DOI QR코드

DOI QR Code

Isolation and characterization of Bradh1 gene encoding alcohol dehydrogenase from Chinese cabbage (Brassica rapa)

  • Abdula, Sailila E. (Department of Crop Science, Chungbuk National University) ;
  • Lee, Hye-Jung (Department of Crop Science, Chungbuk National University) ;
  • Melgar, Reneeliza J. (Department of Crop Science, Chungbuk National University) ;
  • Sun, Mingmao (Department of Crop Science, Chungbuk National University) ;
  • Kang, Kwon-Kyoo (Department of Horticulture, Hankyong National University) ;
  • Cho, Yong-Gu (Department of Crop Science, Chungbuk National University)
  • Received : 2011.03.15
  • Accepted : 2011.03.20
  • Published : 2011.03.31

Abstract

Alcohol dehydrogenase (E.C.1.1.1.1) is an enzyme present in higher plants involved in the anaerobic fermentation pathway that catalyzes the reduction of pyruvate to ethanol, resulting in continuous $NAD^+$ regeneration. It also plays an important role in many plant developments including tolerance to anoxia condition. Here, a cDNA clone encoding alcohol dehydrogenase (ADH) was isolated from Chinese cabbage (Brassica rapa) seedlings. The gene named Bradh1 had a total length of 1,326 bp that contains a single open reading frame of 1,140 bp. The predicted protein consists of 379 amino acid residues with a calculated molecular mass of 41.17 kDa. Expression pattern analysis revealed a tissue-specific expressing gene in different tissues and strongly expressed in the shoot, roots and seeds of Chinese cabbage. Agrobacterium transformation of full-length cDNA Bradh1 into rice Gopumbyeo showed high efficiency. Furthermore, induction of ADH in transgenic rice enhanced tolerance to anaerobiosis stresses and elevated mRNA transcripts. The overexpression of Bradh1 in rice increases germination under anaerobiosis stresses, implying the possibility of developing new varieties suited for direct seeding or flood-prone rice field.

