Cloning of the lycopene β-cyclase gene in nicotiana tabacum and its overexpression confers salt and drought tolerance

International Journal of Molecular Sciences

Volumn 16, Issue 12, 2015, Pages 30438-30457

  Shi, Yanmei ^a,b   Guo, Jinggong ^c   Zhang, Wei ^d   Jin, Lifeng ^b   Liu, Pingping ^b   Chen, Xia ^b   Li, Feng ^b   Wei, Pan ^b   Li, Zefeng ^b   Li, Wenzheng ^e   Wei, Chunyang ^f   Zheng, Qingxia ^b   Chen, Qiansi ^b   Zhang, Jianfeng ^b   Lin, Fucheng ^b   Qu, Lingbo ^a   Snyder, John Hugh ^b   Wang, Ran ^b  

^a ZHENGZHOU UNIVERSITY   (China)

^b ZHENGZHOU TOBACCO RESEARCH INSTITUTE OF CNTC   (China)

^c HENAN UNIVERSITY   (China)

^d China National Tobacco Quality Supervision and Test Centre   (China)

^e Yunnan Academy of Tobacco Agricultural Sciences   (China)

^f Staff Development Institute of CNTC   (China)

Author keywords

Abscisic acid; Carotenoid biosynthesis; Lycopene cyclase; Nicotiana tabacum; Reactive oxygen species; Salt and drought tolerance

Indexed keywords

AMINO ACID SEQUENCE; ARTICLE; CHLOROPHYLL CONTENT; CONTROLLED STUDY; CYCLIZATION; DROUGHT TOLERANCE; GENE; GENE OVEREXPRESSION; GENOTYPE PHENOTYPE CORRELATION; LYCOPENE BETA CYCLASE GENE; NICOTIANA TABACUM; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALT TOLERANCE; SEQUENCE ANALYSIS; DROUGHT; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGICAL STRESS; TOBACCO;

ABSCISIC ACID; ISOMERASE; LYCOPENE CYCLASE-ISOMERASE; PLANT PROTEIN; REACTIVE OXYGEN METABOLITE;

ABSCISIC ACID; AMINO ACID SEQUENCE; DROUGHTS; INTRAMOLECULAR LYASES; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT PROTEINS; REACTIVE OXYGEN SPECIES; SALT-TOLERANCE; STRESS, PHYSIOLOGICAL; TOBACCO;

EID: 84951325964     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms161226243     Document Type: Article

References (57)

