Skip to main content

Glycinebetaine-Mediated Abiotic Oxidative-Stress Tolerance in Plants: Physiological and Biochemical Mechanisms

  • Chapter
  • First Online:
Stress Signaling in Plants: Genomics and Proteomics Perspective, Volume 2

Abstract

Plants face many stressful conditions during their lifetimes and because of their sessile nature they have to adapt to these conditions in order to survive. One unfortunate and unavoidable consequence of all major biotic and abiotic stresses is the overproduction of reactive oxygen species (ROS). ROS are highly reactive and toxic chemical entities and can cause serious damage to cellular proteins, lipids, carbohydrates and DNA, leading to irreparable metabolic dysfunction and cell death. Plant cells and their organelles, particularly the chloroplasts, mitochondria and peroxisomes have antioxidant defence systems, composed of enzymatic and non-enzymatic components, to counter the deleterious effects of ROS and/or to perform signalling functions. It is an established fact that the timely induction of antioxidant defences is a key to protection of plant cells from oxidative damage due to stress. Enzymatic antioxidants include superoxide dismutase, catalase, peroxidases and glutathione reductase, while the major non-enzymatic antioxidants are compatible osmolytes (glycinebetaine, GB; and proline), ascorbic acid, reduced glutathione, α-tocopherol, amino acids and polyphenols. Stimulated biosynthesis and accumulation of low molecular weight compatible osmolytes is one of the most effective mechanisms evolved by plants to maintain their cellular integrity and ensure survival when exposed to multiple abiotic stresses. Glycinebetaine, an N-trimethyl derivative of glycine and a quaternary ammonium compound, is one of the most studied and efficient compatible solutes. Due to its unique structural features, it interacts both with the hydrophobic and hydrophilic domains of macromolecules, including enzymes and proteins. GB has been reported to protect plants from the antagonistic effects of a range of abiotic stresses, by maintaining the water balance between plant cells and environment, osmotic adjustment, protecting the thylakoid membrane system, protein stabilization, photosystem and photosynthetic electron transport chain protection and by modulating ROS detoxification. In recent years, GB has attained unprecedented attention due to its multifunctional roles in plants under stressful conditions. In this chapter, we summarize our understanding of ROS formation under abiotic stress and GB biosynthesis and accumulation, as an adaptive mechanism, with particular emphasis on the new insights into the biochemical and molecular mechanisms involved in GB-mediated abiotic oxidative stress tolerance in plants.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 139.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 179.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abogadallah GM (2010) Antioxidative defence under salt stress. Plant Signal Behav 5:369–375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adams W, Muller O, Cohu C, Demmig-Adams B (2013) May photoinhibition be a consequence, rather than a cause, of limited plant productivity? Photosynth Res 117:31–44

    Article  CAS  PubMed  Google Scholar 

  • Ahmad P, Jaleel CA, Salem MA, Nabi G (2009) Generation of ROS and non-enzymatic antioxidants during abiotic stress in plants. Bot Res Int 2:11–20

    CAS  Google Scholar 

  • Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010a) Roles of enzymatic and non-enzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 30:161–175

    Article  CAS  PubMed  Google Scholar 

  • Ahmad R, Kim YH, Kim MD, Kwon SY, Cho K, Lee HS, Kwak SS (2010b) 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  CAS  PubMed  Google Scholar 

  • Ali S, Chaudhary A, Rizwan M, Anwar HT, Adrees M, Farid M, Irshad MK, Hayat T, Anjum SA (2015) Alleviation of chromium toxicity by glycinebetaine is related to elevated antioxidant enzymes and suppressed chromium uptake and oxidative stress in wheat (Triticum aestivum L.). Environ Sci Pollut Res 22:10669–10678

    Article  CAS  Google Scholar 

  • Allakhverdiev SI, Hayashi H, Nishiyama Y, Ivanov AG, Aliev JA, Klimov VV, Murata N, Carpentier R (2003) Glycinebetaine protects the D1/D2/Cytb559 complex of photosystem II against photo-induced and heat-induced inactivation. J Plant Physiol 160:41–49

    Article  CAS  PubMed  Google Scholar 

  • Allakhverdiev SI, Los DA, Mohanty P, Nishiyama Y, Murata N (2007) Glycinebetaine alleviates the inhibitory effect of moderate heat stress on the repair of photosystem II during photoinhibition. Biochim Biophys Acta 1767:1363–1371

    Article  CAS  PubMed  Google Scholar 

  • Anjum SA, Saleem MF, Wang LC, Bilal MF, Saeed A (2012) Protective role of glycinebetaine in maize against drought-induced lipid peroxidation by enhancing capacity of antioxidative system. Aust J Crop Sci 6:576–583

    CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Aro E-M, Virgin I, Anderson B (1993) Photoinhibition of photosystem II: inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Atal N, Sardini PP, Mohanty P (1991) Inhibition of the chloroplast photochemical reactions by treatment of wheat seedlings with low concentration of cadmium: analysis of electron transport activities and changes in fluorescence yield. Plant Cell Physiol 32:943–951

    CAS  Google Scholar 

  • Badran EG, Abogadallah GM, Nada RM, Alla MMN (2015) Role of glycine in improving the ionic and ROS homeostasis during NaCl stress in wheat. Protoplasma 252:835–844

    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 

  • Blokhina O, Fagerstedt K (2006) Oxidative stress and antioxidant defenses in plants. In: Singh KK (ed) Oxidative stress, disease and cancer. Imperial College Press, London, pp 151–199

    Chapter  Google Scholar 

  • Breitkreuz KE, Shelp BJ, Fischer WN, Schwacke R, Rentsch D (1999) Identification and characterization of GABA, proline and quaternary ammonium compound transporters from Arabidopsis thaliana. FEBS Lett 450:280–284

    Article  CAS  PubMed  Google Scholar 

  • Cabello JV, Lodeyro AF, Zurbriggen MD (2014) Novel perspectives for the engineering of abiotic stress tolerance in plants. Curr Opin Biotechnol 26:62–70

    Article  CAS  PubMed  Google Scholar 

  • Cao F, Ibrahim W, Cai Y, Wu F (2013) Alleviating effects of exogenous glutathione, glyicinebetaine, brassionsteroids and salicylic acid on cadmium toxicity in rice seedlings (Oryza sativa). Agrotechnology 2:107

    Google Scholar 

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

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Corpas FJ, Barroso JB, del Río LA (2001) Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends Plant Sci 6:145–150

    Article  CAS  PubMed  Google Scholar 

  • Cruz FJR, Castro GLS, Silva Junior DD, Festucci-Buselli RA, Pinheiro HA (2013) Exogenous glycinebetaine modulates ascorbate peroxidase and catalase activities and prevent lipid peroxidation in mild water-stressed Carapa guianensis plants. Photosynthetica 51:102–108

    Article  CAS  Google Scholar 

  • Das P, Nutan KK, Singla-Pareek SL, Pareek A (2015) Oxidative environment and redox homeostasis in plants: dissecting out significant contribution of major cellular organelles. Front Environ Sci 2:70

    Article  Google Scholar 

  • de Zwart FJ, Slow S, Payne RJ, Lever M, George PM, Gerrard JA, Chambers ST (2003) Glycine betaine and glycine betaine analogues in common foods. Food Chem 83:197–204

    Article  CAS  Google Scholar 

  • del Río LA, Corpas FJ, Sandalio LM, Palma JM, Gomez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53:1255–1272

    Article  PubMed  Google Scholar 

  • del Río LA, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141:330–335

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Desingh R, Kanagaraj G (2007) Influence of salinity stress on photosynthesis and antioxidative systems in two cotton varieties. Gen Appl Plant Physiol 33:221–234

    CAS  Google Scholar 

  • Di H, Tian Y, Zu H, Meng X, Zeng X, Wang Z (2015) Enhanced salinity tolerance in transgenic maize plants expressing a BADH gene from Atriplex micrantha. Euphytica 2015:1515

    Google Scholar 

  • Doyle SM, Diamond M, McCabe PF (2010) Chloroplast and reactive oxygen species involvement in apoptotic-like programmed cell death in Arabidopsis suspension cultures. J Exp Bot 61:473–482

    Article  CAS  PubMed  Google Scholar 

  • Duman F, Aksoy A, Aydin Z, Temizgul R (2011) Effects of exogenous glycinebetaine and trehalose on cadmium accumulation and biological responses of an aquatic plant (Lemna gibba L.). Water Air Soil Pollut 217:545–556

    Article  CAS  Google Scholar 

  • Fan W, Zhang M, Zhang H, Zhang P (2012) Improved tolerance to various abiotic stresses in transgenic sweet potato (Ipomoea batatas) expressing spinach betaine aldehyde dehydrogenase. PLoS One 7:e37344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farooq M, Aziz T, Hussain M, Rehman H, Jabran K, Khan MB (2008a) Glycinebetaine improves chilling tolerance in hybrid maize. J Agron Crop Sci 194:152–160

