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Overexpression of ALDH2B8, an aldehyde dehydrogenase gene from grapevine, sustains Arabidopsis growth upon salt stress and protects plants against oxidative stress

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Abstract

Aldehyde dehydrogenases (ALDHs) belong to a family of NAD (P)+-dependent enzymes that catalyze the oxidation of various toxic aldehydes to carboxylic acids. They have been reported to play important roles in plant responses to various stresses. Here we report on the isolation of a grapevine ALDH gene, which is rapidly induced in response to NaCl treatment. When transiently expressed in Arabidopsis protoplasts, grapevine ALDH2B8 was found to be localized in mitochondria. Transgenic Arabidopsis plants overexpressing grapevine ALDH2B8 showed sustained growth upon salt stress and increased tolerance against oxidative stress, which was correlated with decreased accumulation of reactive oxygen specie and malondialdehyde derived from cellular lipid peroxidation. In addition, the transgenic line had longer roots and higher chlorophyll content than the wild type under high salinity conditions. Taken together, we suggest that grapevine ALDH2B8 is involved in plant responses to oxidative and salt stress.

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Abbreviations

ABA:

Abscisic acid

ALDHs:

Aldehyde dehydrogenases

cDNA:

Complementary deoxyribonucleic acid

DAB:

Diaminobenzidine

FW:

Fresh weight

GFP:

Green fluorescence protein

H2O2 :

Hydrogen peroxide

MDA:

Malondialdehyde

MS:

Murashige and Skoog medium

NAD (P):

Nicotinamide adenine dinucleotide (phosphate)

NBT:

Nitro blue tetrazolium

O2 :

Superoxide anion

qRT-PCR:

Quantitative reverse transcriptase-polymerase chain reaction

ROS:

Reactive oxygen specie

SOD:

Superoxide dismutase

WT:

Wild type

T-NOS:

Nopaline synthase terminator

References

  • Barclay K, McKersie B (1994) Peroxidation reactions in plant membranes: effects of free fatty acids. Lipids 29:877–882

    Article  PubMed  CAS  Google Scholar 

  • Bartels D (2001) Targetingdetoxification pathways-an efficient approach to obtain plants with multiple stress tolerance? Trends Plant Sci 6:284–286

    Article  PubMed  CAS  Google Scholar 

  • Bartels D, Salamini F (2001) Desiccation tolerance in the resurrection plant Craterostigma plantagineum. A contribution to the study of drought tolerance at the molecular level. Plant Physiol 127:1346–1353

    Article  PubMed  CAS  Google Scholar 

  • Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58

    Article  CAS  Google Scholar 

  • Brocker C, Vasiliou M, Carpenter S, Carpenter C, Zhang Y, Wang X, Kotchoni S, Wood A, Kirch H-H, Kopečný D, Nebert D, Vasiliou V (2012) Aldehyde dehydrogenase (ALDH) superfamily in plants: gene nomenclature and comparative genomics. Planta. http://dx.doi.org/10.1007/s00425-012-1749-0

  • Chen THH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257

    Article  PubMed  CAS  Google Scholar 

  • Chung F-L, Chen H-JC, Nath RG (1996) Lipid peroxidation as a potential endogenous source for the formation of exocyclic DNA adducts. Carcinogenesis 17:2105–2111

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Cui X, Wise RP, Schnable PS (1996) The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science 272:1334–1336

    Article  PubMed  CAS  Google Scholar 

  • Esterbauer H, Schaur RJ, Zollner H (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radical Biol Med 11:81–128

    Article  CAS  Google Scholar 

  • Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319

    Article  PubMed  CAS  Google Scholar 

  • Gao C, Han B (2009) Evolutionary and expression study of the aldehyde dehydrogenase (ALDH) gene superfamily in rice (Oryza sativa). Gene 431:86–94

    Article  PubMed  CAS  Google Scholar 

  • Guerrero FD, Jones JT, Mullet JE (1990) Turgor-responsive gene transcription and RNA levels increase rapidly when pea shoots are wilted. Sequence and expression of three inducible genes. Plant Mol Biol 15:11–26

    Article  PubMed  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  PubMed  CAS  Google Scholar 

  • Huang W, Ma X, Wang Q, Gao Y, Xue Y, Niu X, Yu G, Liu Y (2008) Significant improvement of stress tolerance in tobacco plants by overexpressing a stress-responsive aldehyde dehydrogenase gene from maize (Zea mays). Plant Mol Biol 68:451–463

    Article  PubMed  CAS  Google Scholar 

  • Kim SH, Woo DH, Kim JM, Lee SY, Chung WS, Moon YH (2011) Arabidopsis MKK4 mediates osmotic-stress response via its regulation of MPK3 activity. Biochem Biophys Res Commun 412:150–154

    Article  PubMed  CAS  Google Scholar 

  • Kirch H-H, Nair A, Bartels D (2001) Novel ABA- and dehydration-inducible aldehyde dehydrogenase genes isolated from the resurrection plant Craterostigma plantagineum and Arabidopsis thaliana. Plant J 28:555–567

