) Abscisic acid is involved in the response of grape (Vitis vinifera L.) cv. Malbec leaf tissues to ultraviolet-B radiation by enhancing ultraviolet-absorbing compounds, antioxidant enzymes and membrane sterols. Plant Cell Environ 33: 1-10.
5. Blöchl A, March GG, Sourdioux M, Peterbauer T, Richter A (2005) Induction of raffinose oligosaccharide biosynthesis by abscisic acid in somatic embryos of alfalfa (Medicago sativa L.). Plant Sci 168: 1075-1082.
6. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
7. Chernys JT, Zeevaart JAD (2000) Characterization of the 9-cis-epoxycarotenoid dioxygenase gene family and the regulation of abscisic acid biosynthesis in avocado. Plant Physiol 124: 343-354.
8. Frey A, Effroy D, Anne Frey1, Lefebvre V, Seo M, Perreau F, Berger A, Sechet J, To A, North HM, Marion-Poll A (2012) Epoxycarotenoid cleavage by NCED5 fine-tunes ABA accumulation and affects seed dormancy and drought tolerance with other NCED family members. Plant J 70: 501-512.
9. 2 production and transcriptional alteration. BMC Plant Biol 11: 55.
10. 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. Physiol Plant 147: 15-27.
11. Gómez-Cadenas A, Tadeo FR, Talon M, Primo-Millo E (1996) Leaf abscission induced by ethylene in water-stressed intact seedlings of Cleopatra mandarin requires previous abscisic acid accumulation in roots. Plant Physiol 112: 401-408.
12. Gómez-Cadenas A, Arbona V, Jacas J, Primo-Millo E, Talon M (2002) Abscisic acid reduces leaf abscission and increases salt tolerance in citrus plants. J Plant Growth Regul 21: 234-240.
13. Horsh RB, Fry JE, Hoffmann NL, Eichholtz D, Rogers SC, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227: 1229-1231.
14. 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 Biol 10: 230.
15. Huang XS, Luo T, Fu XZ, Fan QJ, Liu JH (2011) Cloning and molecular characterization of a mitogen-activated protein kinase gene from Poncirus trifoliata whose ectopic expression confers dehydration/drought tolerance in transgenic tobacco. J Exp Bot 62: 5191-5206.
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 Physiol 162: 1178-1194.
17. Hwang SG, Chen HC, Huang WY, Chu YC, Shii CT, Cheng WH (2010) Ectopic expression of rice OsNCED3 in Arabidopsis increases ABA level and alters leaf morphology. Plant Sci 178: 12-22.
18. Iuchi S, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2000) A stress-inducible gene for 9-cis-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis under water stress in drought-tolerant cowpea. Plant Physiol 123: 553-562.
19. Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27: 325-333.
20. Janssen BJ, Gardner RC (1993) The use of transient GUS expression to develop an Agrobacterium-mediated gene transfer system for kiwifruit. Plant Cell Rep 13: 28-31.
21. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901-3907.
22. Jiang MY, Zhang JH (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53: 2401-2410.
23. Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress inducible transcription factor. Nat Biotechnol 17: 287-291.
24. Kumar S, Kaushal N, Nayyar H, Gaur P (2012) Abscisic acid induces heat tolerance in chickpea (Cicer arietinum L.) seedlings by facilitated accumulation of osmoprotectants. Acta Physiol Plant 34: 1651-1658.
25. Lefebvre V, North H, Frey A, Sotta B, Seo M, Okamoto M, Nambara E, Marion-Poll A (2006) Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. Plant J 45: 309-319.
26. Li XJ, Yang MF, Chen H, Qu LQ, Chen F, Shen SH (2010) Abscisic acid pretreatment enhances salt tolerance of rice seedlings: proteomic evidence. Biochim Biophys Acta (BBA) Proteins Proteomics 1804: 929-940.
27. Liu JH, Kitashiba H, Wang J, Ban Y, Moriguchi T (2007) Polyamines and their ability to provide environmental stress tolerance to plants. Plant Biotechnol 24: 117-126.
28. Liu JH, Inoue H, Moriguchi T (2008) Salt stress-mediated changes in free polyamine titers and expression of genes responsible for polyamine biosynthesis of apple in vitro shoots. Environ Exp Bot 62: 28-35.
29. Liu JH, Ban Y, Wen XP, Nakajima I, Moriguchi T (2009) Molecular cloning and expression analysis of an arginine decarboxylase gene from peach (Prunus persica). Gene 429: 10-17.
30. Liu H, Li X, Xiao J, Wang S (2012) A convenient method for simultaneous quantification of multiple phytohormones and metabolites: application in study of rice-bacterium interaction. Plant Methods 8: 2.
31. 2- and NO-induced antioxidant enzyme activities. Plant Physiol Biochem 47: 132-138.
32. 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.
33. 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.
34. Pan X, Welti R, Wang X (2010) Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nat Protoc 5: 986-992.
35. Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TFF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu JK, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324: 1068-1071.
36. Pizzio GA, Rodriguez L, Antoni R, Gonzalez-Guzman M, Yunta C, Merilo E, Kollist H, Albert A, Rodriguez PL (2013) The PYL4 A194T mutant uncovers a key role of PYL4-PP2CA interaction for ABA signaling and plant drought resistance. Plant Physiol doi: 10. 1104/pp. 113. 224162.