    Article  CAS  Google Scholar 

  • Farooq M, Basra S, Wahid A, Cheema Z, Cheema M, Khaliq A (2008b) Physiological role of exogenously applied glycinebetaine to improve drought tolerance in fine grain aromatic rice (Oryza sativa L.). J Agron Crop Sci 194:325–333

    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 

  • Gadallah MAA (1999) Effects of proline and glycinebetaine on Vicia faba responses to salt stress. Biol Plant 42:249–257

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics 2014:1–18

    Article  CAS  Google Scholar 

  • Hao F, Wang X, Chen J (2006) Involvement of plasma-membrane NADPH oxidase in nickel-induced oxidative stress in roots of wheat seedlings. Plant Sci 170:151–158

    Article  CAS  Google Scholar 

  • Hasanuzzaman M, Alam MM, Rahman A, Hasanuzzaman M, Nahar K, Fujita M (2014) Exogenous proline and glycinebetaine mediated upregulation of antioxidant defence and glyoxalase systems provides better protection against salt-induced oxidative stress in two rice (Oryza sativa L.) varieties. BioMed Res Int 2014:1–17

    Google Scholar 

  • Hassine AB, Ghanem ME, Bouzid S, Lutts S (2008) An inland and a coastal population of the Mediterranean xerohalophyte species Atriplex halimus L. differ in their ability to accumulate proline and glycinebetaine in response to salinity and water stress. J Exp Bot 59:1315–1326

    Article  PubMed  CAS  Google Scholar 

  • Hattori T, Mitsuya S, Fujiwara T, Jagendorf AT, Takabe T (2009) Tissue specificity of glycinebetaine synthesis in barley. Plant Sci 176:112–118

    Article  CAS  Google Scholar 

  • Hernández JA, Corpas FJ, Gómez M, del Río LA, Sevilla F (1993) Salt-induced oxidative stress mediated by activated oxygen species in pea leaf mitochondria. Physiol Plant 89:103–110

    Article  Google Scholar 

  • Hernández JA, Ferrer MA, Jiménez A, Barceló AR, Sevilla F (2001) Antioxidant systems and O2 •−/H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiol 127:817–831

    Article  PubMed  PubMed Central  Google Scholar 

  • Heyno E, Mary V, Schopfer P, Krieger-Liszkay A (2011) Oxygen activation at the plasma membrane: relation between superoxide and hydroxyl radical production by isolated membranes. Planta 234:35–45

    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

    Google Scholar 

  • Hibino T, Meng YL, Kawamitsu Y, Uehara N, Matsuda N, Tanaka Y, Ishikawa H, Baba S, Takabe T, Wada K, Ishii 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

    Google Scholar 

  • Higuchi T (2006) Look back over the studies of lignin biochemistry. J Wood Sci 52:2–8

    Article  CAS  Google Scholar 

  • Hoque MA, Banu MNA, Okuma E, Amako K, Nakamura Y, Shimoishi Y, Murata Y (2007) Exogenous proline and glycinebetaine increase NaCl-induced ascorbate-glutathione cycle enzyme activities, and proline improves salt tolerance more than glycinebetaine in tobacco Bright Yellow-2 suspension-cultured cells. J Plant Physiol 164:1457–1468

    Article  CAS  PubMed  Google Scholar 

  • Hoque MA, Banu MNA, Nakamura Y, Shimoishi Y, Murata Y (2008) Proline and glycinebetaine enhance antioxidant defence and methylglyoxal detoxification systems and reduce NaCl-induced damage in cultured tobacco cells. J Plant Physiol 165:813–824

    Article  CAS  PubMed  Google Scholar 

  • Hossain MA, Hasanuzzaman M, Fujita M (2010) Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress. Physiol Mol Biol Plant 16:259–272

    Article  CAS  Google Scholar 

  • Hossain MA, Hasanuzzaman M, Fujita M (2011a) Coordinate induction of antioxidant defense and glyoxalase system by exogenous proline and glycinebetaine is correlated with salt tolerance in mung bean. Front Agric China 5:1–14

    Article  Google Scholar 

  • Hossain MA, Teixeira da Silva JA, Fujita M (2011b) Glyoxalase system and reactive oxygen species detoxification system in plant abiotic stress response and tolerance: an intimate relationship. In: Shanker AK, Venkateswarlu B (eds) Abiotic Stress/Book 1. INTECH Open Access Publisher, Rijeka, pp 235–266

    Google Scholar 

  • Hossain MA, Mostofa MG, Burritt DJ, Fujita M (2014) Modulation of reactive oxygen species and methylglyoxal detoxification systems by exogenous glycinebetaine and proline improves drought tolerance in mustard (Brassica juncea L.). Int J Plant Biol Res 2:2014