    Article  PubMed  CAS  Google Scholar 

  • Kirch H-H, Bartels D, Wei Y, Schnable PS, Wood AJ (2004) The ALDH gene superfamily of Arabidopsis. Trends Plant Sci 9:371–377

    Article  PubMed  CAS  Google Scholar 

  • Kirch H-H, Schlingensiepen S, Kotchoni S, Sunkar R, Bartels D (2005) Detailed expression analysis of selected genes of the aldehyde dehydrogenase (ALDH) gene superfamily in Arabidopsis thaliana. Plant Mol Biol 57:315–332

    Article  PubMed  CAS  Google Scholar 

  • Kotchoni SO, Kuhns C, Ditzer A, Kirch H-H, Bartels D (2006) Over-expression of different aldehyde dehydrogenase genes in Arabidopsis thaliana confers tolerance to abiotic stress and protects plants against lipid peroxidation and oxidative stress. Plant Cell Environ 29:1033–1048

    Article  PubMed  CAS  Google Scholar 

  • Laloi C, Apel K, Danon A (2004) Reactive oxygen signalling: the latest news. Curr Opin Plant Biol 7:323–328

    Article  PubMed  CAS  Google Scholar 

  • Li D, Song S, Xia X, Yin W (2012a) Two CBL genes from populus euphratica confer multiple stress tolerance in transgenic triploid white poplar. Plant Cell Tiss Organ Cult 109:477–489

    Article  CAS  Google Scholar 

  • Li R, Wang A, Sun S, Liang S, Wang X, Ye Q, Li H (2012b) Functional characterization of FT and MFT ortholog genes in orchid (Dendrobium nobile Lindl) that regulate the vegetative to reproductive transition in Arabidopsis. Plant Cell Tiss Organ Cult 111:143–151

    Article  CAS  Google Scholar 

  • Lindahl R (1992) Aldehyde dehydrogenases and their role in carcinogenesis. Crit Rev Biochem Mol Biol 27:283–335

    Article  PubMed  CAS  Google Scholar 

  • Lindahl R, Petersen DR (1991) Lipid aldehyde oxidation as a physiological role for class 3 aldehyde dehydrogenases. Biochem Pharmacol 41:1583–1587

    Article  PubMed  CAS  Google Scholar 

  • Long MC, Nagegowda DA, Kaminaga Y, Ho KK, Kish CM, Schnepp J, Sherman D, Weiner H, Rhodes D, Dudareva N (2009) Involvement of snapdragon benzaldehyde dehydrogenase in benzoic acid biosynthesis. Plant J 59:256–265

    Article  PubMed  CAS  Google Scholar 

  • Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol 127:1781–1787

    Article  PubMed  CAS  Google Scholar 

  • Missihoun TD, Schmitz J, Klug R, Kirch HH, Bartels D (2011) Betaine aldehyde dehydrogenase genes from Arabidopsis with different sub-cellular localization affect stress responses. Planta 233:369–382

    Article  PubMed  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  PubMed  CAS  Google Scholar 

  • Nair RB, Bastress KL, Ruegger MO, Denault JW, Chapple C (2004) The Arabidopsis thaliana reduced epidermal fluorescence1 gene encodes an aldehyde dehydrogenase involved in ferulic acid and sinapic acid biosynthesis. Plant Cell Online 16:544–554

    Article  CAS  Google Scholar 

  • Nakazono M, Tsuji H, Li Y, Saisho D, Arimura S-i, Tsutsumi N, Hirai A (2000) Expression of a gene encoding mitochondrial aldehyde dehydrogenase in rice increases under submerged conditions. Plant Physiol 124:587–598

    Article  PubMed  CAS  Google Scholar 

  • Ohsawa I, Nishimaki K, Yasuda C, Kamino K, Ohta S (2003) Deficiency in a mitochondrial aldehyde dehydrogenase increases vulnerability to oxidative stress in PC12 cells. J Neurochem 84:1110–1117

    Article  PubMed  CAS  Google Scholar 

  • Ozturk ZN, Talamé V, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N, Tuberosa R, Bohnert HJ (2002) Monitoring large-scale changes in transcript abundance in drought- and salt-stressed barley. Plant Mol Biol 48:551–573

    Article  CAS  Google Scholar 

  • Perozich J, Nicholas H, Wang B-C, Lindahl R, Hempel J (1999) Relationships within the aldehyde dehydrogenase extended family. Protein Sci 8:137–146

    Article  PubMed  CAS  Google Scholar 

  • Ramanjulu S, Bartels D (2002) Drought- and desiccation-induced modulation of gene expression in plants. Plant Cell Environ 25:141–151

    Article  PubMed  CAS  Google Scholar 

  • Rodrigues SM, Andrade MO, Gomes APS, DaMatta FM, Baracat-Pereira MC, Fontes EPB (2006) Arabidopsis and tobacco plants ectopically expressing the soybean antiquitin-like ALDH7 gene display enhanced tolerance to drought, salinity, and oxidative stress. J Exp Bot 57:1909–1918

