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Glycine betaine: a versatile compound with great potential for gene pyramiding to improve crop plant performance against environmental stresses

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Abstract

Plants are frequently exposed to a plethora of environmental stresses. Being sessile creatures, they have to tolerate any stresses by altering their metabolism. To achieve tolerance, plants synthesize compatible compounds such as glycine betaine (GB). Continuous research over the years has increased our understanding about the mechanisms of stress protection by GB, which range from an osmolyte to a chaperone and from maintenance of reactive oxygen species to gene expression inducer. Various crop plants have also been transformed to synthesize GB along with model plants by introducing bacterial or plant genes. The GB-synthesizing crop plants exhibit enhanced tolerance to various abiotic stresses and out-yield wild-type plants in stressful conditions. GB has also been utilized to improve enhanced stress tolerance by utilizing it in gene stacking experiments due to its synergistic and stabilizing effects. It is reviewed here (along with comparative analysis of GB synthesis pathways and its mechanism to improve tolerance) showing that gene stacking by using GB as one component provides substantial protection. This synergistic role of GB leads us to hypothesize that it can be utilized in virtually any kind of gene stacking experiments to develop crop plants to be grown in arable and marginal lands for better tolerance to ever-changing environmental conditions and to ensure food security in underdeveloped regions of the world.

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References

  • Ahmad R, Kim MD, Back KH, Kim HS, Lee HS, Kwon SY, Murata N, Chung WI, Kwak SS (2008) Stress-induced expression of choline oxidase in potato plant chloroplasts confers enhanced tolerance to oxidative, salt, and drought stresses. Plant Cell Rep 27:687–698

    Article  PubMed  CAS  Google Scholar 

  • Ahmad R, Kim YH, Kim MD, Kwon SY, Cho K, Lee HS, Kwak SS (2010) Simultaneous expression of choline oxidase, superoxide dismutase and ascorbate peroxidase in potato plant chloroplasts provides synergistically enhanced protection against various abiotic stresses. Physiol Plant 138:520–533

    Article  PubMed  CAS  Google Scholar 

  • Aono M, Saji H, Sakamoto A, Tanaka K, Kondo N, Tanaka K (1995) Paraquat tolerance of transgenic Nicotiana tabacum with enhanced activities of glutathione reductase and superoxide dismutase. Plant Cell Physiol 36:1687–1691

    PubMed  CAS  Google Scholar 

  • Aran I, Tetsuko T, Takashi A (1986) Effect of betaine on enzyme activity and subunit interaction of ribulose-1,5-bisphosphate carboxylase/oxygenase from Aphanothece halophytica. Plant Physiol 81:1044–1049

    Article  Google Scholar 

  • Bhattacharya RC, Maheswari M, Dineshkumar V, Kirti PB, Bhat SR, Chopra VL (2004) Transformation of Brassica oleracea var. Capitata with bacterial betA gene enhances tolerance to salt stress. Sci Hortic 100:215–227

    Article  CAS  Google Scholar 

  • Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111

    PubMed  CAS  Google Scholar 

  • Bourot S, Sire O, Trautwetter A, Touzé T, Wu LF, Blanco C, Bernard T (2000) Glycine betaine-assisted protein folding in a LysA mutant of Escherichia coli. J Biol Chem 275:1050–1056

    Article  PubMed  CAS  Google Scholar 

  • Chen THH, 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

    Article  PubMed  CAS  Google Scholar 

  • Chen TH, Murata N (2008) Glycinebetaine: an effective protectant against abiotic stress in plants. Trends Plant Sci 13:499–505

    Article  PubMed  CAS  Google Scholar 

  • Chen TH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20

    Article  PubMed  CAS  Google Scholar 

  • Csonka LN, Hanson AD (1991) Prokaryotic osmoregulation: genetics and physiology. Annu Rev Microbiol 45:569–606

    Article  PubMed  CAS  Google Scholar 

  • Deshnium P, Los D, Hayashi H, Mustardy L, Murata N (1995) Transformation of synechococcus with a gene for choline oxidase enhances tolerance to salt stress. Plant Mol Biol 29:897–907