    Google Scholar 

  • Hossain MA, Bhattacharjee S, Armin S-M, Qian P, Xin W, Li H-Y, Burritt DJ, Fujita M, Tran L-SP (2015) Hydrogen peroxide-priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci 6:420

    PubMed  PubMed Central  Google Scholar 

  • Hu L, Hu T, Zhang X, Pang H, Fu J (2012) Exogenous glycinebetaine ameliorates the adverse effect of salt stress on perennial ryegrass. J Am Soc Hort Sci 137:38–46

    CAS  Google Scholar 

  • Islam MM, Hoque MA, Okuma E, Banu MNA, Shimoishi Y, Nakamura Y, Murata Y (2009a) Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J Plant Physiol 166:1587–1597

    Article  CAS  PubMed  Google Scholar 

  • Islam MM, Hoque MA, Okuma E, Jannat R, Banu MNA, Jahan MS, Nakamura Y, Murata Y (2009b) Proline and glycinebetaine confer cadmium tolerance on tobacco Bright Yellow-2 cells by increasing ascorbate-glutathione cycle enzyme activities. Biosci Biotechnol Biochem 73:2320–2323

    Article  CAS  PubMed  Google Scholar 

  • Ismail A, Takeda S, Nick P (2014) Life and death under salt stress: same players, different timing? J Exp Bot 65:2963–2979

    Article  CAS  PubMed  Google Scholar 

  • Jewell MC, Campbell BC, Godwin ID (2010) Transgenic plants for abiotic stress resistance. In: Kole C, Michler C, Abbott AG, Hall TC (eds) Transgenic crop plants. Springer, Berlin, pp 67–132

    Chapter  Google Scholar 

  • Juszczuk IM, Wagner AM, Rychter AM (2001) Regulation of alternative oxidase activity during phosphate deficiency in bean roots (Phaseolus vulgaris). Physiol Plant 113:185–192

    Article  CAS  PubMed  Google Scholar 

  • Karabudak T, Bor M, Özdemir F, Türkan İ (2014) Glycinebetaine protects tomato (Solanum lycopersicum) plants at low temperature by inducing fatty acid desaturase7 and lipoxygenase gene expression. Mol Biol Rep 41:1401–1410

    Article  CAS  PubMed  Google Scholar 

  • Karuppanapandian T, Moon JC, Kim C, Manoharan K, Kim W (2011) Reactive oxygen species in plants: their generation, signal transduction, and scavenging mechanisms. Aust J Crop Sci 5:709–725

    Google Scholar 

  • Kathuria H, Giri J, Nataraja KN, Murata N, Udayakumar M, Tyaqi 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  CAS  PubMed  Google Scholar 

  • Kaushal N, Gupta K, Bhandhari K, Kumar S, Thakur P, Nayyar H (2011) Proline induces heat tolerance in chickpea (Cicer arietinum L.) plants by protecting vital enzymes of carbon and antioxidative metabolism. Physiol Mol Biol Plant 17:203–213

    Article  CAS  Google Scholar 

  • Khan MS, Yu X, Kikuchi A, Asahina M, Watanabe K (2009) Genetic engineering of glycine betaine biosynthesis to enhance abiotic stress tolerance in plants. Plant Biotechnol 26:125–134

    Article  CAS  Google Scholar 

  • Khanna-Chopra R (2011) Leaf senescence and abiotic stresses share reactive oxygen species mediated chloroplast degradation. Protoplasma 249:469–481

    Article  PubMed  CAS  Google Scholar 

  • Khare T, Kumar V, Kishor PBK (2015) Na+ and Cl ions show additive effects under NaCl stress on induction of oxidative stress and the responsive antioxidative defense in rice. Protoplasma 252:1149–1165

    Article  CAS  PubMed  Google Scholar 

  • Kim K, Portis J (2004) Oxygen-dependent H2O2 production by Rubisco. FEBS Lett 57:124–128

    Article  CAS  Google Scholar 

  • Kim MJ, Ciani S, Schachtman DP (2010) A peroxidase contributes to ROS production during Arabidopsis root response to potassium deficiency. Mol Plant 3:420–427

    Article  CAS  PubMed  Google Scholar 

  • Kishitani S, Watanabe K, Yasuda S, Arakawa K, Takabe T (1994) Accumulation of glycinebetaine during cold acclimation and freezing tolerance in leaves of winter and spring barley plants. Plant Cell Environ 17:89–95

