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Expression of eggplant ascorbate peroxidase increases the tolerance of transgenic rice plants to flooding stress

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Abstract

Rice is sensitive to flooding during seed germination and early seedling growth. The objective of this study was to transfer ascorbate peroxidase (APX) cDNA from the eggplant (Solanum melongena, Sm) under the control of an ubiquitin promoter into rice (Oryza sativa) via Agrobacterium-mediated transformation. A real-time polymerase chain reaction analysis demonstrated that SmAPX gene was over-expressed in transgenic rice lines (SmAPXs). APX gene expression profiles were well matched with the data for APX enzyme activities and total chlorophyll contents in the non-transgenic (NT) and transgenic plants. The activity of APX in the transgenic line SmAPX6 was 9-fold higher than in NT plants under waterlog, and the amount of APX in the SmAPX6 line also accumulated greatly according to a Western blot analysis. The over-expression of SmAPX in rice seedlings exhibited stronger resistance to flood tolerance, less oxidative injury, and grew faster than NT plants exposed to flood treatment.

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References

  • Angaji SA, Septiningsih EM, Mackill DJ, Ismail AM (2010) QTLs associated with tolerance of flooding during germination in rice (Oryza sativa L.). Euphytica 172:159–168

    Article  Google Scholar 

  • Bailey-Serres J, Fukao T, Ronald P, Ismail A, Heuer S, Mackill D (2010) Submergence tolerant rice: SUB1’s Journey from landrace to modern cultivar. Rice 3:138–147

    Article  Google Scholar 

  • Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chaves MM, Maroc JP, Pereira LS (2003) Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol 30:239–264

    Article  CAS  Google Scholar 

  • Chiang CM, Chen SP, Chen LFO, Chiang MC, Chien HL, Lin KH (2013) Expression of the broccoli catalase gene (BoCAT) enhances heat tolerance in transgenic Arabidopsis. J Plant Biochem Biotechnol. doi:10.1007/s13562-013-0210

    Google Scholar 

  • Choe YH, Kim YS, Kim YH, Park HM, Yoon HS (2013) Homologous expression of r-glutamylcysteine synthetase increases grain yield and tolerance of transgenic rice plants to environmental stresses. J Plant Physiol 170:610–618

    Article  CAS  PubMed  Google Scholar 

  • Counce PA, Keisling TC, Mitchell AJ (2000) A uniform, objective, and adaptive system for expressing rice development. Crop Sci 40:436–443

    Article  Google Scholar 

  • Diaz-Vivancos P, Faize M, Barba-Espin G, Faize L, Petri C, Hernández JA, Burgos L (2013a) Ectopic expression of cytosolic superoxide dismutase and ascorbate peroxidase leads to salt stress tolerance in transgenic plums. Plant Biotechnol J 11(8):976–985

    Article  CAS  PubMed  Google Scholar 

  • Diaz-Vivancos P, Faize M, Petri C, Burgos L, Hernández JA (2013b) Environmental stress tolerance mediated by over-expression of antioxidant defences. ISB news report. August 2013

  • Djanaguiraman M, Prasad PV, Seppanen M (2010) Selenium protects sorghum leaves from oxidative damage under high temperature stress by enhancing antioxidant defense system. Plant Physiol Biochem 48(12):999–1007

    Article  CAS  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Ella ES, Dionisio-Sese ML, Ismail AM (2010) Proper management improves seedling survival and growth during early flooding in contrasting rice genotypes. Crop Sci 50:1997–2008

    Article  Google Scholar 

  • Fukao T, Bailey-Serres J (2008) Ethylene—a key regulator of submergence responses in rice. Plant Sci 175:43–51

    Article  CAS  Google Scholar 

  • Fukao T, Xu K, Ronald PC, Bailey-Serres J (2006) A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18:2021–2034

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gapper C, Dolan L (2006) Control of plant development by reactive oxygen species. Plant Physiol 141:341–345