Keywords

References

  1. Alpi A, Beevers H (1983) Effects of $O_2$ concentration on rice seedlings. Plant Physiol 7:30-34
  2. Armstrong W, Brandle R, Jackson MB (1994) Mechanisms of flood tolerance in plants. Acta Bot Neeri 43:307-358. https://doi.org/10.1111/j.1438-8677.1994.tb00756.x
  3. Aspart L, Got A, Delseny M, Mocquot B, Pradet A (1983) Adaptation of ribonucleic acid metabolism to anoxia in rice embryos. Plant Physiol 7:115-121
  4. Atwell BJ, Waters I, Greenway H (1982) The effect of oxygen and turbulence on elongation of coleoptiles of submergencetolerant and intolerant cultivars. J Exp Bot 33:1030-1044 https://doi.org/10.1093/jxb/33.5.1030
  5. Battraw MJ, Hall TC (1992) Expression of a chimeric neomycin phosphotransferase II gene in first and second generation transgenic rice plants. Plant Sci 86:191-202 https://doi.org/10.1016/0168-9452(92)90165-I
  6. Chan MT, Chang HH, Ho SL, Tong WF, Yu SM (1993) Agrobacterium-mediated production of transgenic rice plants expressing a chimeric $\alpha$-amylase promoter/$\beta$-glucuronidase gene. Plant Mol Biol 22:491-506 https://doi.org/10.1007/BF00015978
  7. Chang C, Meyerowitz EM (1986) Molecular cloning and DNA sequence of the Arabidopsis thaliana alcohol dehydrogenase gene. Proc Natl Acad Sci USA 83:1408-1412 https://doi.org/10.1073/pnas.83.5.1408
  8. Cho YG, Kang HJ, Lee JS, Lee YT, Lim SJ, Gauch H, Eun MY, McCouch SR (2007) Identification of quantitative trait loci in rice for yield, yield components, and agronomic traits across years and locations. Crop Sci 47:2403-2417 https://doi.org/10.2135/cropsci2006.08.0509
  9. Christou P, Ford TL, Kofron M (1991) Production of transgenic rice (Oryza sativa L.) plants from agronomically important indica and japonica varieties via electric discharge particle acceleration of exogenous DNA into immature zygotic embryos. Bio Technology 9:957-962 https://doi.org/10.1038/nbt1091-957
  10. Chung H-J, Ferl RJ (1999) Arabidopsis alcohol dehydrogenase expression in both shoots and roots is conditioned by root growth environment. Plant Physiol 121:429-436 https://doi.org/10.1104/pp.121.2.429
  11. Cobb BG, Kennedy RA (1987) Distribution of alcohol dehydrogenase in roots and shoots of rice (Oryza sativa) and Echinochloa seedlings. Plant Cell Environ 10:633-638 https://doi.org/10.1111/j.1365-3040.1987.tb01845.x
  12. Colmer TD (2003) Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant Cell Environ 26:17-36 https://doi.org/10.1046/j.1365-3040.2003.00846.x
  13. Crawford R MM (1992) Oxygen availability as an ecological limit to plant distribution. Adv Ecol Res 23:93-185 https://doi.org/10.1016/S0065-2504(08)60147-6
  14. Datta SK, Peterhans A, Datta K, Potrykus I (1990) Genetically engineered fertile indica rice recovered from protoplasts. Bio Technology 8:736-740 https://doi.org/10.1038/nbt0890-736
  15. Davey MR, Kothari SL, Zhang H, Rech EL, Cocking EC, Lynch PT (1991) Transgenic rice: characterization of protoplast- derived plants and their seed progeny. J Exp Bot 42:1159-1169 https://doi.org/10.1093/jxb/42.9.1159
  16. Dennis ES, Dolferus R, Ellis M, Rahman M, Wu Y, Hoeren FU, Grover A, Ismond KP, Good AG, Peacock WJ (2000) Molecular strategies for improving waterlogging tolerance in plants. J Exp Bot 51:89-97 https://doi.org/10.1093/jexbot/51.342.89
  17. Dolferus R, Klok EJ, Delessert C, Wilson S, Ismond KP, Good AG, Peacock WJ, Dennis ES (2003) Enhancing the anaerobic response. Ann Bot 91:111-117 https://doi.org/10.1093/aob/mcf048
  18. Drew MC (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annu Rev Plant Physiol Plant Mol Biol 48:223-250 https://doi.org/10.1146/annurev.arplant.48.1.223
  19. Drew MC, He CJ, Morgan PW (2000) Programmed cell death and aerenchyma formation in roots. Trends Plant Sci 5: 123-127 https://doi.org/10.1016/S1360-1385(00)01570-3
  20. Freeling M, Bennett DC (1985) Maize Adh1. Ann Rev Genet 19:297-323 https://doi.org/10.1146/annurev.ge.19.120185.001501
  21. Gibbs J, Greenway H (2003) Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Funct Plant Biol 30:41-47
  22. Grichko VP and Glick BR (2001) Flooding tolerance of transgenic tomato plants expressing the bacterial enzyme ACC deaminase controlled by the 35S, rolD or PRB-1b promoter. Plant Physiol Biochem 39:19-25 https://doi.org/10.1016/S0981-9428(00)01217-1
  23. Gottlieb LD (1982) Conservation and duplication of isozymes in plants. Science 216:373-380 https://doi.org/10.1126/science.216.4544.373
  24. Hansen G (2000) Evidence for Agrobacterium-induced apoptosis in maize cells. Mol Plant-Microbe Interact 13:649-657 https://doi.org/10.1094/MPMI.2000.13.6.649