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Krishnamurthy A, Rathinasabapathi B (2013) Oxidative stress tolerance in plants: novel interplay between auxin and reactive oxygen species signaling. Plant Signal Behav 8:e25761

    Article  PubMed Central  CAS  Google Scholar 

  • Kumar V, Khare T (2015) Individual and additive effects of Na+ and Cl ions on rice under salinity stress. Arch Agron Soil Sci 61:381–395

    Article  CAS  Google Scholar 

  • Kurepin LV, Ivanov AG, Zaman M, Pharis RP, Allakhverdiev SI, Hurry V, Hüner NPA (2015) Stress-related hormones and glycinebetaine interplay in protection of photosynthesis under abiotic stress conditions. Photosynth Res 126(2):221–235. doi:10.1007/s11120-015-0125-x

    Article  CAS  PubMed  Google Scholar 

  • Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JDG, Schroeder JI (2003) NADPH oxidase AtrbohD andAtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ladyman JAR, Hitz WD, Hanson AD (1980) Translocation and metabolism of glycinebetaine in barley plants in relation to water stress. Planta 150:191–196

    Article  CAS  PubMed  Google Scholar 

  • Ladyman JAR, Ditz KM, Grumet R, Hanson AD (1983) Genetic variation for glycinebetaine accumulation by cultivated and wild barley in relation to water stress. Crop Sci 23:465–469

    Article  CAS  Google Scholar 

  • Li M, Li Z, Li S, Guo S, Meng Q, Li G, Yang X (2014a) Genetic engineering of glycinebetaine biosynthesis reduces heat-enhanced photoinhibition by enhancing antioxidative defense and alleviating lipid peroxidation in tomato. Plant Mol Biol Rep 32:42–51

    Article  CAS  Google Scholar 

  • Li H, Wang ZX, Ke Q, Ji CY, Jeong JC, Lee HS, Lim YP, Xu B, Deng XP, Kwak SS (2014b) Overexpression of codA gene confers enhanced tolerance to abiotic stresses in alfalfa. Plant Physiol Biochem 85:31–40

    Article  CAS  PubMed  Google Scholar 

  • Liszkay A, van der Zalm E, Schopfer P (2004) Production of reactive oxygen intermediates (O2 •−, H2O2, and OH) by maize roots and their role in wall loosening and elongation growth. Plant Physiol 136:3114–3123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lou Y, Yang Y, Hy L, Liu H, Xu Q (2015) Exogenous glycinebetaine alleviates the detrimental effect of Cd stress on perennial ryegrass. Ecotoxicology 24:1330–1340

    Article  CAS  PubMed  Google Scholar 

  • Low PS (1985) Molecular basis of the biological compatibility of nature’s osmolytes. In: Gilles R, Gilles-Baillien M (eds) Transport processes, iono- and osmoregulation. Springer, Berlin, pp 469–477

    Chapter  Google Scholar 

  • Makela P, Peltonen-Sainio P, Jokinen K, Pehu E, Setala H, Hinkkanen R, Somersalo S (1996) Uptake and translocation of foliar-applied glycinebetaine in crop plants. Plant Sci 121:221–230

    Article  Google Scholar 

  • Malusa E, Laurenti E, Juszczuk I, Ferrari RP, Rychter AM (2002) Free radical production in roots of Phaseolus vulgaris subjected to phosphate deficiency stress. Plant Physiol Biochem 40:963–967

    Article  CAS  Google Scholar 

  • Martinez JL, Montillet E, Bresson E, Agnel JP, Dai GH, Daniel JF, Geiger JP (1998) Apoplastic peroxidase generates superoxide anions in cells of cotton cotyledons undergoing the hypersensitive reaction to Xanthomonas campestris pv. malvacearum race 18. Mol. Plant Microbe Interact 11:1038–1047

    Article  CAS  Google Scholar 

  • McCue KF, Hanson AD (1990) Drought and salt tolerance: towards understanding and application. Trends Biotechnol 8:358–362

    Article  CAS  Google Scholar 

  • McDonnell E, Jones RGW (1988) Glycinebetaine biosynthesis and accumulation in unstressed and salt-stressed wheat. J Exp Bot 39:421–430

    Article  CAS  Google Scholar 

  • McNeil SD, Nuccio ML, Ziemak MJ, Hanson AD (2001) Enhanced synthesis of choline and glycinebetaine in transgenic tobacco plants that overexpress phosphoethanolamine N-methyltransferase. Proc Natl Acad Sci U S A 98:10001–10005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meloni DA, Gulotta MR, Martinez CA, Oliva MA (2004) The effects of salt stress on growth, nitrate reduction and proline and glycinebetaine accumulation in Prosopis alba. Braz J Plant Physiol 16:39–46