    Article  PubMed  CAS  Google Scholar 

  • Diamant S, Rosenthal D, Azem A, Eliahu N, Ben-Zvi AP, Goloubinoff P (2003) Dicarboxylic amino acids and glycine-betaine regulate chaperone-mediated protein-disaggregation under stress. Mol Microbiol 49:401–410

    Article  PubMed  CAS  Google Scholar 

  • Duan X, Song Y, Yang A, Zhang J (2009) The transgene pyramiding tobacco with betaine synthesis and heterologous expression of AtNHX1 is more tolerant to salt stress than either of the tobacco lines with betaine synthesis or AtNHX1. Physiol Plant 135:281–295

    Article  PubMed  CAS  Google Scholar 

  • Einset J, Nielsen E, Connolly EL, Bones A, Sparstad T, Winge P, Zhu J-K (2007) Membrane-trafficking RabA4c involved in the effect of glycine betaine on recovery from chilling stress in Arabidopsis. Physiol Plant 130:511–518

    Article  CAS  Google Scholar 

  • Einset J, Winge P, Bones AM, Connolly EL (2008) The Fro2 ferric reductase is required for glycine betaine’s effect on chilling tolerance in Arabidopsis roots. Physiol Plant 134:334–341

    Article  PubMed  Google Scholar 

  • Gao M, Sakamoto A, Miura K, Murata N, Sugiura A, Tao R (2000) Transformation of Japanese persimmon (Diospyros kaki thunb.) with a bacterial gene for choline oxidase. Mol Breed 6:501–510

    Article  CAS  Google Scholar 

  • Giri J (2011) Glycinebetaine and abiotic stress tolerance in plants. Plant Signal Behav 6:1746–1751

    Google Scholar 

  • Goel D, Singh AK, Yadav V, Babbar SB, Murata N, Bansal KC (2011) Transformation of tomato with a bacterial codA gene enhances tolerance to salt and water stresses. J Plant Physiol 168:1286–1294

    Article  PubMed  CAS  Google Scholar 

  • He C, Yang A, Zhang W, Gao Q, Zhang J (2010) Improved salt tolerance of transgenic wheat by introducing betA gene for glycine betaine synthesis. Plant Cell Tiss Org Cult 101:65–78

    Article  CAS  Google Scholar 

  • Heuer B (2003) Influence of exogenous application of proline and glycinebetaine on growth of salt-stressed tomato plants. Plant Sci 165:693–699

    Article  CAS  Google Scholar 

  • Huang J, Hirji R, Adam L, Rozwadowski KL, Hammerlindl JK, Keller WA, Selvaraj G (2000) Genetic engineering of glycinebetaine production toward enhancing stress tolerance in plants: metabolic limitations. Plant Physiol 122:747–756

    Article  PubMed  CAS  Google Scholar 

  • Jones R, Storey R (1981) Betaines. In: Paleg LG, Aspinall D (eds) The physiology and biochemistry of drought resistance in plants. Academic, New York, pp 171–204

  • Kathuria H, Giri J, Nataraja KN, Murata N, Udayakumar M, Tyagi AK (2009) Glycinebetaine-induced water-stress tolerance in codA-expressing transgenic indica rice is associated with up-regulation of several stress responsive genes. Plant Biotechnol J 7:512–526

    Article  PubMed  CAS  Google Scholar 

  • Konrad Z, Bar-Zvi D (2008) Synergism between the chaperone-like activity of the stress regulated Asr1 protein and the osmolyte glycine-betaine. Planta 227:1213–1219

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Dhingra A, Daniell H (2004) Plastid-expressed betaine aldehyde dehydrogenase gene in carrot cultured cells, roots, and leaves confers enhanced salt tolerance. Plant Physiol 136:2843–2854

    Article  PubMed  CAS  Google Scholar 

  • Kwon SY, Jeong YJ, Lee HS, Kim JS, Cho KY, Allen RD, Kwak SS (2002) Enhanced tolerances of transgenic tobacco plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against methyl viologen-mediated oxidative stress. Plant Cell Environ 25:873–882

    Article  Google Scholar 

  • Larher F, Rotival-Garnier N, Lemesle P, Plasman M, Bouchereau A (1996) The glycine betaine inhibitory effect on the osmoinduced proline response of rape leaf discs. Plant Sci 113:21–31