1. Mahajan, S.; Tuteja, N. Cold, salinity and drought stresses: An overview. Arch. Biochem. Biophys. 2005, 444, 139-158. [CrossRef] [PubMed]
2. Bromham, L.; Saslis-Lagoudakis, C.H.; Bennett, T.H.; Flowers, T.J. Soil alkalinity and salt tolerance: adapting to multiple stresses. Biol. Lett. 2013, 9, 1744. [CrossRef] [PubMed]
3. Evers, D.; Lefevre, I.; Legay, S.; Lamoureux, D.; Hausman, J.F.; Rosales, R.O.G.; Marca, L.R.T.; Hoffmann, L.; Bonierbale, M.; Schafleitner, R. Identification of drought-responsive compounds in potato through a combined transcriptomic and targeted metabolite approach. J. Exp. Bot. 2010, 61, 2327-2343. [CrossRef] [PubMed]
4. Natwar, S.; Avinash, M.; Bhavanath, J. Over-expression of the Peroxisomal Ascorbate Peroxidase (SbpAPX) gene cloned from Halophyte Salicornia brachiata confers salt and drought stress tolerance in transgenic Tobacco. Mar. Biotechnol. 2014, 16, 321-332.
5. Wu, G.; Wang, G.; Ji, J.; Gao, H.; Guan, W.; Wu, J.; Guan, C.; Wang, Y. Cloning of a cytosolic ascorbate peroxidase gene from Lycium chinense Mill. and enhanced salt tolerance by overexpressing in tobacco. Gene 2014, 543, 85-92. [CrossRef] [PubMed]
6. Zhang, D.Y.; Yang, H.L.; Li, X.S.; Li, H.Y.; Wang, Y.C. Overexpression of Tamarix albiflonum TaMnSOD increases drought tolerance in transgenic cotton. Mol. Breed. 2014, 34, 1-11. [CrossRef]
7. Tang, L.L.; Cai, H.; Zhai, H.; Luo, X.; Wang, Z.Y.; Cui, L.; Bai, X. Overexpression of Glycine soja WRKY20 enhances both drought and salt tolerance in transgenic alfalfa (Medicago sativa L.). Plant Cell Tissue Organ Cult. 2014, 118, 77-86. [CrossRef]
8. Xu, Q.; He, Q.; Li, S.; Tian, Z. Molecular characterization of StNAC2 in potato and its overexpression confers drought and salt tolerance. Acta Physiol. Plant 2014, 36, 1841-1851. [CrossRef]
9. Min, D.H.; Zhao, Y.; Huo, D.Y.; Li, L.C.; Chen, M.; Xu, Z.S.; Ma, Y.Z. Isolation and identification of a wheat gene encoding a zinc finger protein (TaZnFP) responsive to abiotic stresses. Acta Physiol. Plant 2013, 35, 1597-1604. [CrossRef]
10. Sun, P.P.; Zhu, X.F.; Huang, X.S.; Liu, J.H. Overexpression of a stress-responsive MYB transcription factor of Poncirus trifoliata confers enhanced dehydration tolerance and increases polyamine biosynthesis. Plant Physiol. Biochem. 2014, 78, 71-79. [CrossRef] [PubMed]
11. Muhammad, R.; Khurram, S.; Rashid, A.; Moddassir, A.; Imran, H.; Shahid, M.; Gerald, A.B.; Nasir, A.S. Cloning and characterization of Na+/H+ antiporter (LfNHX1) gene from a halophyte grass Leptochloa fusca for drought and salt tolerance. Mol. Biol. Rep. 2014, 41, 1669-1682.
12. Yarra, R.; He, S.J.; Abbagani, S.; Ma, B.; Bulle, M.; Zhang, W.K. Overexpression of a wheat Na+/H+ antiporter gene (TaNHX2) enhances tolerance to salt stress in transgenic tomato plants (Solanum lycopersicum L.). Plant Cell Tissue Organ Cult. 2012, 111, 49-57. [CrossRef]
13. Bramley, P.M. The regulation and genetic manipulation of carotenoid biosynthesis in tomato fruit. Pure Appl. Chem. 1997, 69, 2159-2162. [CrossRef]
14. Dall'Osto, L.; Fiore, A.; Cazzaniga, S.; Giuliano, G.; Bassi, R. Different roles of α-and β-branch xanthophylls in photosystem assembly and photoprotection. J. Biol. Chem. 2007, 282, 35056-35068. [CrossRef] [PubMed]