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hattori Y, Nagai K, Furukawa S, Song XJ, Kawano R, Sakakibara H, Wu J, Matsumoto T, Yoshimura A, Kitano H, Matsuoka M, Mori H, Ashikari M (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460:1026–1030

    Article  CAS  PubMed  Google Scholar 

  • Hossain Z, López-Climent M, Arbona V, Pérez-Clemente R, Gómez-Cadenas A (2009) Modulation of the antioxidant system in citrus under waterlogging and subsequent drainage. J Plant Physiol 166:1391–1404

    Article  CAS  PubMed  Google Scholar 

  • Hsing YI, Chern CG, Fan MJ, Lu PC, Chen KT, Lo SF, Sun PK, Ho SL, Lee KW, Wang YC, Huang WL, Ko SS, Chen S, Chen JL, Chung CI, Lin YC, Hour AL, Wang YW, Chang YC, Tsai MW, Lin YS, Chen YC, Yen HM, Li CP, Wey CK, Tseng CS, Lai MH, Huang SC, Chen LJ, Yu SM (2007) A rice gene activation/knockout mutant resource for high throughput functional genomics. Plant Mol Biol 63:351–364

    Article  CAS  PubMed  Google Scholar 

  • Iseri OD, Korpe DA, Yurtcu E, Sahin FI, Haberal M (2011) Copper-induced oxidative damage, antioxidant response and genotoxicity in Lycopersicum esculentum Mill. and Cucumis sativus L. Plant Cell Rep 30:1713–1721

    Article  CAS  PubMed  Google Scholar 

  • Ismail AM, Ella ES, Vergara GV, Mackill DJ (2009) Mechanisms associated with tolerance to flooding during germination and early seedling growth in rice (Oryza sativa L). Ann Bot 103:197–209

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ismail AM, Johnson DE, Ella ES, Vergara GV, Baltazar AM (2012) Adaptation to flooding during emergence and seedling growth in rice and weeds, and implications for crop establishment. AoB Plants: pls019. doi:10.1093/aobpla/pls019

  • Jyothishwaran G, Kotresha D, Selvaraj T, Srideshikan S, Rajvanshi P, Jayabaskaran C (2007) A modified freeze and thaw method for efficient transformation of Agrobacterium tumefaciens. Curr Sci 93:770–772

    CAS  Google Scholar 

  • Keisuke N, Yoko H, Motoyuki A (2010) Stunt or elongate? Two opposite strategies by which rice adapts to floods. J Plant Res 123:303–309

    Article  Google Scholar 

  • Lee SH, Ahsan N, Lee KW, Kim DH, Lee DG, Kwak SS, Kwon SY, Kim TH, Lee BH (2007) Simultaneous overexpression of both CuZn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. J Plant Physiol 164:1626–1638

    Article  CAS  PubMed  Google Scholar 

  • Lee KW, Chen PW, Lu CA, Chen S, Ho TH, Yu SM (2009) Coordinated responses to oxygen and sugar deficiency allow rice seedlings to tolerate flooding. Sci Signal 2:ra61

    PubMed  Google Scholar 

  • Lin KH, Weng CC, Lo HF, Chen JT (2004) Study of the root antioxidative system of tomatoes and eggplants under waterlogged conditions. Plant Sci 167:355–365

    Article  CAS  Google Scholar 

  • Lin KH, Lo HF, Lin CH, Chan MT (2007) Cloning and expression analysis of ascorbate peroxidase gene from eggplant under flooding stress. Bot Stud 48:25–34

    CAS  Google Scholar 

  • Lin KH, Huang HC, Lin CY (2010) Cloning, expression and physiological analysis of broccoli catalase gene and Chinese cabbage ascorbate peroxidase gene under heat stress. Plant Cell Rep 29:575–593

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Murgia I, Tarantino D, Carravieri S, Soave C (2004) Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to paraquat-induced photooxidative stress and to nitric oxide-induced cell death. Plant J 38:945–953

