Downregulation of the lycopene ε-cyclase gene confers tolerance to salt and drought stress in Nicotiana tabacum

• Autorzy: Shi J. , Liu P. , Xia Y. , Wei P. , Li W. , Zhang W. , Chen X. , Cao P. , Xu Y. , Jin L. , Li F. , Luo Z. , Wei C. , Zhang J. , Xie X. , Qu L. , Yang J. , Lin F. , Wang R.
• Języki publikacji: EN

Abstrakty

EN

Lycopene ε-cyclase (ε-LCY) functions at a branch point of the carotenoid biosynthesis pathway and modulates the ratio of lutein to the β-carotenoids. RNA interference (RNAi) and overexpression (OE) of Ntε-LCY were used to evaluate the physiological roles of ε-LCY in Nicotiana tobacum. In leaves, strong accumulation of β branch carotenoids and high expression of carotenoid biosynthesis genes resulted from suppression of Ntε-LCY expression. RNAi plants showed enhanced salt and drought tolerance, while overexpression of the Ntε-LCY gene weakened tolerance to salt and drought stress, as compared to control. Further analysis revealed that RNAi plants exhibited less water loss and had lower reactive oxygen species levels than did WT plants after both the salt and drought treatments. Further, higher levels of ABA accumulated in the RNAi lines than in the WT lines under stress conditions. These results suggest that reduced Ntε-LCY expression can improve drought and salinity tolerance in Nicotiana tabacum by enhancing their ROS scavenging ability.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2015
• Tom: 37
• Numer: 10
• Opis fizyczny: Article: 210 [15 p.], fig.,ref.

Twórcy

autor

Shi J.

• College of Chemistry and Molecular Engineering, Zhengzhou University, Zhengzhou, 450001, People’s Republic of China
• Zhengzhou Tobacco Research Institute, Zhengzhou, 450001, People’s Republic of China

autor

Liu P.

• Zhengzhou Tobacco Research Institute, Zhengzhou, 450001, People’s Republic of China

autor

Xia Y.

• Hongta Tobacco (Group) Co. Ltd., Yuxi, 653100, People’s Republic of China

autor

Wei P.

• Zhengzhou Tobacco Research Institute, Zhengzhou, 450001, People’s Republic of China

autor

Li W.

• Yunnan Academy of Tobacco Agricultural Sciences, Kunming, 650031, Yunnan, People’s Republic of China

autor

Zhang W.

• China National Tobacco Quality Supervision and Test Centre, Zhengzhou, 450001, People’s Republic of China

autor

Chen X.

• Zhengzhou Tobacco Research Institute, Zhengzhou, 450001, People’s Republic of China

autor

Cao P.

• Zhengzhou Tobacco Research Institute, Zhengzhou, 450001, People’s Republic of China

autor

Xu Y.

• Zhengzhou Tobacco Research Institute, Zhengzhou, 450001, People’s Republic of China

autor

Jin L.

• Zhengzhou Tobacco Research Institute, Zhengzhou, 450001, People’s Republic of China

autor

Li F.

• Zhengzhou Tobacco Research Institute, Zhengzhou, 450001, People’s Republic of China

autor

Luo Z.

• Zhengzhou Tobacco Research Institute, Zhengzhou, 450001, People’s Republic of China

autor

Wei C.

• Zhengzhou Tobacco Research Institute, Zhengzhou, 450001, People’s Republic of China

autor

Zhang J.

• Zhengzhou Tobacco Research Institute, Zhengzhou, 450001, People’s Republic of China

autor

Xie X.

• Zhengzhou Tobacco Research Institute, Zhengzhou, 450001, People’s Republic of China

autor

Qu L.

• College of Chemistry and Molecular Engineering, Zhengzhou University, Zhengzhou, 450001, People’s Republic of China
• College of Chemistry and Chemical Engineering, Henan University of Technology, Zhengzhou, 450001, People’s Republic of China

autor

Yang J.

• Zhengzhou Tobacco Research Institute, Zhengzhou, 450001, People’s Republic of China

autor

Lin F.

• Zhengzhou Tobacco Research Institute, Zhengzhou, 450001, People’s Republic of China

autor

Wang R.