15. Andrade-Souza, V.; Costa, M.G.C.; Chen, C.X.; Gmitter, F.G., Jr.; Costa, M.A. Physical location of the carotenoid biosynthesis genes Psy and b-Lcy in Capsicum annuum (Solanaceae) using heterologous probes from Citrus sinensis (Rutaceae). Genet. Mol. Res. 2011, 10, 404-409. [CrossRef] [PubMed]
16. Nambara, E.; Marion-Poll, A. Abscisic acid biosynthesis and catabolism. Annu. Rev. Plant Biol. 2005, 56, 165-185. [CrossRef] [PubMed]
17. Taylor, I.B.; Sonneveld, T.; Bugg, T.D.H.; Thompson, A.J. Regulation and manipulation of the biosynthesis of abscisic acid, including the supply of xanthophyll precursors. J. Plant Growth Regul. 2005, 24, 253-273. [CrossRef]
18. Miller, G.; Suzuki, N.; Ciftci-Yilmaz, S.; Mittler, R. Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ. 2010, 33, 453-467. [CrossRef] [PubMed]
19. Götz, T.; Sandmann, G.; Römer, S. Expression of bacterial carotene hydroxylase gene (crtZ) enhances UV tolerance in tobacco. Plant Mol. Biol. 2002, 50, 127-140. [CrossRef]
20. Davison, P.A.; Hunter, C.N.; Horton, P. Overexpression of β-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 2002, 418, 203-206. [CrossRef] [PubMed]
21. Han, H.; Li, Y.; Zhou, S. Overexpression of phytoene synthase gene from Salicornia europaea alters response to reactive oxygen species under salt stress in transgenic Arabidopsis. Biotechnol. Lett. 2008, 30, 1501-1507. [CrossRef] [PubMed]
22. Howitt, C.A.; Cavanagh, C.R.; Bowerman, A.F.; Cazzonelli, C.; Rampling, L.; Mimica, J.L.; Pogson, B.J. Alternative splicing, activation of cryptic exons and amino acid substitutions in carotenoid biosynthetic genes are associated with lutein accumulation in wheat endosperm. Funct. Integr. Genom. 2009, 9, 363-376. [CrossRef] [PubMed]
23. Harjes, C.E.; Rocheford, T.R.; Bai, L.; Brutnell, T.P.; Kandianis, C.B.; Sowinski, S.G.; Stapleton, A.E.; Vallabhaneni, R.; Williams, M.; Wurtzel, E.T.; et al. Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification. Science 2008, 319, 330-333. [CrossRef] [PubMed]
24. Apel, W.; Bock, R. Enhancement of carotenoid biosynthesis in transplastomic tomatoes by induced lycopene-to-provitamin A conversion. Plant Physiol. 2009, 151, 59-66. [CrossRef] [PubMed]
25. Diretto, G.; Welsch, R.; Tavazza, R.; Mourgues, F.; Pizzichini, D.; Beyer, P.; Giuliano, G. Silencing of beta-carotene hydroxylase increases total carotenoid and beta-carotene levels in potato tubers. BMC Plant Biol. 2007, 7, 11. [CrossRef] [PubMed]
26. Bang, H.; Kim, S.; Leskovar, D.; King, S. Development of a codominant CAPS marker for allelic selection between canary yellow and red watermelon based on SNP in lycopene β-cyclase (LCYB) gene. Mol. Breed. 2007, 20, 63-72. [CrossRef]
27. Cazzonelli, C.I.; Pogson, B.J. Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci. 2010, 15, 266-274. [CrossRef] [PubMed]
28. D'Ambrosio, C.; Giorio, G.; Marino, I.; Merendino, A.; Petrozza, A.; Salfi, L.; Stigliani, A.; Cellini, F. Virtually complete conversion of lycopene into β-carotene in fruits of tomato plants transformed with the tomato lycopene β-cyclase (tlcy-β) cDNA. Plant Sci. 2004, 166, 207-214. [CrossRef]
