Betaine aldehyde dehydrogenase genes from Arabidopsis with different sub-cellular localization affect stress responses

Planta

Volumn 233, Issue 2, 2011, Pages 369-382

  Missihoun, Tagnon D ^a   Schmitz, Jessica ^a,b   Klug, Rebecca ^a   Kirch, Hans Hubert ^a   Bartels, Dorothea ^a  

^a UNIVERSITY OF BONN   (Germany)

^b Botanical Institute   (Germany)

Author keywords

Abiotic stress; Aminoaldehyde; Betaine aldehyde; Glycine betaine; Leucoplasts; Peroxisomes

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 79151481012     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-010-1297-4     Document Type: Article

References (72)

1. Alonso JM et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
2. An Y-Q, McDowell JM, Huang S, McKinney EC, Chambliss S, Meagher RB (1996) Strong, constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass in vegetative tissues. Plant J 10: 107-121.
3. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59: 206-216.
4. Aziz A, Martin-Tanguy J, Larher F (1998) Stress-induced changes in polyamine and tyramine levels can regulate proline accumulation in tomato leaf discs treated with sodium chloride. Physiol Plant 104: 195-202.
5. Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. CRC Crit Rev Plant Sci 24: 23-58.
6. Bartels D, Schneider K, Terstappen G, Piatkowski D, Salamini F (1990) Molecular cloning of abscisic acid-modulated genes which are induced during desiccation of the resurrection plant Craterostigma plantagineum. Planta 181: 27-34.
7. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39: 205-207.
8. Bevan M (1984) Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res 12: 8711-8721.
9. Bhuiyan NH, Hamada A, Yamada N, Rai V, Hibino T, Takabe T (2007) Regulation of betaine synthesis by precursor supply and choline monooxygenase expression in Amaranthus tricolor. J Exp Bot 58: 4203-4212.
10. Bouché N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9: 110-115.
11. Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140: 103-125.
12. Bradbury LME, Gillies SA, Brushett D, Waters DLE, Henry RJ (2008) Inactivation of an aminoaldehyde dehydrogenase is responsible for fragrance in rice. Plant Mol Biol 68: 439-449.
13. Bradley MO (1973) Microfilaments and cytoplasmic streaming: Inhibition of streaming with cytochalasin. J Cell Sci 12: 327-343.
14. Burnet M, Lafontaine PJ, Hanson AD (1995) Assay, purification, and partial characterization of choline monooxygenase from spinach. Plant Physiol 108: 581-588.
15. Chen WP, Li PH, Chen THH (2000) Glycinebetaine increases chilling tolerance and reduces chilling-induced lipid peroxidation in Zea mays L. Plant Cell Environ 23: 609-618.
16. Chen S, Yang Y, Shi W, Ji Q, He F, Zhang Z, Cheng Z, Liu X, Xu M (2008) Badh2, encoding betaine aldehyde dehydrogenase, inhibits the biosynthesis of 2-acetyl-1-pyrroline, a major component in rice fragrance. Plant Cell 20: 1850-1861.
17. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
18. Cona A, Rea G, Angelini R, Federico R, Tavladoraki P (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci 11: 80-88.
19. Cuevas JC, Lopez-Cobollo R, Alcazar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol 148: 1094-1105.
20. Duhazé C, Gouzerh G, Gagneul D, Larher F, Bouchereau A (2002) The conversion of spermidine to putrescine and 1, 3-diaminopropane in the roots of Limonium tataricum. Plant Sci 163: 639-646.
21. Eubel H, Meyer EH, Taylor NL, Bussell JD, O'Toole N, Heazlewood JL, Castleden I, Small ID, Smith SM, Millar AH (2008) Novel proteins, putative membrane transporters, and an integrated metabolic network are revealed by quantitative proteomic analysis of Arabidopsis cell culture peroxisomes. Plant Physiol 148: 1809-1829.
22. Fitzgerald TL, Waters DLE, Henry RJ (2008) The effect of salt on betaine aldehyde dehydrogenase transcript levels and 2-acetyl-1-pyrroline concentration in fragrant and non-fragrant rice (Oryza sativa). Plant Sci 174: 539-546.
23. Fitzgerald TL, Waters DLE, Henry RJ (2009) Betaine aldehyde dehydrogenase in plants. Plant Biol 11: 119-130.
24. Fitzgerald TL, Waters DLE, Brooks LO, Henry RJ (2010) Fragrance in rice (Oryza sativa L.) is associated with reduced yield under salt treatment. Environ Exp Bot 68: 292-300.
