Abstract
Aldehyde dehydrogenases (ALDHs) play a central role in detoxification processes of aldehydes generated in plants when exposed to the stressed conditions. In order to identify genes required for the stresses responses in the grass crop Zea mays, an ALDH (ZmALDH22A1) gene was isolated and characterized. ZmALDH22A1 belongs to the family ALDH22 that is currently known only in plants. The ZmALDH22A1 encodes a protein of 593 amino acids that shares high identity with the orthologs from Saccharum officinarum (95%), Oryza sativa (89%), Triticum aestivum (87%) and Arabidopsis thaliana (77%), respectively. Real-time PCR analysis indicates that ZmALDH22A1 is expressed differentially in different tissues. Various elevated levels of ZmALDH22A1 expression have been detected when the seedling roots exposed to abiotic stresses including dehydration, high salinity and abscisic acid (ABA). Tomato stable transformation of construct expressing the ZmALDH22A1 signal peptide fused with yellow fluorescent protein (YFP) driven by the CaMV35S-promoter reveals that the fusion protein is targeted to plastid. Transgenic tobacco plants overexpressing ZmALDH22A1 shows elevated stresses tolerance. Stresses tolerance in transgenic plants is accompanied by a reduction of malondialdehyde (MDA) derived from cellular lipid peroxidation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bouché N, Fait A, Bouchez D, Møller 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 100:6843–6849. doi:10.1073/pnas.1037532100
Busch KB, Fromm H (1999) Plant succinic semialdehyde dehydrogenase. Cloning, purification, localization in mitochondria, and regulation by adenine nucleotides. Plant Physiol 121:589–597. doi:10.1104/pp.121.2.589
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. doi:10.1016/S1369-5266(02)00255-8
Chen X, Zeng Q, Wood AJ (2002) The stress-responsive Tortula ruralis gene ALDH21A1 describes a novel eukaryotic aldehyde dehydrogenase protein family. J Plant Physiol 159:677–684. doi:10.1078/0176-1617-0813
Choi H, Hong J, Ha J, Kang J, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730. doi:10.1074/jbc.275.3.1723
Cui X, Wise RP, Schnable PS (1996) The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science 272:1334–1336. doi:10.1126/science.272.5266.1334
Deuschle K, Funck D, Hellmann H, Däschner K, Binder S, Frommer WB (2001) A nuclear gene encoding mitochondrial delta-pyrroline-5-carboxylate dehydrogenase and its potential role in protection from proline toxicity. Plant J 27:345–356. doi:10.1046/j.1365-313X.2001.01101.x
Fillatti J, Kiser J, Rose R, Comai L (1987) Efficient transfer of glyphosate tolerance gene into tomato using a binary Agrobacterium-tumefaciens vector. Biotechnology 5:726–730. doi:10.1038/nbt0787-726
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. doi:10.1007/BF00017720
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. doi:10.1016/0003-9861(68)90654-1
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300. doi:10.1093/nar/27.1.297
Ishitani M, Nakamura T, Han SY, Takabe T (1995) Expression of the betaine aldehyde dehydrogenase gene in barley in response to osmotic stress and abscisic acid. Plant Mol Biol 27:307–315. doi:10.1007/BF00020185
Janero DR (1990) Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radic Biol Med 9:515–540. doi:10.1016/0891-5849(90)90131-2
Kaplan B, Davydov O, Knight H, Galon Y, Knight MR, Fluhr R et al (2006) Rapid transcriptome changes induced by cytosolic Ca2+ transients reveal ABRE-related sequences as Ca2+-responsive cis elements in Arabidopsis. Plant Cell 18:2733–2748. doi:10.1105/tpc.106.042713
Kirch HH, 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. doi:10.1046/j.1365-313X.2001.01176.x
Kirch HH, Bartels D, Wei Y, Schnable PS, Wood AJ (2004) The ALDH gene superfamily of Arabidopsis. Trends Plant Sci 9:371–377. doi:10.1016/j.tplants.2004.06.004
Kirch HH, Schlingensiepen S, Kotchoni OS, 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. doi:10.1007/s11103-004-7796-6
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. doi:10.1111/j.1365-3040.2005.01458.x
Li Y, Nakazono M, Tsutsumi N, Hirai A (2000) Molecular and cellular characterizations of a cDNA clone encoding a novel isozyme of aldehyde dehydrogenase from rice. Gene 249:67–74. doi:10.1016/S0378-1119(00)00152-9
Liang Z, Ma D, Tang L, Hong Y, Luo A, Dai X (1997) Expression of the spinach aldehyde dehydrogenase (BADH) gene in transgenic tobacco plants. Chin J Biotechnol 13:236–240
Liu F, Schnable PS (2002) Functional specialization of maize mitochondrial aldehyde dehydrogenases. Plant Physiol 130:1657–1674. doi:10.1104/pp. 012336
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
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. doi:10.1104/pp. 127.4.1781
Mano J, Torii Y, Hayashi S, Takimoto K, Matsui K, Nakamura K et al (2002) The NADPH: quinone oxidoreductase P1-zeta-crystallin in Arabidopsis catalyzes the alpha, beta-hydrogenation of 2-alkenals: detoxication of the lipid peroxide-derived reactive aldehydes. Plant Cell Physiol 43:1445–1455. doi:10.1093/pcp/pcf187