• Zhengzhou Tobacco Research Institute, Zhengzhou, 450001, People’s Republic of China

Bibliografia

• Agarwal PK, Shukla PS, Gupta K, Jha B (2013) Bioengineering for salinity tolerance in plants: state of the art. Mol Biotechnol 54:102–123. doi:10.1007/s12033-012-9538-3
• Bai L, Kim EH, DellaPenna D, Brutnell TP (2009) Novel lycopene-ecyclase activities in maize revealed through perturbation of carotenoid biosynthesis. Plant J 59:588–599. doi:10.1111/j.1365-313X.2009.03899.x
• Bode S, Quentmeier CC, Liao PN, Barrosc T, Walla PJ (2008) 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 450:379–385. doi:10.1016/j.cplett.2007.11.035
• Boyer JS (1969) Measurement of the water status of plants. Annu Rev Plant Physiol 9:351–363
• Cazzonelli CI (2011) Carotenoids in nature: insights from plants and beyond. Funct Plant Biol 38:833–847. doi:10.1071/FP11192
• Cazzonelli CI, Pogson BJ (2010) Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci 15:266–274.doi:10.1016/j.tplants.2010.02.003
• Cazzonelli CI, Cuttriss AJ, Cossetto SB, Pye W, Crisp P, Whelan J, Finnegan EJ, Turnbull C, Pogson BJ (2009) Regulation of carotenoid composition and shoot branching in Arabidopsis by a chromatin modifying histone methyltransferase, SDG8. Plant Cell 21:39–53. doi:10.1105/tpc.108.063131
• Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560. doi:10.1093/aob/mcn125
• Chen XY, Han HP, Jiang P, Nie LL, Bao HX, Fan PX, Lv S, Feng J, Li Y (2011) Transformation of b-lycopene cyclase genes from Salicornia europaea and Arabidopsis conferred salt tolerance in Arabidopsis and tobacco. Plant Cell Physiol 52:909–921. doi:10.1093/pcp/pcr043
• Cordero BF, Couso I, Leon R, Rodriguez H, Vargas MA (2012) Isolation and Characterization of a Lycopene e-Cyclase Gene of Chlorella (Chromochloris) zofingiensis. Regulation of the Carotenogenic Pathway by Nitrogen and Light. Mar Drugs 10:2069–2088. doi:10.3390/md10092069
• Cunningham FX, Pogson B, Sun Z, McDonald KA, DellaPenna D, Gantt E (1996) Functional analysis of the beta and epsilon lycopene cyclase enzymes of Arabidopsis reveals a mechanism for control of cyclic carotenoid formation. Plant Cell 8:1613–1626
• Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679. doi:10.1146/annurev-arplant-042809-112122
• Davison PA, Hunter CN, Horton P (2002) Overexpression of betacarotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418:203–206. doi:10.1038/nature00861
• Diretto G, Tavazza R, Welsch R, Pizzichini D, Mourgues F, Papacchioli V, Beyer P, Giuliano G et al (2006) Metabolic engineering of potato tuber carotenoids through tuber-specific silencing of lycopene-e-cyclase. BMC Plant Biol 6:13–24. doi:10.1186/1471-2229-6-13
• Ducreux LJM, Morris WL, Hedley PE, Shepherd T, Davies HV, Millam S, Taylor MA (2005) Metabolic engineering of high carotenoid potato tubers containing enhanced levels of betacarotene and lutein. J Exp Bot 56:81–89. doi:10.1093/jxb/eri016
• Giuliano G, Tavazza R, Diretto G, Beyer P, Taylor MA (2008) Metabolic engineering of carotenoid biosynthesis in plants. Trends Biotechnol 26:139–145. doi:10.1016/j.tibtech.2007.12.003
• Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5:151. doi:10.3389/fpls.2014.00151
• Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC et al (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194. doi:10.1038/nature07271
• Götz T, Sandmann G, Römer S (2002) Expression of abacterial carotene hydroxylase gene (crtZ) enhances UV tolerance in tobacco. Plant Mol Biol 50:127–140. doi:10.1023/A:1016072218801
• Guo X, Yang L, Hu H, Yang L (2009) Cloning and expression analysis of carotenogenic genes during ripening of Autumn Olive fruit (Elaeagnus umbellata). J Agric Food Chem 57:5334–5339. doi:10.1021/jf900547e
• Han H, Li Y, Zhou S (2008) Overexpression of phytoene synthase gene from Salicornia europaea alters response to reactive oxygen species under salt stress in transgenic Arabidopsis. Biotechnol Lett 30:1501–1507. doi:10.1007/s10529-008-9705-6
