Abstract
Aldehyde dehydrogenases (ALDHs) catalyze the irreversible oxidation of a broad spectrum of reactive aldehydes to their corresponding carboxylic acids. Although the proteins have been studied from various organisms and at different growth stages in plants, their potential roles in pathogen infection have not been examined. Here we isolated and functionally characterized a pathogen-inducible ALDH gene (VpALDH2B4) from Chinese wild grapevine Vitis pseudoreticulata accession Baihe-35-1. When transiently expressed in Arabidopsis leaves, VpALDH2B4 was found to be localized in mitochondria. Escherichia coli expressed GST-VpALDH2B4 exhibited ALDH activity in vitro and was capable of utilizing malondialdehyde (MDA), acetaldehyde and glyceraldehydes as its substrate. Over-expression of VpALDH2B4 in Arabidopsis resulted in hypersensitive response-like cell death, enhanced resistance to downy mildew and powdery mildew presumably via the SA-signaling pathway. The same Arabidopsis transgenic plants also showed enhanced tolerance to salt stress, which is accompanied by less MDA accumulation and upregulation of the stress-responsive superoxide dismutase activity. Taken together, our results suggest that VpALDH2B4 and perhaps its orthologous genes may be involved in responses of plants to stresses imposed by both biotrophic pathogens and high salinity conditions.
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Abbreviations
- qRT-PCR:
-
Quantitative reverse transcriptase-polymerase chain reaction
- VpALDH2B4 :
-
Vitis pseudoreticulata ALDH2B4
- HR:
-
Hypersensitive response
- DR:
-
Disease reaction
- SA:
-
Salicylic acid
- MDA:
-
Malondialdehyde
- SOD:
-
Superoxide dismutase
- Hpi:
-
Hours post inoculation
- Dpi:
-
Days post inoculation
References
Black W, Vasiliou V (2009) The aldehyde dehydrogenase gene superfamily resource center. Hum Genomics 4:136–142
Bolwell GP (1999) Role of active oxygen species and NO in plant defence responses. Curr Opin Plant Biol 2:287–294
Bouche N, Fait A, Bouchez D, Moller SG, Fromm H (2003) Mitochondrial succinic-semialdehyde dehydrogenase of the gamma-aminobutyrate shunt is required to restrict levels of reactive oxygen intermediates in plants. Proc Natl Acad Sci USA 100:6843–6848
Brocker C, Lassen N, Estey T, Pappa A, Cantore M, Orlova VV, Chavakis T, Kavanagh KL, Oppermann U, Vasiliou V (2010) Aldehyde dehydrogenase 7A1 (ALDH7A1) is a novel enzyme involved in cellular defense against hyperosmotic stress. J Biol Chem 285:18452–18463
Chen TH, 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
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Cui X, Wise RP, Schnable PS (1996) The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science 272:1334–1336
Durrant WE, Dong X (2004) Systemic acquired resistance. Ann Rev Phytopathol 42:185–209
Grant MR, Jones JD (2009) Hormone (dis)harmony moulds plant health and disease. Science 324:750–752
Greenberg JT (1997) Programmed cell death in plant–pathogen interactions. Ann Rev Plant Physiol Plant Mol Biol 48:525–545
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
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
Kirch HH, Bartels D, Wei Y, Schnable PS, Wood AJ (2004) The ALDH gene superfamily of Arabidopsis. Trends Plant Sci 9:371–377
Kirch HH, 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
Kotchoni SO, Kuhns C, Ditzer A, Kirch HH, 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
Laloi C, Apel K, Danon A (2004) Reactive oxygen signalling: the latest news. Curr Opin Plant Biol 7:323–328
Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Ann Rev Plant Physiol Plant Mol Biol 48:251–275
Liu F, Schnable PS (2002) Functional specialization of maize mitochondrial aldehyde dehydrogenases. Plant Physiol 130:1657–1674
Liu F, Cui X, Horner HT, Weiner H, Schnable PS (2001) Mitochondrial aldehyde dehydrogenase activity is required for male fertility in maize. Plant Cell 13:1063–1078
Ma HS, Liang D, Shuai P, Xia XL, Yin WL (2010) The salt- and drought-inducible poplar GRAS protein SCL7 confers salt and drought tolerance in Arabidopsis thaliana. J Exp Bot 61:4011–4019
Marchitti SA, Brocker C, Stagos D, Vasiliou V (2008) Non-P450 aldehyde oxidizing enzymes: the aldehyde dehydrogenase superfamily. Expert Opin Drug Metab Toxicol 4:697–720
McCord JM, Fridovich I (1969) Superoxide dismutase: an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055