  25. Hensel G, Valkov V, Middlefell-Williams J, Kumlehn J (2008) Efficient generation of transgenic barley: the way forward to modulate plant-microbe interactions. J Plant Physiol 165:71-82 https://doi.org/10.1016/j.jplph.2007.06.015
  26. Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271-282 https://doi.org/10.1046/j.1365-313X.1994.6020271.x
  27. Ishida Y, Saito H, Oita S, Hiei Y, Komari T, Kumashito T (1996) High efficiency transformation of maize (Zea mays L.) mediated by Agrobacterium tumefaciens. Nat Biotechnol 14:745-750 https://doi.org/10.1038/nbt0696-745
  28. Jackson MB (1985) Ethylene and the responses of plants to soil water-logging and submergence. Annu Rev Plant Physiol 36:145-174 https://doi.org/10.1146/annurev.pp.36.060185.001045
  29. Jeon JS, Lee S, Jung KH (2000) T-DNA insertional mutagenesis for functional genomics in rice. Plant J 22:561-570 https://doi.org/10.1046/j.1365-313x.2000.00767.x
  30. Johnson JR, Cobb BG, Drew MC (1994) Hypoxic induction of anoxia tolerance in roots of Adh1 null Zea mays L. Plant Physiol 105:61-67 https://doi.org/10.1104/pp.105.1.61
  31. Kadowaki KI, Matsuoka M, Murai N, Harada K (1988) Induction of two alcohol dehydrogenase polypeptides in rice roots during anaerobiosis. Plant Science. 54:29-36. https://doi.org/10.1016/0168-9452(88)90052-0
  32. Kennedy RA, Rumpho ME, Fox TC (1992) Anaerobic metabolism in plants. Plant Physiol 84:1204-1209
  33. Kordan HA (1977) Coleoptile emergence in rice seedlings in different oxygen environments. Annals of Botany 41:1205-1209 https://doi.org/10.1093/oxfordjournals.aob.a085410
  34. Lasanthi-Kudahettige R, Magneschi L, Loreti E, Gonzali S, Licausi F, Giacomo N, Berreta O, Federico V, Alpi A, Perata P (2007) Transcript profiling of the anoxic rice coleoptile. Plant Physiol 144:218-231. https://doi.org/10.1104/pp.106.093997
  35. Lee S, Jeon JS, Jung KH, An G (1999) Binary vector for efficient transformation of rice. J Plant Biol 42:310-316 https://doi.org/10.1007/BF03030346
  36. Li Z, Burow MD, Murai N (1990) High frequency generation of fertile transgenic rice plants after PEG-mediated protoplast transformation. Plant Mol Biol Rep 8:276-291 https://doi.org/10.1007/BF02668764
  37. Liao CT, Lin CL (2001) Physiological adaptation of crop plants to flooding stress. Proc Natl Sci Counc Repub China B 25:148-157
  38. Mergemann H, Sauter M (2000) Ethylene induces epidermal cell death at the site of adventitious root emergence in rice. Plant Physiol 124:609-614 https://doi.org/10.1104/pp.124.2.609
  39. Mooney PA, Goodwin PB, Dennis ES, Liewellyn DJ (1991) Agrobacterium tumefaciens-gene transfer into wheat tissues. Plant Cell Tissue Organ Cult 25:209-218
  40. Mujer CV, Rumpho ME, Lin JJ, Kennedy RA (1993) Constitutive and inducible aerobic and anaerobic stress proteins in the Echinochloa complex and rice. Plant Physiol 101:217-226 https://doi.org/10.1104/pp.101.1.217
  41. Mocquot B, Prat C, Mouches C, Pradet A (1981) Effect of anoxia on energy charge and protein synthesis in rice embryo. Plant Phy.siology 68:636-640 https://doi.org/10.1104/pp.68.3.636
  42. Narashimulu SB, Deng XB, Sarria R, Gelvin SB (1996) Early transcription of Agrobacterium T-DNA genes in tobacco and maize. Plant Cell 8:873-886 https://doi.org/10.1105/tpc.8.5.873
  43. Pathuri IP, Reitberger IE, Hückelhoven R, Proels RK (2011) Alcohol dehydrogenase 1 of barley modulates susceptibility to the parasitic fungus Blumeria graminis f.sp. hordei. J Exp Bot in press
  44. Perata P, Gugloelminetti L, Alpi A (1997) Mobilization of endorsperm reserves in cereal seeds under anoxia. Ann Bot 79:49-56 https://doi.org/10.1093/oxfordjournals.aob.a010306
  45. Quimio CA, Torrizo LB, Setter TL, Ellis M, Grover A, Abrigo EM, Oliva NP, Ella ES, Carpena AL, Ito O et al. (2000) Enhancement of submergence tolerance in transgenic rice overproducing pyruvate decarboxylase. J Plant Physiol 156:516-521 https://doi.org/10.1016/S0176-1617(00)80167-4
  46. Raineri DM, Bonitto P, Gordon MP, Nester EW (1990) Agrobacterium-mediated transformation in rice (Oryza sativa L.). Bio Technology 8:33-38 https://doi.org/10.1038/nbt0190-33
  47. Ricard B, Mocquot B, Fournier A, Delseny M, Pradet A (1986) Expression of alcohol dehydrogenase in rice embryos under anoxia. Plant Mol Bio 7:321-329 https://doi.org/10.1007/BF00032562
  48. Ritchie SW, Lui CHN, Sellmer JC, Kononowicz H, Hodges TK, Gelvin SB (1993) Agrobacterium tumefaciens-mediated expression of gusA in maize tissues. Trans Res 2:252-265 https://doi.org/10.1007/BF01968838