    Article  PubMed  CAS  Google Scholar 

  • Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292

    Article  PubMed  CAS  Google Scholar 

  • Sheen J (2002) A transient expression assay using Arabidopsis mesophyll protoplasts. http://genetics.mgh.harvard.edu/sheenweb/

  • Shen Y, Zhang Y, Yang C, Lan Y, Liu L, Liu S, Chen Z, Ren G, Wan J (2012) Mutation of OsALDH7 causes a yellow-colored endosperm associated with accumulation of oryzamutaic acid A in rice. Planta 235:433–441

    Article  PubMed  CAS  Google Scholar 

  • Shin J-H, Kim S-R, An G (2009) Rice aldehyde dehydrogenase7 is needed for seed maturation and viability. Plant Physiol 149:905–915

    Article  PubMed  CAS  Google Scholar 

  • Stiti N, Missihoun TD, Kotchoni SO, Kirch HH, Bartels D (2011) Aldehyde dehydrogenases in Arabidopsis thaliana: biochemical requirements, metabolic pathways, and functional analysis. Front Plant Sci 2:65

    Article  PubMed  CAS  Google Scholar 

  • Stroeher VL, Boothe JG, Good AG (1995) Molecular cloning and expression of a turgor-responsive gene in Brassica napus. Plant Mol Biol 27:541–551

    Article  PubMed  CAS  Google Scholar 

  • Sunkar R, Bartels D, Kirch H-H (2003) Overexpression of a stress-inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance. Plant J 35:452–464

    Article  PubMed  CAS  Google Scholar 

  • Székely G, Ábrahám E, Cséplő Á, Rigó G, Zsigmond L, Csiszár J, Ayaydin F, Strizhov N, Jásik J, Schmelzer E, Koncz C, Szabados L (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J 53:11–28

    Article  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Google Scholar 

  • Vasiliou V, Bairoch A, Tipton KF, Nebert DW (1999) Eukaryotic aldehyde dehydrogenase (ALDH) genes: human polymorphisms, and recommended nomenclature based on divergent evolution and chromosomal mapping. Pharmacogenetics 9:421–434

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Wang Y, Hao W (2007) cDNA cloning and characterization of the novel genes related to aldehyde dehydrogenase from wild Chinese grape (Vitis pseudoreticulata W. T. Wang). Mitochondrial DNA 18:9–18

    Google Scholar 

  • Wei Y, Lin M, Oliver D, Schnable P (2009) The roles of aldehyde dehydrogenases (ALDHs) in the PDH bypass of Arabidopsis. BMC Biochem 10:7

    Article  PubMed  Google Scholar 

  • Wen Y, Wang X, Xiao S, Wang Y (2012) Ectopic expression of VpALDH2B4, a novel aldehyde dehydrogenase gene from Chinese wild grapevine (Vitis pseudoreticulata), enhances resistance to mildew pathogens and salt stress in Arabidopsis. Planta 236:525–539

    Article  PubMed  CAS  Google Scholar 

  • Wenzel P, Müller J, Zurmeyer S, Schuhmacher S, Schulz E, Oelze M, Pautz A, Kawamoto T, Wojnowski L, Kleinert H, Münzel T, Daiber A (2008) ALDH-2 deficiency increases cardiovascular oxidative stress—evidence for indirect antioxidative properties. Biochem Biophys Res Commun 367:137–143

    Article  PubMed  CAS  Google Scholar 

  • Yoshida A, Rzhetsky A, Hsu LC, Chang C (1998) Human aldehyde dehydrogenase gene family. Eur J Biochem 251:549–557

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Liu Y, Xu Y, Chapman S, Love A, Xia T (2012a) A newly isolated Na+/H+ antiporter gene, DmNHX1, confers salt tolerance when expressed transiently in Nicotiana benthamiana or stably in Arabidopsis thaliana. Plant Cell Tiss Organ Cult 110:189–200

    Article  CAS  Google Scholar 

  • Zhang Y, Mao L, Wang H, Brocker C, Yin X, Vasiliou V, Fei Z, Wang X (2012b) Genome-wide identification and analysis of grape aldehyde dehydrogenase (ALDH) gene superfamily. PLoS ONE 7:e32153

    Article  PubMed  CAS  Google Scholar 

  • Zhu Z, Shi J, Cao J, He M, Wang Y (2012) VpWRKY3, a biotic and abiotic stress-related transcription factor from the Chinese wild Vitis pseudoreticulata. Plant Cell Rep 31:2109–2120

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) Genevestigator. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Zhangjun Fei for critical revision of this manuscript. This work was supported by the National Natural Science Foundation of China (31071782), 948 Project from Ministry of Agriculture of China (2012-S12), and Chinese Universities Scientific Fund (QN2011056).

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Correspondence to Xiping Wang.

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Xu, X., Guo, R., Cheng, C. et al. Overexpression of ALDH2B8, an aldehyde dehydrogenase gene from grapevine, sustains Arabidopsis growth upon salt stress and protects plants against oxidative stress. Plant Cell Tiss Organ Cult 114, 187–196 (2013). https://doi.org/10.1007/s11240-013-0314-2

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