Skip to main content
Log in

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

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Arabidopsis thaliana belongs to those plants that do not naturally accumulate glycine betaine (GB), although its genome contains two genes, ALDH10A8 and ALDH10A9 that code for betaine aldehyde dehydrogenases (BADHs). BADHs were initially known to catalyze the last step of the biosynthesis of GB in plants. But they can also oxidize metabolism-derived aminoaldehydes to their corresponding amino acids in some cases. This study was carried out to investigate the functional properties of Arabidopsis BADH genes. Here, we have shown that ALDH10A8 and ALDH10A9 proteins are targeted to leucoplasts and peroxisomes, respectively. The expression patterns of ALDH10A8 and ALDH10A9 genes have been analysed under abiotic stress conditions. Both genes are expressed in the plant and weakly induced by ABA, salt, chilling (4°C), methyl viologen and dehydration. The role of the ALDH10A8 gene was analysed using T-DNA insertion mutants. There was no phenotypic difference between wild-type and mutant plants in the absence of stress. But ALDH10A8 seedlings and 4-week-old plants were more sensitive to dehydration and salt stress than wild-type plants. The recombinant ALDH10A9 enzyme was shown to oxidize betaine aldehyde, 4-aminobutyraldehyde and 3-aminopropionaldehyde to their corresponding carboxylic acids. We hypothesize that ALDH10A8 or ALDH10A9 may serve as detoxification enzymes controlling the level of aminoaldehydes, which are produced in cellular metabolism under stress conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

ABAL:

4-Aminobutyraldehyde

AMADH:

Aminoaldehyde dehydrogenase

APAL:

3-Aminopropionaldehyde

BADH:

Betaine aldehyde dehydrogenase

CAO:

Copper amine oxidase

CDS:

Coding sequence

COX:

Choline oxidase

CMO:

Choline monooxygenase

GABA:

4-Aminobutyric acid

GB:

Glycine betaine

GFP:

Green fluorescent protein

PAO:

Polyamine oxidase

References

  • Alonso JM et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bevan M (1984) Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res 12:8711–8721

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bouché N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9:110–115

    Article  PubMed  Google Scholar 

  • Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bradley MO (1973) Microfilaments and cytoplasmic streaming: Inhibition of streaming with cytochalasin. J Cell Sci 12:327–343

    CAS  PubMed  Google Scholar 

  • Burnet M, Lafontaine PJ, Hanson AD (1995) Assay, purification, and partial characterization of choline monooxygenase from spinach. Plant Physiol 108:581–588

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Fitzgerald TL, Waters DLE, Henry RJ (2009) Betaine aldehyde dehydrogenase in plants. Plant Biol 11:119–130

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kinnersley AM, Turano FJ (2000) Gama aminobutyric acid (GABA) and plant responses to stress, Crit. Rev. Plant Sci 19:479–509

    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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Maiale S, Sanchez DH, Guirda A, Vidal A, Ruiz O (2004) Spermine accumulation under salt stress. J Plant Physiol 161:35–42

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA (2008b) Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell 20:1708–1724

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Sandford JC, Smith FD, Russel JA (1993) Optimizing the biolistic process for different biological applications. Methods Enzymol 217:483–509

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Shelp BJ, Bown AW, McLean MD (1999) Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci 4:446–452

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochem 28:1057–1060

    Article  CAS  Google Scholar 

  • Smith TA (1985) The di and polyamine oxidases of higher plants. Biochem Soc Trans 13:319–322

    CAS  PubMed  Google Scholar 

  • Sophos NA, Vasiliou V (2003) Aldehyde dehydrogenase gene superfamily: the 2002 update. Chem Biol Interact 143–144:5–22

    Article  PubMed  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 35:452–465

    Article  CAS  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Tsien RY (1998) The green fluorescent protein. Annu Rev Biochem 67:509–544

    Article  CAS  PubMed  Google Scholar 

  • Weigel P, Weretilnyk EA, Hanson AD (1986) Betaine aldehyde oxidation by spinach chloroplasts. Plant Physiol 82:753–759

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1993) Arabidopsis DNA encoding two desiccation-responsive rd29 genes. Plant Physiol 101:1119–1120

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Financial support is gratefully acknowledged from the German Academic Exchange Service (Deutscher Akademischer Austauschdienst Dienst: DAAD) (fellowship to Tagnon D. Missihoun) and from the German Research Foundation (Deutsche Forschungsgemeinschaft: DFG)–Arabidopsis Functional Genomics Network (AFGN) project (BA 712/3-3). We would like to thank Dr G. Jach for making the GFP vector pGJ280 available, Dr. G. Pilot for providing the binary vector pPTkan3, Dr. B. Buchen for advice on the microscopy and for critically reading the manuscript, Prof. Dr. A. Weber, University of Düsseldorf, for discussing betaine measurements. D.B. is a member of the European COST action INPAS (International Network of Abiotic Stress).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dorothea Bartels.

Electronic supplementary material

Below is the link to the electronic supplementary material.

425_2010_1297_MOESM1_ESM.doc

Purification of the A. thaliana ALDH10A8 and ALDH10A9 recombinant proteins by His-tag affinity chromatography under native conditions. F0: total soluble fraction; Ft: Flow- through fraction; F1F8: Eluted fractions (250 µl). Five microliters from each fraction were loaded onto the SDS-polyacrylamide gel (DOC 3270 kb)

425_2010_1297_MOESM2_ESM.doc

Expression of ALDH10A8 and ALDH10A9 in E. coli BL21 cells.(a) Growth in liquid medium. Cells harbouring empty pET28 (pET), pET-10A8 or pET-10A9 vectors were cultured in liquid LB medium supplemented with 1 mM H2O2 or 500 mM NaCl. Neither H2O2 (b) nor NaCl (c) were added to the control cultures (a). The expression of the recombinant protein was induced by adding IPTG to 0.1 mM final concentration. Cell density was determined at various time points as absorbance at 600 nm. Arrows indicate the time-point when H2O2 or NaCl were added (DOC 50 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Missihoun, T.D., Schmitz, J., Klug, R. et al. Betaine aldehyde dehydrogenase genes from Arabidopsis with different sub-cellular localization affect stress responses. Planta 233, 369–382 (2011). https://doi.org/10.1007/s00425-010-1297-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-010-1297-4

Keywords

Navigation