25. Fujiwara T, Hori K, Ozaki K, Yokota Y, Mitsuya S, Ichiyanagi T, Hattori T, Takabe T (2008) Enzymatic characterization of peroxisomal and cytosolic betaine aldehyde dehydrogenases in barley. Physiol Plant 134: 22-30.
26. Harinasut P, Tsutsui K, Takabe T, Nomura M, Takabe T, Kishitani S (1996) Exogenous glycinebetaine accumulation and increased salt-tolerance in rice seedlings. Biosci Biotech Biochem 60: 366-368.
27. Hibino T, Meng YL, Kawamitsu Y, Uehara N, Matsuda N, Tanaka Y, Ishikawa H, Baba S, Takabe T, Wada K, Ishii T, Takabe T (2001) Molecular cloning and functional characterization of two kinds of betaine-aldehyde dehydrogenase in betaine-accumulating mangrove Avicennia marina (Forsk.) Vierh. Plant Mol Biol 45: 353-363.
28. Hibino T, Waditee R, Araki E, Ishikawa H, Aoki K, Tanaka Y, Takabe T (2002) Functional characterization of choline monooxygenase, an enzyme for betaine synthesis in plants. J Biol Chem 277: 41352-41360.
29. Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207: 604-611.
30. Holmström KO, Somersalo S, Mandal A, Palva TE, Welin B (2000) Improved tolerance to salinity and low temperature in transgenic tobacco producing glycine betaine. J Exp Bot 51: 177-185.
31. Incharoensakdi A, Takabe T, Akazawa T (1986) Effect of betaine on enzyme activity and subunit interaction of ribulose-1, 5-bisphosphate carboxylase/oxygenase from Aphanothece halophytical. Plant Physiol 81: 1044-1049.
32. Jedd G, Chua NH (2002) Visualization of peroxisomes in living plant cells reveals acto-myosin-dependent cytoplasmic streaming and peroxisome budding. Plant Cell Physiol 43: 384-392.
33. Kamada-Nobusada T, Hayashi M, Fukazawa M, Sakakibara H, Nishimura M (2008) A putative peroxisomal polyamine oxidase, AtPAO4, is involved in polyamine catabolism in Arabidopsis thaliana. Plant Cell Physiol 49: 1272-1282.
34. Kinnersley AM, Turano FJ (2000) Gama aminobutyric acid (GABA) and plant responses to stress, Crit. Rev. Plant Sci 19: 479-509.
35. 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.
36. Kirch H-H, Bartels D, Wei Y, Schnable PS, Wood AJ (2004) The ALDH gene superfamily of Arabidopsis. Trends Plant Sci 9: 371-377.
37. Kotchoni S, 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.
38. Livingstone JR, Maruo T, Yoshida I, Tarui Y, Hirooka K, Yamamoto Y, Tsutui N, Hirasawa E (2003) Purification and properties of betaine aldehyde dehydrogenase from Avena sativa. J Plant Res 116: 133-140.
39. Maiale S, Sanchez DH, Guirda A, Vidal A, Ruiz O (2004) Spermine accumulation under salt stress. J Plant Physiol 161: 35-42.
40. Morgan DM (1987) Oxidized polyamines and the growth of human vascular endothelial cells. Prevention of cytotoxic effects by selective acetylation. Biochem J 242: 347-352.
41. Moschou PN, Sanmartin M, Andriopoulou AH, Rojo E, Sanchez-Serrano JJ, Roubelakis-Angelakis KA (2008a) Bridging the gap between plant and mammalian polyamine catabolism: a novel peroxisomal polyamine oxidase responsible for a full back-conversion pathway in Arabidopsis. Plant Physiol 147: 1845-1857.
42. 2 signatures that direct tolerance responses in tobacco. Plant Cell 20: 1708-1724.
43. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15: 473-497.
44. Nakamura T, Yokota S, Muramoto Y, Tsutsui K, Oguri Y, Fukui K, Takabe T (1997) Expression of a betaine aldehyde dehydrogenase gene in rice, a glycine betaine nonaccumulator, and possible localization of its protein in peroxisomes. Plant J 11: 1115-1120.
45. Nakamura T, Nomura M, Mori H, Jagendorf A, Ueda A, Takabe T (2001) An isozyme of betaine aldehyde dehydrogenase in barley. Plant Cell Physiol 42: 1088-1092.
46. Niu X, Tang W, Huang W, Ren G, Wang Q, Luo D, Xiao Y, Yang S, Wang F, Lu BR, Gao F, Lu T, Liu Y (2008) RNAi-directed downregulation of OsBADH2 results in aroma (2-acetyl-1-pyrroline) production in rice (Oryza sativa L.). BMC Plant Biol 8: 100.
47. Nuccio ML, Russell BL, Nolte KD, Rathinasabapathi B, Gage DA, Hanson AD (1998) The endogenous choline supply limits glycine betaine synthesis in transgenic tobacco expressing choline monooxygenase. Plant J 16: 487-496.
48. Petrivalsky M, Brauner F, Luhova L, Gagneul D, Sebela M (2007) Aminoaldehyde dehydrogenase activity during wound healing of mechanically injured pea seedlings. J Plant Physiol 164: 1410-1418.