    Article  CAS  Google Scholar 

  • Mickelbart MV, Peel G, Joly RJ, Rhodes D, Ejeta G, Goldsbrough PB (2003) Development and characterization of near-isogenic lines of sorghum segregating for glycinebetaine accumulation. Physiol Plant 118:253–261

    Article  CAS  Google Scholar 

  • Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2:ra45

    Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309

    Article  CAS  PubMed  Google Scholar 

  • Mittova V, Tal M, Volokita M, Guy M (2003) Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ 26:845–856

    Article  CAS  PubMed  Google Scholar 

  • Mohanty N, Mohanty P (1988) Cation effects on primary processes of photosynthesis. In: Singh R, Sawheny SK (eds) Advances in frontier areas of plant biochemistry. Prentice-Hall, Delhi, pp 1–18

    Google Scholar 

  • Molla MR, Ali MR, Hasanuzzaman M, Al-Mamun MH, Ahmed A, Nazim-ud-Dowla MAN, Rohman MM (2014) Exogenousproline and betaine-induced upregulation of glutathione transferase and glyoxalase I in lentil (Lens culinaris) under drought stress. Not Bot Horti Agrobo 42:73–80

    CAS  Google Scholar 

  • Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481

    Article  PubMed  CAS  Google Scholar 

  • Mostofa MG, Hossain MA, Fujita M, Tran LS (2015a) Trehalose pretreatment reduces copper-induced oxidative damage and improves resistance to copper toxicity in rice (Oryza sativa L.) seedlings. Sci Rep 5:11433

    Google Scholar 

  • Mostofa MG, Hossain MA, Fujita M (2015a) Trehalose pretreatment induces salt tolerance in rice (Oryza sativa L.) seedlings: oxidative damage and co-induction of antioxidant defense and glyoxalase systems. Protoplasma 252:461–475

    Article  CAS  PubMed  Google Scholar 

  • Murata N, Mohanty PS, Hayashi H, Papageorgiou GC (1992) Glycinebetaine stabilizes the association of extrinsic proteins with the photosynthetic oxygen-evolving complex. FEBS Lett 296:187–189

    Article  CAS  PubMed  Google Scholar 

  • Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421

    Article  CAS  PubMed  Google Scholar 

  • Nawaz K, Ashraf M (2010) Exogenous application of glycinebetaine modulates activities of antioxidants in maize plants subjected to salt stress. J Agron Crop Sci 196:28–37

    Article  CAS  Google Scholar 

  • Noctor G, De Paepe R, Foyer CH (2007) Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci 12:125–134

    Article  CAS  PubMed  Google Scholar 

  • Nouet C, Motte P, Hanikenne M (2011) Chloroplastic and mitochondrial metal homeostasis. Trends Plant Sci 16:395–404

    Article  CAS  PubMed  Google Scholar 

  • Nuccio ML, Russell BL, Nolte KD, Rathinasabapathi B, Gage DA, Hanson AD (1998) The endogenous choline supply limits glycinebetaine synthesis in transgenic tobacco expressing choline monooxygenase. Plant J 16:487–496

    Article  CAS  PubMed  Google Scholar 

  • O’Brien JA, Daudi A, Butt VS, Bolwell GP (2012) Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 236:765–779

    Article  PubMed  CAS  Google Scholar 

  • Orozco-Cardenas ML, Narvaez-Vasquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179–191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pang CH, Wang BS (2008) Oxidative stress and salt tolerance in plants. In: Lüttge U, Beyschlag W, Murata J (eds) Progress in Botany, vol 69. Springer, Berlin, pp 231–245

    Chapter  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Papageorgiou GC, Fujimura Y, Murata N (1985) On the mechanism of betaine protection of photosynthetic structures in high salt environment. In: Current research in photosynthesis. Proceedings of the 8th congress of photosynthesis research, Stockholm, pp 957–960

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Park EJ, Jeknic Z, Chen THH (2006) Exogenous application of glycinebetaine increases chilling tolerance in tomato plants. Plant Cell Physiol 47:706–714

    Article  PubMed  CAS  Google Scholar 

  • Park EJ, Jeknic Z, Pino MT, Murata N, Chen THH (2007) 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  CAS  PubMed  Google Scholar 

  • Petrov V, Hille J, Mueller-Roeber B, Gechev TS (2015) ROS-mediated abiotic stress-induced programmed cell death in plants. Front Plant Sci 6:69