• Harjes CE, Rocheford TR, Bai L, Brutnell TP, Kandianis CB, Sowinski SG, Stapleton AE, Vallabhaneni R, Williams M, Wurtzel ET et al (2008) Natural genetic variation in lycopene-ecyclase tapped for maize biofortification. Science 319:330–333. doi:10.1126/science.1150255
• Horsch RB, Fry JE, Hoffmann NL, Eicholtz D, Rogers SG, Fraley RT (1985) A simple method for transferring genes into plants. Science 227:1229–1231
• Howitt CA, Pogson BJ (2006) Carotenoid accumulation and functions in seeds and non-green tissues. Plant, Cell Environ 29:435–445. doi:10.1111/j.1365-3040.2005.01492.x
• Kim SH, Kim YH, Ahn YO, Ahn MJ, Jeong JC, Lee HS, Kwak SS (2012a) Down-regulation of the lycopene-e-cyclase gene increases carotenoid synthesis via the b-branch-specific pathway and enhances salt-stress tolerance in sweetpotato transgenic calli. Physiol Plantarum 147:432–442. doi:10.1111/j.1399-3054.2012.01688.x
• Kim SH, Ahn YO, Ahn MJ, Lee HS, Kwak SS (2012b) Downregulation of β-carotene hydroxylase increases b-carotene and total carotenoids enhancing salt stress tolerance in transgenic cultured cells of sweet potato. Phytochemistry 74:69–78. doi:10.1016/j.phytochem.2011.11.003
• Krasensky J, Jonak C (2012) Drought, salt, and temperature stressinduced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608. doi:10.1093/jxb/err460
• Li F, Vallabhaneni R, Wurtzel ET (2008) PSY3, a new member of the phytoene synthase gene family conserved in the poaceae and regulator of abiotic stress-induced root carotenogenesis. Plant Physiol 146:1333–1345. doi:10.1104/pp.107.111120
• Lindgren L, Stahlberg KG, Hoglund AS (2003) Seed-specific overexpression of an endogenous Arabidopsis phytoene synthase gene results in delayed germination and increased levels of carotenoids, chlorophyll, and abscisic acid. Plant Physiol 132:779–785. doi:10.1104/pp.102.017053
• Liu HB, Li XH, Xiao JH, Wang SP (2012) A convenient method for simultaneous quantification of multiple phytohormones and metabolites: application in study of rice-bacterium interaction. Plant Methods 8:2. doi:10.1186/1746-4811-8-2
• Ma C, Ma BG, He J, Hao QN, Lu XY, Wang L (2011) Regulation of carotenoid content in tomato by silencing of Lycopene β/ε-Cyclase genes. Plant Mol Biol Rep 29:117–124. doi:10.1007/s11105-010-0211-3
• Matusova R, Rani K, Verstappen FW, Franssen MC, Beale MH, Bouwmeester HJ (2005) The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139:920–934. doi:10.1104/pp.105.061382
• Meier S, Tzfadia O, Vallabhaneni R, Gehring C, Wurtzel ET (2011) A transcriptional analysis of carotenoid, chlorophyll and plastidial isoprenoid biosynthesis genes during development and osmotic stress responses in Arabidopsis thaliana. BMC Syst Biol 5:77–96. doi:10.1186/1752-0509-5-77
• Min DH, Zhao Y, Huo DY, Li LC, Chen M, Xu ZS, Ma YZ (2013) Isolation and identification of a wheat gene encoding a zinc finger protein (TaZnFP) responsive to abiotic stresses. Acta Physiol Plant 35:1597–1604. doi:10.1007/s11738-012-1202-9
• Moreno JC, Pizarro L, Fuentes P, Handford M, Cifuentes V, Stange C (2013) Levels of lycopene-β-cyclase 1 modulate carotenoid gene expression and accumulation in daucus carota. PLoS ONE 8:e58144. doi:10.1371/journal.pone.0058144
• Muhammad R, Khurram S, Rashid A, Moddassir A, Imran H, Shahid M, Gerald AB, Nasir AS (2014) Cloning and characterization of Na +/H + antiporter (LfNHX1) gene from a halophyte grass Leptochloa fusca for drought and salt tolerance. Mol Biol Rep 41:1669–1682. doi:10.1007/s11033-013-3015-3
• Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185. doi:10.1146/ annurev.arplant.56.032604.144046
• Natwar S, Avinash M, Bhavanath J (2014) 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 16:321–332. doi:10.1007/s10126-013-9548-6
• Pogson BJ, Rissler HM (2000) Genetic manipulation of carotenoid biosynthesis and photoprotection. Philos Trans R Soc Lond B 355:1395–1403. doi:10.1098/rstb.2000.0701
• Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signaling. Trends Plant Sci 15:395–401. doi:10.1016/j.tplants.2010.04.006
• Rock CD (2000) Pathways to abscisic acid-regulated gene expression. New Phytol 148:357–396. doi:10.1046/j.1469-8137.2000.00769.x
• Ruiz-Sola MÁ , Arbona V, Gómez-Cadenas A, Rodríguez-Concepción M, Rodríguez-Villalón AA (2014) Root specific induction of carotenoid biosynthesis contributes to ABA production upon salt Stress in Arabidopsis. PLoS ONE 9:e90765. Doi:10.1371/journal.pone.0090765
• Shi YM, Wang R, Luo ZP, Jin LF, Liu PP, Chen QS, Li ZF, Li F, Wei CY, Wu MZ et al (2014) Molecular cloning and functional characterization of the lycopene ε-Cyclase gene via virusinduced gene silencing and its expression pattern in Nicotiana tabacum. Int J Mol Sci 15:14766–14785. doi:10.3390/ijms150814766
• Sun PP, Zhu XF, Huang XS, Liu JH (2014) Overexpression of a stress-responsive MYB transcription factor of Poncirus trifoliata confers enhanced dehydration tolerance and increases polyamine biosynthesis. Plant Physiol Biochem 78:71–79. doi:10.1016/j. plaphy.2014.02.022
• Tang LL, Cai H, Zhai H, Luo X, Wang ZY, Cui L, Bai X (2014) Overexpression of Glycine soja WRKY20 enhances both drought and salt tolerance in transgenic alfalfa (Medicago sativa L.). Plant Cell Tiss Organ Cult 118:77–86. doi:10.1007/s11240-014-0463-y
• Tao N, Hu Z, Liu Q, Xu J, Cheng Y, Guo L, Guo W, Deng X (2007) Expression of phytoene synthase gene (Psy) is enhanced during fruit ripening of Cara Cara navel orange (Citrus sinensis Osbeck). Plant Cell Rep 26:837–843. doi:10.1007/s00299-006-0289-0
• Taylor IB, Sonneveld T, Bugg TDH, Thompson AJ (2005) Regulation and manipulation of the biosynthesis of abscisic acid, including the supply of xanthophyll precursors. J Plant Growth Regul 24:253–273. doi:10.1007/s00344-005-0070-6
• Tester M, Langridg P (2010) Breeding technologies to increase crop production in a changing world. Science 327:818–822. doi:10.1126/science.1183700
• Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K et al (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200. doi:10.1038/nature07272
• Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28:663–692. doi:10.1039/c0np00036a
• 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. doi:10.1093/jxb/erq463
• Wu G, Wang G, Ji J, Gao H, Guan W, Wu J, Guan C, Wang Y (2014) Cloning of a cytosolic ascorbate peroxidase gene from Lycium chinense Mill. and enhanced salt tolerance by overexpressing in tobacco. Gene 543:85–92. doi:10.1016/j.gene.2014.03.061
• Xiong L, Zhu JK (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant, Cell Environ 25:131–139.doi:10.1046/j.1365-3040.2002.00782.x
• Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant cell 14:165–183. doi:10.1105/tpc. 000596
• Xu Q, He Q, Li S, Tian Z (2014) Molecular characterization of StNAC2 in potato and its overexpression confers drought and salt tolerance. Acta Physiol Plant 36:1841–1851. doi:10.1007/s11738-014-1558-0
• Yarra R, He SJ, Abbagani S, Ma B, Bulle M, Zhang WK (2012) 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 111:49–57. doi:10.1007/s11240-012-0169-y
• Yu B, Lydiate DJ, Young LW, Schafer UA, Hannoufa A (2008) Enhancing the carotenoid content of Brassica napus seeds by down-regulating lycopene-e-cyclase. Transgenic Res 17:573–585. doi:10.1007/s11248-007-9131-x
• Zhang X, Wang L, Meng H, Wen HT, Fan YL, Zhao J (2011) Maize ABP9 enhances tolerance to multiple stresses in transgenic Arabidopsis by modulating ABA signaling and cellular levels of reactive oxygen species. Plant Mol Biol 75:365–378. doi:10.1007/s11103-011-9732-x
• Zhang DY, Yang HL, Li XS, Li HY, Wang YC (2014) Overexpression of Tamarix albiflonum TaMnSOD increases drought tolerance in transgenic cotton. Mol Breeding 34:1–11. doi:10.1007/s11032-014-0015-5
• Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273. doi:10.1146/annurev.arplant. 53.091401.143329

Identyfikatory

DOI

10.1007/s11738-015-1958-9