McDowell JM, Cuzick A, Can C, Beynon J, Dangl JL, Holub EB (2000) Downy mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1, EDS1, NPR1 and salicylic acid accumulation. Plant J 22:523–529
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498
Nakazono M, Tsuji H, Li Y, Saisho D, Arimura S, Tsutsumi N, Hirai A (2000) Expression of a gene encoding mitochondrial aldehyde dehydrogenase in rice increases under submerged conditions. Plant Physiol 124:587–598
Niyogi KK, Bjorkman O, Grossman AR (1997) The roles of specific xanthophylls in photoprotection. Proc Natl Acad Sci USA 94:14162–14167
op den Camp RG, Kuhlemeier C (1997) Aldehyde dehydrogenase in tobacco pollen. Plant Mol Biol 35:355–365
Oztur ZN, Talame 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
Perozich J, Nicholas H, Lindahl R, Hempel J (1999) The big book of aldehyde dehydrogenase sequences. An overview of the extended family. Adv Exp Med Biol 463:1–7
Rodrigues SM, Andrade MO, Gomes AP, Damatta FM, Baracat-Pereira MC, Fontes EP (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
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
Shin JH, Kim SR, An G (2009) Rice aldehyde dehydrogenase 7 is needed for seed maturation and viability. Plant Physiol 149:905–915
Sophos NA, Vasiliou V (2003) Aldehyde dehydrogenase gene superfamily: the 2002 update. Chem Biol Interact 143–144:5–22
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
Sunkar R, Bartels D, Kirch HH (2003) Overexpression of a stress-inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance. Plant J 35:452–464
Szekely G, Abraham E, Cseplo A, Rigo G, Zsigmond L, Csiszar J, Ayaydin F, Strizhov N, Jasik 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
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Torres MA, Jones JD, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–378
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
Vasiliou V, Pappa A, Estey T (2004) Role of human aldehyde dehydrogenases in endobiotic and xenobiotic metabolism. Drug Metab Rev 36:279–299
Wang YJ, He PC (1997) Study on inheritance of leaves’ resistance to powdery mildew in Chinese native wild Vitis species. Agric Sci China 30:19–25
Wang YJ, Liu Y, He P, Chen J, Lamicanra O, Lu J (1995) Evaluation of foliar resistance to Uncinula necator in Chinese wild Vitis species. Vitis 34:159–164
Wang W, Devoto A, Turner JG, Xiao S (2007a) Expression of the membrane-associated resistance protein RPW8 enhances basal defense against biotrophic pathogens. Mol Plant Microbe Interact 20:966–976
Wang X, Wang Y, Hao W (2007b) cDNA cloning and characterization of the novel genes related to aldehyde dehydrogenase from wild Chinese grape (Vitis pseudoreticulata W. T. Wang). DNA Seq 18:9–18
Xiao S, Brown S, Patrick E, Brearley C, Turner JG (2003) Enhanced transcription of the Arabidopsis disease resistance genes RPW8.1 and RPW8.2 via a salicylic acid-dependent amplification circuit is required for hypersensitive cell death. Plant Cell 15:33–45
Xiao S, Calis O, Patrick E, Zhang G, Charoenwattana P, Muskett P, Parker JE, Turner JG (2005) The atypical resistance gene, RPW8, recruits components of basal defence for powdery mildew resistance in Arabidopsis. Plant J 42:95–110
Yang X, Wang W, Coleman M, Orgil U, Feng J, Ma X, Ferl R, Turner JG, Xiao S (2009) Arabidopsis 14-3-3 lambda is a positive regulator of RPW8-mediated disease resistance. Plant J 60:539–550
Yoshida A, Rzhetsky A, Hsu LC, Chang C (1998) Human aldehyde dehydrogenase gene family. Eur J Biochem 251:549–557
Zhang JJ, Wang YJ, Wang XP (2003) An improved method for rapidly extracting total RNA from Vitis. J Fruit Sci 20:178–181 in Chinese with English abstract
Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632
Acknowledgments
We are grateful to Dr. Wenming Wang (Sichuan Agricultural University), Robert Berkey (University of Maryland, USA) and Dr. Zhiyong Pan (Huazhong Agricultural University) for critical review of this manuscript. A fellowship from China Scholarship Council to Y.W. for his visiting research in the lab of S.X. (which is also partially supported by an NSF-IOS Grant #0842877) is gratefully acknowledged. This work was supported by the National Natural Science Foundation of China (Grant No. 30771493, 30571280).
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Wen, Y., Wang, X., Xiao, S. et al. 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 (2012). https://doi.org/10.1007/s00425-012-1624-z
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DOI: https://doi.org/10.1007/s00425-012-1624-z