29. Cunningham, F.X.; Pogson, B.; Sun, Z.; McDonald, K.A.; DellaPenna, D.; Gantt, E. Functional analysis of the beta and epsilon lycopene cyclase enzymes of Arabidopsis reveals a mechanism for control of cyclic carotenoid formation. Plant Cell 1996, 8, 1613-1626. [CrossRef] [PubMed]
30. Tian, L.; Musetti, V.; Kim, J.; Magallanes-Lundback, M.; DellaPenna, D. The Arabidopsis LUT1 locus encodes a member of the cytochrome P450 family that is required for carotenoid epsilon-ring hydroxylation activity. Proc. Natl. Acad. Sci. USA 2004, 101, 402-407. [CrossRef] [PubMed]
31. Guo, F.; Zhou, W.; Zhang, J.; Xu, Q.; Deng, X. Effect of the Citrus Lycopene β-Cyclase Transgene on Carotenoid Metabolism in Transgenic Tomato Fruits. PLoS ONE 2012, 7, e32221. [CrossRef] [PubMed]
32. Chen, X.Y.; Han, H.P.; Jiang, P.; Nie, L.L.; Bao, H.X.; Fan, P.X.; Lv, S.; Feng, J.; Li, Y. Transformation of β-lycopene cyclase genes from Salicornia europaea and Arabidopsis conferred salt tolerance in Arabidopsis and tobacco. Plant Cell Physiol. 2011, 52, 909-921. [CrossRef] [PubMed]
33. Tamura, K.; Peterson, D.; Peterson, N.; Stecher, G.; Nei, M.; Kumar, S. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28, 2731-2739. [CrossRef] [PubMed]
34. Robles, P.; Micol, J.L.; Quesada, V. Arabidopsis MDA1, a nuclearencoded protein, functions in chloroplast development and abiotic stress responses. PLoS ONE 2012, 7, e42924. [CrossRef] [PubMed]
35. Zhou, M.L.; Ma, J.T.; Zhao, Y.M.; Wei, Y.H.; Tang, Y.X.; Wu, Y.M. Improvement of drought and salt tolerance in Arabidopsis and Lotus corniculatus by overexpression of a novel DREB transcription factor from Populus euphratica. Gene 2012, 506, 10-17. [CrossRef] [PubMed]
36. Danquah, A.; de Zelicourt, A.; Colcombet, J.; Hirt, H. The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol. Adv. 2014, 32, 40-52. [CrossRef] [PubMed]
37. Liu, J.X.; Chiou, C.Y.; Shen, C.H.; Chen, P.J.; Liu, Y.C.; Jian, C.D.; Shen, X.L.; Shen, F.Q.; Yeh, K.W. RNA interference-based gene silencing of phytoene synthase impairs growth, carotenoids, and plastid phenotype in Oncidium hybrid orchid. SpringerPlus 2014, 3, 478. [CrossRef] [PubMed]
38. Kim, S.H.; Jeong, J.C.; Park, S.; Bae, J.Y.; Ahn, M.J.; Lee, H.S.; Kwak, S.S. Down-regulation of sweetpotato lycopene β-cyclase gene enhances tolerance to abiotic stress in transgenic calli. Mol. Biol. Rep. 2014, 41, 8137-8148. [CrossRef] [PubMed]
39. Pogson, B.J.; Rissler, H.M. Genetic manipulation of carotenoid biosynthesis and photoprotection. Philos. Trans. R. Soc. Lond. B 2000, 355, 1395-1403. [CrossRef] [PubMed]
40. De Azevedo Neto, A.D.; Prisco, J.T.; Enéas-Filho, J.; Braga de Abreu, C.E.; Gomes-Filho, E. Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ. Exp. Bot. 2006, 56, 87-94. [CrossRef]
41. Bode, S.; Quentmeier, C.C.; Liao, P.N.; Barrosc, T.; Walla, P.J. Xanthophyll-cycle dependence of the energy transfer between carotenoid dark states and chlorophylls in NPQ mutants of living plants and in LHC II. Chem. Phys. Lett. 2008, 450, 379-385. [CrossRef]
42. Demmig-Adams, B.; Adams,W.W. Antioxidants in photosynthesis and human nutrition. Science 2002, 298, 2149-2153. [CrossRef] [PubMed]