    Article  PubMed  PubMed Central  Google Scholar 

  • Prasad TK, Anderson MD, Martin BA, Stewart CR (1994a) Evidence for chilling- induced oxidative stress in maize seedlings and a regulatory role for hydrogen-peroxide. Plant Cell 6:65–74

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prasad TK, Anderson MD, Stewart CR (1994b) Acclimation, hydrogen-peroxide, and abscisic-acid protect mitochondria against irreversible chilling injury in maize seedlings. Plant Physiol 105:619–627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Purvis AC, Shewfelt RL, Gegogeine JW (1995) Superoxide production by mitochondria isolated from green bell pepper fruit. Physiol Plant 94:743–749

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Quartacci MF, Cosi E, Navari-Izzo F (2001) Lipids and NADPH-dependent superoxide production in plasma membrane vesicles from roots of wheat grown under copper deficiency or excess. J Exp Bot 52:77–84

    Article  CAS  PubMed  Google Scholar 

  • Qureshi MI, Abdin MZ, Ahmad J, Iqbal M (2013) Effect of long-term salinity on cellular antioxidants, compatible solute and fatty acid profile of sweet annie (Artemisia annua L.). Phytochemistry 95:215–223

    Google Scholar 

  • Rajashekar CB, Zhou H, Marcum KB, Prakash O (1999) Glycinebetaine accumulation and induction of cold tolerance in strawberry (Fragaria × ananassa Duch.) plants. Plant Sci 148:175–183

    Article  CAS  Google Scholar 

  • Rathinasbapathi B, Burnet M, Russell BL, Gage DA, Liao PC, Nye GJ, Scott P, Golbeck JH, Hanson AD (1997) Choline monooxygenase, an unusual iron-sulfur enzyme catalyzing the first step of glycinebetaine synthesis in plants: prosthetic group characterization and cDNA cloning. Proc Natl Acad Sci U S A 94:3454–3458

    Article  Google Scholar 

  • Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol 141:357–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Rodríguez AA, Córdoba AR, Ortega L, Taleisnik E (2004) Decreased reactive oxygen species concentration in the elongation zone contributes to the reduction in maize leaf growth under salinity. J Exp Bot 55:1383–1390

    Article  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  CAS  PubMed  Google Scholar 

  • Sakamoto A, Murata N (2002) The role of glycinebetaine in the protection of plants from stress: clue from transgenic plants. Plant Cell Environ 25:163–171

    Article  CAS  PubMed  Google Scholar 

  • Sanda S, Yoshida K, Kuwano M, Kawamura T, Munekage YN, Akashi K, Yokota A (2011) Responses of the photosynthetic electron transport system to excess light energy caused by water deficit in wild watermelon. Physiol Plant 142:247–264

    Article  CAS  PubMed  Google Scholar 

  • Sarwas MKS, Ullah I, Rahman MU, Ashraf MY, Zafar Y (2006) Glycinebetaine accumulation and its relation to yield and yield components in cotton genotypes grown under water deficit conditions. Pak J Bot 38:1449–1456

    Google Scholar 

  • Schopfer P (2001) Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. Plant J 28:679–688

    Article  CAS  PubMed  Google Scholar 

  • Schwacke R, Grallath S, Breitkreuz KE, Stransky E, Stransky H, Frommer WB, Rentsch D (1999) LeProT1, a transporter for proline, glycinebetaine, and gamma-amino butyric acid in tomato pollen. Plant Cell 11:377–392

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schwarzlander M, Fricker MD, Sweetlove LJ (2009) Monitoring the in vivo redox state of plant mitochondria: effect of respiratory inhibitors, abiotic stress and assessment of recovery from oxidative challenge. Biochim Biophys Acta 1787:468–475

    Article  PubMed  CAS  Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:1–26

    Article  CAS  Google Scholar 

  • Sorwong A, Sakhonwasee S (2015) Foliar application of glycinebetaine mitigates the effect of heat stress in three marigold (Tagetes erecta) cultivars. Hort J 84:161–171

    Article  CAS  Google Scholar 

  • Spiteller G (2003) The relationship between changes in the cell wall, lipid peroxidation, proliferation, senescence and cell death. Physiol Plant 119:5–18

    Article  CAS  Google Scholar 

  • Storey R, Ahmad N, Wyn Jones RG (1977) Taxonomic and ecological aspects of the distribution of glycinebetaine and related compounds in plants. Oecologia 27:319–332

    Article  Google Scholar 

  • Sulpice R, Tsukaya H, Nonaka H, Mustardy L, Chen TH, Murata N (2003) Enhanced formation of flowers in salt-stressed Arabidopsis after genetic engineering of the synthesis of glycine betaine. Plant J 36:165–176