  49. Roberts JKM, Callis J, Wemmer D, Walbot V, Jardetzky O (1984) Mechanism of cytosolic pH regulation in hypoxic maize root tips and its role in survival under anoxia. Proc Nat Acad Sci USA 81:33791-3383
  50. Sallaud C, Meynard D, Boxtel JV (2003) Highly efficient production and characterization of T-DNA plants for rice (Oryza sativa L.) functional genomics. Theor Appl Genet 106:1396-1408 https://doi.org/10.1007/s00122-002-1184-x
  51. Sauter M (2000) Rice in deep water: How to take heed against a sea of troubles. Naturwissenschaften. 87:289-303 https://doi.org/10.1007/s001140050725
  52. Setter TL, Ellis M, Laureles EV, Ella ES, Senadhira D, Mishra SB, Sarkarung S, Datta S (1997) Physiology and genetics of submergence tolerance in in rice. Ann Bot 79:67-77 https://doi.org/10.1006/anbo.1996.0304
  53. Shimamoto K, Terada R, Izawa T, Fujimoto H (1989) Fertile transgenic rice plants regenerated from transformed protoplasts. Nature 238:274-276
  54. Shimomura S, Beevers H (1983) Alcohol dehydrogenase and an inactivator from rice seedlings. Plant Physiol 71:736-741 https://doi.org/10.1104/pp.71.4.736
  55. Tai HT, Tanksley SD (1990) A rapid and inexpensive method for isolation of total DNA from dehydrated plant tissue. Plant Mol Bio Reporter 8:297-303 https://doi.org/10.1007/BF02668766
  56. Takahaski N (1978) Adaptive importance of mesocotyl and coleopile growth in rice under different moisture regimes. Australian J Pant Physiol 5:511-517 https://doi.org/10.1071/PP9780511
  57. Tingay S, McElroy D, Kalla R, Fieg S, Wang M, Thornton S, Brettel R (1997) Agrobacterium tumefaciens-mediated barley transformation. Plant J 11:1369-1376 https://doi.org/10.1046/j.1365-313X.1997.11061369.x
  58. Toki S, Hara N, Ono K, Onodera H, Tagiri A, Oka S, Tanaka H (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J 47:969-976 https://doi.org/10.1111/j.1365-313X.2006.02836.x
  59. Thompson C, Fernandes C, De Souza O, De Freitas L, Salzano F (2010) Evaluation of the impact of functional diversification on Poaceae, Brassicaceae, Fabaceae, and Pinaceae alcohol dehydrogenase enzymes. J Mol Modeling 16:919-928 https://doi.org/10.1007/s00894-009-0576-0
  60. Turner F, Chen TC, McCauly GN (1981) Morphological development of rice seedling in water at controlled oxygen levels. Agronomy J 73:566-570 https://doi.org/10.2134/agronj1981.00021962007300030037x
  61. Uze M, Wunn J, Puonti-Kaerlas J, Potrykus I, Sautter C (1997) Plasmolysis of precultured immature embryos improves Agrobacterium mediated gene transfer to rice (Oryza sativa L.). Plant Sci 130:87-95 https://doi.org/10.1016/S0168-9452(97)00211-2
  62. Vartepetian BB, Mazlik P, Lance C (1978) Lipid biosynthesis in rice coleoptiles grown in the presence or in the absence of oxygen. Plant Sci Lett 13:321-328 https://doi.org/10.1016/0304-4211(78)90209-2
  63. Vartapetian BB, Jackson MB (1997) Plant adaptations to anaerobic stress. Ann Bot 79:3-20 https://doi.org/10.1006/anbo.1996.0295
  64. Voesenek LACJ, Benschop JJ, Bou J, Cox MCH, Groeneveld HW, Millenaar FF, Vreeburg RAM, Peeters AJM (2003) Interactions between plant hormones regulate submergenceinduced shoot elongation in the flooding-tolerant dicot Rumex palustris. Ann Bot 91:205-211 https://doi.org/10.1093/aob/mcf116
  65. Voesenek LACJ, Colmer TD, Pierik R, Millenaar FF, Peters AJM (2006) How plants cope with complete submergence. New Phytol 170:213-226 https://doi.org/10.1111/j.1469-8137.2006.01692.x
  66. Xie Y, Wu R (1989) Rice alcohol dehydrogenase genes: anaerobic induction, organ specific expression and characterization of cDNA clones. Plant Mol Bio 13:53-68 https://doi.org/10.1007/BF00027335
  67. Xu Y, Buchholz WG, DeRose RT, Hall TC (1995) Characterization of a novel gene family from rice that encodes root-specific proteins. Plant Mol Biol 27:237-248 https://doi.org/10.1007/BF00020180
  68. Zhang J, Van Toai T, Huynh L, Preiszner J (2000) Development of flooding tolerant Arabidopsis thaliana by autoregulated cytokinin production. Mol Breed 6:135-144 https://doi.org/10.1023/A:1009694029297

Cited by

  1. Overexpression of the glutamine synthetase gene modulates oxidative stress response in rice after exposure to cadmium stress vol.32, pp.10, 2013, https://doi.org/10.1007/s00299-013-1464-8
  2. BrUGE1 transgenic rice showed improved growth performance with enhanced drought tolerance vol.66, pp.2, 2016, https://doi.org/10.1270/jsbbs.66.226
  3. Isolation and functional characterization of BrUGT gene encoding a UDP-glycosyltransferase from Chinese cabbage (Brassica rapa) vol.39, pp.3, 2012, https://doi.org/10.5010/JPB.2012.39.3.212