    Article  CAS  Google Scholar 

  • Lim S, Kim Y-H, Kim S-H, Kwon S-Y, Lee H-S, Kim J-S, Cho K-Y, Paek K-Y, Kwak S–S (2007) Enhanced tolerance of transgenic sweetpotato plants that expressing both CuZnSOD and APX in chloroplasts to methyl viologen-mediated oxidative stress and chilling. Mol Breed 19:227–239

    Article  CAS  Google Scholar 

  • Lv S, Yang A, Zhang K, Wang L, Zhang J (2007) Increase of glycinebetaine synthesis improves drought tolerance in cotton. Mol Breed 20:233–248

    Article  CAS  Google Scholar 

  • Mohanty A, Kathuria H, Ferjani A, Sakamoto A, Mohanty P, Murata N, Tyagi A (2002) Transgenics of an elite rice variety pusa basmati 1 harbouring the codA gene are highly tolerant to salt stress. Theor Appl Genet 106:51–57

    PubMed  CAS  Google Scholar 

  • Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Nyyssölä A, Kerovuo J, Kaukinen P, von Weymarn N, Reinikainen T (2000) Extreme halophiles synthesize betaine from glycine by methylation. J Biol Chem 275:22196–22201

    Article  PubMed  Google Scholar 

  • Ohnishi N, Murata N (2006) Glycinebetaine counteracts the inhibitory effects of salt stress on the degradation and synthesis of d1 protein during photoinhibition in synechococcus sp. Pcc 7942. Plant Physiol 141:758–765

    Article  PubMed  CAS  Google Scholar 

  • Papageorgiou GC, Murata N (1995) The unusually strong stabilizing effects of glycine betaine on the structure and function of the oxygen-evolving photosystem ii complex. Photosynth Res 44:243–252

    Article  CAS  Google Scholar 

  • Park EJ, Jeknic Z, Sakamoto A, DeNoma J, Yuwansiri R, Murata N, Chen TH (2004) Genetic engineering of glycinebetaine synthesis in tomato protects seeds, plants, and flowers from chilling damage. Plant J 40:474–487

    Article  PubMed  CAS  Google Scholar 

  • Park E-J, Jeknić Z, Chen THH, Murata N (2007a) The codA transgene for glycinebetaine synthesis increases the size of flowers and fruits in tomato. Plant Biotechnol J 5:422–430

    Article  PubMed  CAS  Google Scholar 

  • Park EJ, Jeknic Z, Pino MT, Murata N, Chen TH (2007b) Glycinebetaine accumulation is more effective in chloroplasts than in the cytosol for protecting transgenic tomato plants against abiotic stress. Plant Cell Environ 30:994–1005

    Article  PubMed  CAS  Google Scholar 

  • Pollard A, Wyn Jones RG (1979) Enzyme activities in concentrated solutions of glycinebetaine and other solutes. Planta 144:291–298

    Article  CAS  Google Scholar 

  • Prasad KVSK, Sharmila P, Kumar PA, Saradhi PP (2000) Transformation of Brassica juncea (l.) czern with bacterial codA gene enhances its tolerance to salt stress. Mol Breed 6:489–499

    Article  CAS  Google Scholar 

  • Quan R, Shang M, Zhang H, Zhao Y, Zhang J (2004a) Engineering of enhanced glycine betaine synthesis improves drought tolerance in maize. Plant Biotechnol J 2:477–486

    Article  PubMed  CAS  Google Scholar 

  • Quan R, Shang M, Zhang H, Zhao Y, Zhang J (2004b) Improved chilling tolerance by transformation with betA gene for the enhancement of glycinebetaine synthesis in maize. Plant Sci 166:141–149

    Article  CAS  Google Scholar 

  • Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annl Rev Plant Physiol Plant Mol Biol 44:357–384

    Article  CAS  Google Scholar 

  • Rozwadowski KL, Khachatourians GG, Selvaraj G (1991) Choline oxidase, a catabolic enzyme in Arthrobacter pascens, facilitates adaptation to osmotic stress in Escherichia coli. J Bacteriol 173:472–478

    PubMed  CAS  Google Scholar 

  • Sakamoto A, Murata AN (1998) Metabolic engineering of rice leading to biosynthesis of glycinebetaine and tolerance to salt and cold. Plant Mol Biol 38:1011–1019