37. Qin XQ, Zeevaart JAD (1999) The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci USA 96: 15354-15361.
38. Qin X, Zeevaart JAD (2002) Overexpression of a 9-cis-epoxycarotenoid dioxygenase gene in Nicotiana plumbaginifolia increases abscisic acid and phaseic acid levels and enhances drought tolerance. Plant Physiol 128: 544-551.
39. Rodrigo MJ, Alquezar B, Zacarías L (2006) Cloning and characterization of two 9-cis-epoxycarotenoid dioxygenase genes, differentially regulated during fruit maturation and under stress conditions, from orange (Citrus sinensis L. Osbeck). J Exp Bot 57: 633-643.
40. Schwartz SH, Tan BC, Gage DA, Zeevaart JAD, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276: 1872-1874.
41. Seo M, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7: 41-48.
42. Shi B, Ni L, Zhang AY, Cao JM, Zhang H, Qin TT, Tan MP, Zhang JH, Jiang MY (2012) OsDMI3 is a novel component of abscisic acid signaling in the induction of antioxidant defense in leaves of rice. Mol Plant 5: 1359-1374.
43. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58: 221-227.
44. Shulaev V, Oliver DJ (2006) Metabolic and proteomic markers for oxidative stress. New tools for reactive oxygen species research. Plant Physiol 141: 367-372.
45. Silva-Ortega CO, Ochoa-Alfaro AE, Reyes-Agüero JA, Aguado-Santacruz GA, Jiménez-Bremont JF (2008) Salt stress increases the expression of p5cs gene and induces proline accumulation in cactus pear. Plant Physiol Biochem 46: 82-92.
46. Strizhov N, Ábrahám E, Ökrész L, Blickling S, Zilberstein A, Schell J, Koncz C, Szabados L (1997) Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. Plant J 12: 557-569.
47. 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.
48. Thompson AJ, Jackson AC, Symonds RC, Mulholland BJ, Dadswell AR, Blake PS, Burbidge A, Taylor IB (2000) Ectopic expression of a tomato 9-cis-epoxycarotenoid dioxygenase gene causes over-production of abscisic acid. Plant J 23: 363-374.
49. Thompson AJ, Mulholland BJ, Jackson AC, Mckee JMT, Hilton HW, Symonds RC, Sonneveld T, Burbidge A, Stevenson P, Taylor IB (2007) Regulation and manipulation of ABA biosynthesis in roots. Plant Cell Environ 30: 67-78.
50. Toh S, Imamura A, Watanabe A, Nakabayashi K, Okamoto M, Jikumaru Y, Hanada A, Ishiyama K, Tamura N, Iuchi S, Kobayashi M, Yamaguchi S, Kamiya Y, Nambara E, Kawakami N (2008) High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiol 146: 1368-1385.
51. Wan XR, Li L (2005) Molecular cloning and characterization of a dehydration-inducible cDNA encoding a putative 9-cis-epoxycarotenoid dioxygenase in Arachis hygogaea L. DNA Seq 16: 217-223.
52. Wan XR, Li L (2006) Regulation of ABA level and water-stress tolerance of Arabidopsis by ectopic expression of a peanut 9-cis-epoxycarotenoid dioxygenase gene. Biochem Biophys Res Commun 347: 1030-1038.
53. 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. J Exp Bot 62: 2899-2914.
54. Welsch R, Wüst F, Bär C, Al-Babili S, Beyer P (2008) A third phytoene synthase is devoted to abiotic stress-induced abscisic acid formation in rice and defines functional diversification of phytoene synthase genes. Plant Physiol 147: 367-380.
55. Xiong LM, Lee H, Ishitani M, Zhu JK (2002) Regulation of osmotic stress-responsive gene expression by the LOS6/ABA1 locus in Arabidopsis. J Biol Chem 277: 8588-8596.
56. Yang JF, Guo ZF (2007) Cloning of a 9-cis-epoxycarotenoid dioxygenase gene (SgNCED1) from Stylosanthes guianensis and its expression in response to abiotic stresses. Plant Cell Rep 26: 1383-1390.
57. Zhang X, Zhang L, Dong FC, Gao JF, Galbraith DW, Song CP (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126: 1438-1448.
58. Zhang AY, Jiang MY, Zhang JH, Tan MP, Hu XL (2006) Mitogen-activated protein kinase is involved in abscisic acid-induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiol 141: 475-487.
59. Zhang YM, Yang JF, Lu SY, Cai JL, Guo ZF (2008) Overexpressing SgNCED1 in tobacco increases ABA level, antioxidant enzyme activities, and stress tolerance. J Plant Growth Regul 27: 151-158.
60. Zhu CF, Kauder F, Römer S, Sandmann G (2007) Cloning of two individual cDNAs encoding 9-cis-epoxycarotenoid dioxygenase from Gentiana lutea, their tissue-specific expression and physiological effect in transgenic tobacco. Plant Physiol 164: 195-204.
61. Zhu Q, Song B, Zhang C, Ou Y, Xie C, Liu J (2008) Construction and functional characteristics of tuber-specific and cold-inducible chimeric promoters in potato. Plant Cell Rep 27: 47-55.
62. Zhu SQ, Chen MW, Ji BH, Jiao DM, Liang JS (2011) Roles of xanthophylls and exogenous ABA in protection against NaCl-induced photodamage in rice (Oryza sativa L) and cabbage (Brassica campestris). J Exp Bot 62: 4617-4625.