    Article  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–869

    CAS  Google Scholar 

  • Passaia G, Spagnolo Fonini L, Caverzan A, Jardim-Messeder D, Christoff AP, Gaeta ML, de Araujo Mariath JE, Margis R, Margis-Pinheiro M (2013) The mitochondrial glutathione peroxidase GPX3 is essential for H2O2 homeostasis and root and shoot development in rice. Plant Sci 208:93–101

    Article  CAS  PubMed  Google Scholar 

  • Porra RJ, Thompson WA, Kriedelman PE (1989) Determination of accurate extraction and simultaneously equation for assaying chlorophyll a and b extracted with different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochem Biophys Acta 975:384–394

    CAS  Google Scholar 

  • Schwarz D, Rouphael Y, Colla G, Venema JH (2010) Grafting as a tool to improve tolerance of vegetables to abiotic stresses: thermal stress, water stress and organic pollutants. Sci Hortic 127:162–171

    Article  CAS  Google Scholar 

  • Sheu JJ, Yu TS, Tong WF, Yu SM (1996) Carbohydrate starvation stimulates differential expression of rice alpha-amylase genes that is modulated through complicated transcriptional and posttranscriptional processes. J Biol Chem 271:26998–27004

    Article  CAS  PubMed  Google Scholar 

  • Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Yabuta Y, Youshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319

    Article  CAS  PubMed  Google Scholar 

  • Shiono K, Takahashi H, Colmer TD, Nakazono M (2008) Role of ethylene in acclimations to promote oxygen transport in roots of plants in waterlogged soils. Plant Sci 175:52–58

    Article  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL X windows interface: flexible stragies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 5:4876–4882

    Article  Google Scholar 

  • Toki S (1997) Rapid and efficient Agrobacterium-mediated transformation in rice. Plant Mol Biol Report 15:16–21

    Article  CAS  Google Scholar 

  • Wang W, Vignani R, Scali M, Cresti M (2006) An universal and rapid protocol for protein extraction from recalcitrant plant tissues for proteomic analysis. Electrophoresis 27:2782–2786

    Article  CAS  PubMed  Google Scholar 

  • Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu C, Van Inzé D, Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO 16:4806–4816

    Article  CAS  Google Scholar 

  • Xi DM, Liu WS, Yang GD, Wu CA, Zheng CC (2010) Seed-specific overexpression of antioxidant genes in Arabidopsis enhances oxidative stress tolerance during germination and early seedling growth. Plant Biotechnol J 8:796–806

    Article  CAS  PubMed  Google Scholar 

  • Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriquez R, Huer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442:705–708

    Article  CAS  PubMed  Google Scholar 

  • Yildiztugay E, Sekmen AH, Turkan I, Kucukoduk M (2011) Elucidation of physiological and biochemical mechanisms of an endemic halophyte Centaurea tuzgoluensis under salt stress. Plant Physiol Biochem 49:816–824

    Article  CAS  PubMed  Google Scholar 

  • Zhao FY, Liu W, Zhang SY (2009) Different responses of plant growth and antioxidant system to the combination of cadmium and heat stress in transgenic and non-transgenic rice. J Integr Plant Biol 51:942–950

    Article  CAS  PubMed  Google Scholar 

  • Zheng J, Zhao JF, Tao YZ, Wang JH, Liu YJ, Fu JJ, Jin Y, Gao P, Zhang JP, Bai YF, Wang GY (2004) Isolation and analysis of water stress induced genes in maize seedlings by subtractive PCR and cDNA microarray. Plant Mol Biol 55:807–823

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Kuan Hung Lin.

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Chiang, C.M., Chen, L.F.O., Shih, S.W. et al. Expression of eggplant ascorbate peroxidase increases the tolerance of transgenic rice plants to flooding stress. J. Plant Biochem. Biotechnol. 24, 257–267 (2015). https://doi.org/10.1007/s13562-014-0265-7

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