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Sakamoto A, Valverde R, Alia, Chen TH, Murata N (2000) Tranformation of Arabidopsis with the codA gene for choline oxidase enhances freezing tolerance of plants. Plant J 22:449–453

  • Shirasawa K, Takabe T, Kishitani S (2006) Accumulation of glycinebetaine in rice plants that overexpress choline monooxygenase from spinach and evaluation of their tolerance to abiotic stress. Ann Bot 98:565–571

    Article  PubMed  CAS  Google Scholar 

  • Su J, Hirji R, Zhang L, He C, Selvaraj G, Wu R (2006) Evaluation of the stress-inducible production of choline oxidase in transgenic rice as a strategy for producing the stress-protectant glycine betaine. J Exp Bot 57:1129–1135

    Article  PubMed  CAS  Google Scholar 

  • Sulpice R, Gibon Y, Bouchereau A, Larher F (1998) Exogenously supplied glycine betaine in spinach and rapeseed leaf discs: compatibility or non-compatibility? Plant Cell Environ 21:1285–1292

    Article  CAS  Google Scholar 

  • Tang L, Kwon S-Y, Kim S-H, Kim J-S, Choi J, Cho K, Sung C, Kwak S-S, Lee H-S (2006) Enhanced tolerance of transgenic potato plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against oxidative stress and high temperature. Plant Cell Rep 25:1380–1386

    Article  PubMed  CAS  Google Scholar 

  • Waditee R, Bhuiyan MNH, Rai V, Aoki K, Tanaka Y, Hibino T, Suzuki S, Takano J, Jagendorf AT, Takabe T, Takabe T (2005) Genes for direct methylation of glycine provide high levels of glycinebetaine and abiotic-stress tolerance in Synechococcus and Arabidopsis. Proc Natl Acad Sci USA 102:1318–1323

    Article  PubMed  CAS  Google Scholar 

  • Wang GP, Li F, Zhang J, Zhao MR, Hui Z, Wang W (2010) Overaccumulation of glycine betaine enhances tolerance of the photosynthetic apparatus to drought and heat stress in wheat. Photosynthesis 48:30–41

    Article  CAS  Google Scholar 

  • Wei A, He C, Li B, Li N, Zhang J (2011) The pyramid of transgenes TsVP and BetA effectively enhances the drought tolerance of maize plants. Plant Biotechnol J 9:216–229

    Article  PubMed  CAS  Google Scholar 

  • Yang X, Wen X, Gong H, Lu Q, Yang Z, Tang Y, Liang Z, Lu C (2007) Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants. Planta 225:719–733

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Dong H, L i W, Sun Y, Chen S, Kong X (2009) Increased glycine betaine synthesis and salinity tolerance in AhCMO transgenic cotton lines. Mol Breed 23:289–298

    Article  CAS  Google Scholar 

  • Zhang N, Si H-J, Wen G, Du H-H, Liu B-L, Wang D (2011) Enhanced drought and salinity tolerance in transgenic potato plants with a BADH gene from spinach. Plant Biotechnol Rep 5:71–77

    Article  Google Scholar 

  • Zhou S-F, Chen X-Y, Xue X-N, Zhang X-G, Li Y-X (2007) Physiological and growth responses of tomato progenies harboring the betaine aldehyde dehydrogenase gene to salt stress. J Integ Plant Biol 49:628–637

    Article  CAS  Google Scholar 

  • Zhou S, Chen X, Zhang X, Li Y (2008) Improved salt tolerance in tobacco plants by co-transformation of a betaine synthesis gene BADH and a vacuolar antiporter gene SeNHX1. Biotechnol Lett 30:369–376

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

This study was supported by a grant from the Next-Generation Biogreen 21 program (PJ008103), the Rural Development Administration (RDA), Republic of Korea. It is declared that there is no conflict of interest among the authors of this manuscript.

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Correspondence to Suk-Yoon Kwon.

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Ahmad, R., Lim, C.J. & Kwon, SY. Glycine betaine: a versatile compound with great potential for gene pyramiding to improve crop plant performance against environmental stresses. Plant Biotechnol Rep 7, 49–57 (2013). https://doi.org/10.1007/s11816-012-0266-8

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