49. Rathinasabapathi B, Burnet M, Russell BL, Gage DA, Liao PO, Nye GJ, Scott P, Golbeck JH, Hanson AD (1997) Choline monooxygenase, an unusual iron-sulfur enzyme catalyzing the first step of glycine betaine synthesis in plants: prosthetic group characterization and cDNA cloning. Proc Natl Acad Sci USA 94: 3454-3458.
50. Reichel C, Mathur J, Ecker P, Langenkemper K, Koncz C, Schell J, Reiss B, Maas C (1996) Enhanced green fluorescence by the expression of an aequorea victoria green fluorescent protein mutant in mono- and dicotyledonous plant cells. Proc Natl Acad Sci USA 93: 5888-5893.
51. Reumann S (2004) Specification of the peroxisome targeting signals type 1 and type 2 of plant peroxisomes by bioinformatics analyses. Plant Physiol 135: 783-800.
52. Reumann S, Quan S, Aung K, Yang P, Manandhar-Shrestha K, Holbrook D, Linka N, Switzenberg R, Wilkerson CG, Weber APM, Olsen LJ, Hu J (2009) In-depth proteome analysis of Arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes. Plant Physiol 150: 125-143.
53. Robinson SJ, Tang LH, Mooney BA, McKay SJ, Clarke WE, Links MG, Karcz S, Regan S, Wu YY, Gruber MY, Cui D, Yu M, Parkin IA (2009) An archived activation tagged population of Arabidopsis thaliana to facilitate forward genetics approaches. BMC Plant Biol 9: 101.
54. Rosso MG, Li Y, Strizhov N, Reiss B, Dekker K, Weisshaar B (2003) An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol Biol 53: 247-259.
55. Sakamoto A, Murata N (2002) The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ 25: 163-171.
56. Sandford JC, Smith FD, Russel JA (1993) Optimizing the biolistic process for different biological applications. Methods Enzymol 217: 483-509.
57. Sebela M, Brauner F, Radova A, Jacobsen S, Havlis J, Galuszka P, Pec P (2000) Characterisation of a homogeneous plant aminoaldehyde dehydrogenase. Biochim Biophys Acta 1480: 329-341.
58. Seki M, Narusaka M, Kamiya A, Ishida J, Satou M, Sakurai T, Nakajima M, Enju A, Akiyama K, Oono Y, Muramatsu M, Hayashizaki Y, Kawai J, Carninci P, Itoh M, Ishii Y, Arakawa T, Shibata K, Shinagawa A, Shinozaki K (2002) Functional annotation of a full-length Arabidopsis cDNA collection. Science 296: 141-145.
59. Shelp BJ, Bown AW, McLean MD (1999) Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci 4: 446-452.
60. Shirasawa K, Takabe T, Takabe T, Kishitani S (2006) Accumulation of glycine betaine in rice plants that overexpress choline monooxygenase from spinach and evaluation of their tolerance to abiotic stress. Ann Bot 98: 565-571.
61. Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochem 28: 1057-1060.
62. Smith TA (1985) The di and polyamine oxidases of higher plants. Biochem Soc Trans 13: 319-322.
63. Sophos NA, Vasiliou V (2003) Aldehyde dehydrogenase gene superfamily: the 2002 update. Chem Biol Interact 143-144: 5-22.
64. 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: 452-465.
65. Takabe T, Rai V, Hibino T (2006) Metabolic engineering of glycinebetaine. In: Rai AK, Takabe T (eds) Abiotic stress tolerance in plants. Springer, Berlin, pp 137-151.
66. Trossat C, Rathinasabapathi B, Hanson AD (1997) Transgenically expressed betaine aldehyde dehydrogenase efficiently catalyzes oxidation of dimethylsulfoniopropionaldehyde and (omega)-aminoaldehydes. Plant Physiol 113: 1457-1461.
67. Tsien RY (1998) The green fluorescent protein. Annu Rev Biochem 67: 509-544.
68. Weigel P, Weretilnyk EA, Hanson AD (1986) Betaine aldehyde oxidation by spinach chloroplasts. Plant Physiol 82: 753-759.
69. Xing SG, Jun YB, Hau ZW, Liang LY (2007) Higher accumulation of γ-aminobutyric acid induced by salt stress through stimulating the activity of diamine oxidases in Glycine max (L.) Merr. roots. Plant Physiol Biochem 45: 560-566.
70. Yamaguchi-Shinozaki K, Shinozaki K (1993) Arabidopsis DNA encoding two desiccation-responsive rd29 genes. Plant Physiol 101: 1119-1120.
71. Yang J, Zhang J, Liu K, Wang Z, Liu L (2007) Involvement of polyamines in the drought resistance of rice. J Exp Bot 58: 1545-1555.
72. Yu Z, Li W, Brunk UT (2003) 3-Aminopropanal is a lysosomotropic aldehyde that causes oxidative stress and apoptosis by rupturing lysosomes. APMIS 111: 643-652.