43. Parvaiz, A.; Satyawati, S. Salt stress and phyto-biochemical responses of plants-a review. Plant Soil Environ. 2008, 54, 89-99.
44. Jithesh, M.N.; Prashanth, S.R.; Sivaprakash, K.R.; Parida, A.K. Antioxidative response mechanisms in halophytes: Their role in stress defense. J. Genet. 2006, 85, 237-254. [CrossRef] [PubMed]
45. Kim, S.H.; Ahn, Y.O.; Ahn, M.J.; Lee, H.S.; Kwak, S.S. Down-regulation of β-carotene hydroxylase increases β-carotene and total carotenoids enhancing salt stress tolerance in transgenic cultured cells of sweet potato. Phytochemistry 2012, 74, 69-78. [CrossRef] [PubMed]
46. Shi, Y.M.; Wang, R.; Luo, Z.P.; Jin, L.F.; Liu, P.P.; Chen, Q.S.; Li, Z.F.; Li, F.; Wei, C.Y.; Wu, M.Z.; et al. Molecular cloning and functional characterization of the lycopene "-Cyclase gene via virus-induced gene silencing and its expression pattern in Nicotiana tabacum. Int. J. Mol. Sci. 2014, 15, 14766-14785. [CrossRef] [PubMed]
47. Shi, Y.M.; Liu, P.P.; Xia, Y.Z.; Wei, P.; Li, W.Z.; Zhang, W.; Chen, X.; Cao, P.J.; Xu, Y.L.; Jin, L.F.; et al. Downregulation of the lycopene #-cyclase gene confers tolerance to salt and drought stress in Nicotiana tabacum. Acta Physiol. Plant 2015, 37, 210. [CrossRef]
48. Kim, S.H.; Kim, Y.H.; Ahn, Y.O.; Ahn, M.J.; Jeong, J.C.; Lee, H.S.; Kwak, S.S. Down-regulation of the lycopene-#-cyclase gene increases carotenoid synthesis via the β-branch-specific pathway and enhances salt-stress tolerance in sweetpotato transgenic calli. Physiol. Plant 2012, 147, 432-442. [CrossRef] [PubMed]
49. Zhu, J.K. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 2002, 53, 247-273. [CrossRef] [PubMed]
50. Shinozaki, K.; Yamaguchi-Shinozaki, K. Gene expression and signal transduction in water-stress response. Plant Physiol. 1997, 115, 327-334. [CrossRef] [PubMed]
51. Pang, T.; Ye, C.Y.; Xia, X.L.; Yin, W.L. De novo sequencing and transcriptome analysis of the desert shrub, Ammopiptanthus mongolicus, during cold acclimation using Illumina/Solexa. BMC Genom. 2013, 14, 488. [CrossRef] [PubMed]
52. Horsch, R.B.; Fry, J.E.; Hoffmann, N.L.; Eicholtz, D.; Rogers, S.G.; Fraley, R.T. A simple method for transferring genes into plants. Science 1985, 227, 1229-1231.
53. Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt Method. Methods 2001, 25, 402-408. [CrossRef] [PubMed]
54. Boyer, J.S. Measurement of the water status of plants. Annu. Rev. Plant Physiol. 1969, 9, 351-363. [CrossRef]
55. Zhang, X.; Wang, L.; Meng, H.; Wen, H.T.; Fan, Y.L.; Zhao, J. Maize ABP9 enhances tolerance to multiple stresses in transgenic Arabidopsis by modulating ABA signaling and cellular levels of reactive oxygen species. Plant Mol. Biol. 2011, 75, 365-378. [CrossRef] [PubMed]
56. Wang, J.; Sun, P.P.; Chen, C.L.; Wang, Y.; Fu, X.Z.; Liu, J.H. An arginine decarboxylase gene PtADC from Poncirus trifoliata confers abiotic stress tolerance and promotes primary root growth in Arabidopsis. J. Exp. Bot. 2011, 62, 2899-2914. [CrossRef] [PubMed]
57. Liu, H.B.; Li, X.H.; Xiao, J.H.; Wang, S.P. A convenient method for simultaneous quantification of multiple phytohormones and metabolites: Application in study of rice-bacterium interaction. Plant Methods 2012, 8, [CrossRef] [PubMed]