Mao J, Zhang YC, Sang Y, Li QH, Yang HQ (2005) A role for Arabidopsis cryptochromes and COP1 in the regulation of stomatal opening. Proc Natl Acad Sci USA 102:12270–12275
Marcotte WR Jr, Russell SH, Quatrano RS (1989) Abscisic acid-responsive sequences from the Em gene of wheat. Plant Cell 1:969–976
McCue KF, Hanson AD (1992) Salt-inducible betaine aldehyde dehydrogenase from sugar beet: cDNA cloning and expression. Plant Mol Biol 18:1–11. doi:10.1007/BF00018451
Moore K, Roberts LJ (1998) Measurement of lipid peroxidation. Free Radic Res 28:659–671. doi:10.3109/10715769809065821
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 16:544–554. doi:10.1105/tpc.017509
Nakamura T, Yokota S, Muramoto Y, Tsutsui K, Oguri Y, Fukui K et al (1997) Expression of a betaine aldehyde dehydrogenase gene in rice, a glycinebetaine nonaccumulator, and possible localization of its protein in peroxisomes. Plant J 11:1115–1120. doi:10.1046/j.1365-313X.1997.11051115.x
Nakazono M, Tsuji H, Li Y, Saisho D, Arimura S, Tsutsumi N et al (2000) Expression of a gene encoding mitochondrial aldehyde dehydrogenase in rice increases under submerged conditions. Plant Physiol 124:587–598. doi:10.1104/pp.124.2.587
Oberschall A, Deák M, Török K, Sass L, Vass I, Kovács I et al (2000) A novel aldose/aldehyde reductase protects transgenic plants against lipid peroxidation under chemical and drought stresses. Plant J 24:437–446. doi:10.1046/j.1365-313x.2000.00885.x
Ozturk ZN, Talamé V, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N et al (2002) Monitoring large-scale changes in transcript abundance in drought- and salt-stressed barley. Plant Mol Biol 48:551–573. doi:10.1023/A:1014875215580
Perozich J, Nicholas H, Wang BC, Lindahl R, Hempel J (1999) Relationships within the aldehyde dehydrogenase extended family. Protein Sci 8:137–146
Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (RESTa) for group-wise comparison and statistical analysis if relative expression results in real-time PCR. Nucleic Acids Res 30:e36. doi:10.1093/nar/30.9.e36
Rumpho ME, Edwards GE, Loescher WH (1983) A pathway for photosynthetic carbon flow to mannitol in celery leaves: activity and localization of key enzymes. Plant Physiol 73:869–873
Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y et al (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. doi:10.1046/j.1365-313X.2002.01359.x
Simpson SD, Nakashima K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J 33:259–270. doi:10.1046/j.1365-313X.2003.01624.x
Skibbe DS, Liu F, Wen TJ, Yandeau MD, Xiangqin C, Cao J et al (2002) Characterization of the aldehyde dehydrogenase gene families of Zea mays and Arabidopsis. Plant Mol Biol 48:751–764. doi:10.1023/A:1014870429630
Sophos NA, Pappa A, Ziegler TL, Vasiliou V (2001) Aldehyde dehydrogenase gene superfamily: the 2000 update. Chem Biol Interact 130–132:323–337. doi:10.1016/S0009-2797(00)00275-1
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. doi:10.1007/BF00019320
Sunkar R, Bartels D, Kirch HH (2003) Overexpression of a stree-inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance. Plant J 35:452–464. doi:10.1046/j.1365-313X.2003.01819.x
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. doi:10.1097/00008571-199910000-00004
Wang SH, Liu JK, Feng YY, Niu XL, Giovannoni J, Liu Y (2008) Altered plastid levels and potential for improved fruit nutrient content via down-regulation of the tomato DDB1 interacting protein CUL4. Plant J 55:89–103
Weigel P, Weretilnyk EA, Hanson AD (1986) Betaine aldehyde oxidation by spinach chloroplasts. Plant Physiol 82:753–759
Weretilnyk EA, Hanson AD (1990) Molecular cloning of a plant betaine-aldehyde dehydrogenase, an enzyme implicated in adaptation to salinity and drought. Proc Natl Acad Sci USA 87:2745–2749. doi:10.1073/pnas.87.7.2745
Wood AJ, Saneoka H, Rhodes D, Joly RJ, Goldsbrough PB (1996) Betaine aldehyde dehydrogenase in sorghum. Plant Physiol 110:1301–1308. doi:10.1104/pp. 110.4.1301
Yoshida A, Rzhetsky A, Hsu LC, Chang C (1998) Human aldehyde dehydrogenase gene family. Eur J Biochem 251:549–557. doi:10.1046/j.1432-1327.1998.2510549.x
Acknowledgements
We thank Dr. Hongquan Yang from Shanghai Jiaotong University for kindly providing us with pHB vector. This work was supported by the Natural Science Foundation of China (Grant nos. 30770466 & 90717110), biotechnology application projects (Grant nos. 2006Z-05-0039 and 07KJT-11) from the local government of Sichuan Province, and 985 youth talent program (Grant No. 0082204127106) from Sichuan University.
Author information
Authors and Affiliations
Corresponding author
Additional information
The authors Weizao Huang, Xinrong Ma, and Qilin Wang contributed equally to this work.
Rights and permissions
About this article
Cite this article
Huang, W., Ma, X., Wang, Q. et al. 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 (2008). https://doi.org/10.1007/s11103-008-9382-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-008-9382-9