    Article  CAS  PubMed  Google Scholar 

  • Takahashi S, Murata N (2006) Glycerate-3-phosphate, produced by CO2 fixation in the Calvin cycle, is critical for the synthesis of the D1 protein of photosystem II. Biochim Biophys Acta 1757:198–205

    Article  CAS  PubMed  Google Scholar 

  • Takhtajan AL (1980) Outline of the classification of flowering plants (magnoliophyta). Bot Rev 46:225–359

    Article  Google Scholar 

  • Tan YF, O’Toole N, Taylor NL, Millar AH (2010) Divalent metal ions in plant mitochondria and their role in interactions with proteins and oxidative stress-induced damage to respiratory function. Plant Physiol 152:747–761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuteja N, Gill SS, Tuteja R (2011) Plant responses to abiotic stresses: shedding light on salt drought cold heavy metal stress. In: Tuteja N, Gill SS, Tuteja R (eds) Omics and plant abiotic stress tolerance. Bentham Science Publishers Ltd., Beijing, pp 39–64

    Google Scholar 

  • Ueda A, Shi W, Sanmiya K, Shono M, Takabe T (2001) Functional analysis of salt-inducible proline transporter of barley roots. Plant Cell Physiol 42:1282–1289

    Article  CAS  PubMed  Google Scholar 

  • Vahisalu T, Puzorjova I, Brosche M, Valk E, Lepiku M, Moldau H, Pechter P, Wang YS, Lindgren O, Salojarvi J, Loog M, Kangasjärvi J, Kollist H (2010) Ozone-triggered rapid stomatal response involves the production of reactive oxygen species, and is controlled by SLAC1 and OST1. Plant J 62:442–453

    Article  CAS  PubMed  Google Scholar 

  • Wang GP, Li F, Zhang J, Zhao MR, Hui Z, Wang W (2010) Over-accumulation of glycinebetaine enhances tolerance of the photosynthetic apparatus to drought and heat stress in wheat. Photosynthetica 48:30–41

    Article  CAS  Google Scholar 

  • Wani SH, Singh NB, Haribhushan A, Mir JI (2013) Compatible solute engineering in plants for abiotic stress tolerance-role of glycinebetaine. Curr Genomics 14:157–165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wise RR (1995) Chilling-enhanced photooxidation—the production, action and study of reactive oxygen species produced during chilling in the light. Photosynth Res 45:79–97

    Article  CAS  PubMed  Google Scholar 

  • Wood KV, Stringham KJ, Smith DL, Volenec JJ, Hendershot KL, Jackson KA, Rich PJ, Yang WJ, Rhodes D (1991) Betaines of alfalfa. Characterization by fast atom bombardment and desorption chemical ionization mass spectrometry. Plant Physiol 96:892–897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada N, Promden W, Yamane K, Tamagake H, Hibino T, Tanaka Y, Takabe T (2009) Preferential accumulation of betaine uncoupled to choline monooxygenase in young leaves of sugar beet—importance of long-distance translocation of betaine under normal and salt-stressed conditions. J Plant Physiol 166:2058–2070

    Article  CAS  PubMed  Google Scholar 

  • Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Yildirim E, Ekinci M, Turan M, Dursun A, Kul R, Parlakova F (2015) Roles of glycinebetaine in mitigating deleterious effect of salt stress on lettuce (Lactuca sativa L.). Arch Agron Soil Sci 61(12):1673–1689. doi:10.1080/03650340.2015.1030611

  • Zhang K, Guo N, Lian L, Wang J, Lv A, Zhang J (2011) Improved salt tolerance and seed cotton yield in cotton (Gossypium hirsutum L.) by transformation with betA gene for glycinebetaine synthesis. Euphytica 181:1–16

    Article  CAS  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The financial support from the Science and Engineering Research Board, Government of India [grant number SR/FT/LS-93/2011] to V.K. as a Young Scientist Project is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mohammad Anwar Hossain .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Kumar, V., Shriram, V., Hoque, T.S., Hasan, M.M., Burritt, D.J., Hossain, M.A. (2017). Glycinebetaine-Mediated Abiotic Oxidative-Stress Tolerance in Plants: Physiological and Biochemical Mechanisms. In: Sarwat, M., Ahmad, A., Abdin, M., Ibrahim, M. (eds) Stress Signaling in Plants: Genomics and Proteomics Perspective, Volume 2. Springer, Cham. https://doi.org/10.1007/978-3-319-42183-4_5

Download citation

Publish with us

Policies and ethics