Skip to main content

Interaction of Glycine Betaine and Plant Hormones: Protection of the Photosynthetic Apparatus During Abiotic Stress

  • Chapter
  • First Online:
Photosynthesis: Structures, Mechanisms, and Applications

Summary

The growth and development of higher plants depends not only upon an active photosynthetic apparatus and adequate water and mineral nutrient supply, but also tight regulation of growth by plant hormones and specific secondary metabolites. Environmental (abiotic) stresses influence plant growth via changes in the metabolism and action of plant hormones, their interactions with secondary metabolites, as well as a reduction in photosynthetic activity. An initial response to abiotic stress often includes an increasing accumulation of two “stress” hormones, abscisic acid (ABA) and salicylic acid (SA). This is followed by an activation of multiple physiological pathways which yield an increase in tolerance to the stress. Also associated with these increases in ABA and SA levels are a reduction in the biosynthesis and/or action of plant “growth” hormones, such as the gibberellins, auxin and cytokinins. The plant’s internal resources are then diverted toward enhancing stress tolerance which is usually associated with diminished photosynthetic productivity. However, some plant varieties (genotypes) are capable of biosynthesising a unique secondary metabolite, glycine betaine (GB). These genotypes exhibit a greater tolerance to abiotic stress, and often have an enhanced growth and yield, relative to varieties which do not accumulate GB. The increased GB accumulation occurs mainly in the chloroplast and is responsible for initiating a network of interactions between the plant’s photosynthetic apparatus, its “stress” and “growth” hormones, and reactive oxygen species. The end result of these GB-induced interactions is the alleviation of abiotic stress effects.

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 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
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

  • Abbas W, Ashraf M, Akram NA. Alleviation of salt-induced adverse effects in eggplant (Solanum melongena L.) by glycinebetaine and sugarbeet extracts. Sci Horticul 2010; 125: 188–95.

    Article  CAS  Google Scholar 

  • Abeles FB, Morgan PW, Saltveit ME. Ethylene in Plant Biology, second edition. Academic Press, New York 1992.

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Agboma PC, Jones MGK, Peltonen-Sainio P, Rita H, Pehu E. Exogenous glycinebetaine enhances grain yield of maize, sorghum and wheat grown under two supplementary watering regimes. J Agron Crop Sci 1997a; 178: 29–37.

    Article  CAS  Google Scholar 

  • Agboma PC, Sinclair TR, Jokinen K, Peltonen-Sainio P, Pehu E. An evaluation of the effect of exogenous glycinebetaine on the growth and yield of soybean: timing of application, watering regimes and cultivars. Field Crop Res 1997b; 54: 51–64.

    Article  Google Scholar 

  • Agboma PC, Peltonen-Sainio P, Hinkkanen R, Pehu E. Effect of foliar application of glycinebetaine on yield components of drought-stressed tobacco plants. Exp Agric 1997c; 33: 345–52.

    Article  CAS  Google Scholar 

  • Aldesuquy HS, Abbas MA, Abo-Hamed SA, Elhakem AH, Alsokari SS. Glycine betaine and salicylic acid induced modification in productivity of two different cultivars of wheat grown under water stress. J Stress Physiol Biochem 2012; 8: 72–89.

    Google Scholar 

  • Ali Q, Ashraf M. Exogenously applied glycinebetaine enhances seed and seed oil quality of maize (Zea mays L.) under water deficit conditions. Environ Exp Bot 2011; 71: 249–59.

    Article  CAS  Google Scholar 

  • Alia, Hayashi H, Sakamoto A, Murata N. Enhancement of the tolerance of Arabidopsis to high temperatures by genetic engineering of the synthesis of glycinebetaine. Plant J 1998; 16: 155–61.

    Article  CAS  PubMed  Google Scholar 

  • Allakhverdiev SI, Feyziev YM, Ahmed A, Hayashi H, Aliev JA, Kimlov VV, Murata N, Carpentier R. Stabilization of oxygen evolution and primary electron transport reactions in photosystem II against heat stress with glycinebetaine and sucrose. J Photochem Photobiol 1996; 34: 149–57.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Allard F, Houde M, Krol M, Ivanov A, Huner NPA, Sarhan F. Betaine improves freezing tolerance in wheat. Plant Cell Physiol 1998; 39: 1194–202.

    Article  CAS  Google Scholar 

  • Anjum SA, Farooq M, Wang LC, Xue LL, Wang SG, Wang L, Zhang S, Chen M. Gas exchange and chlorophyll synthesis of maize cultivars are enhanced by exogenously-applied glycinebetaine under drought conditions. Plant Soil Environ 2011; 57: 326–31.

    CAS  Google Scholar 

  • Arakawa K, Katayama M, Takabe T. Levels of glycinebetaine and glycinebetaine aldehyde dehydrogenase activity in the green leaves, and etiolated leaves and roots of barley. Plant Cell Physiol 1990; 31: 797–803.

    CAS  Google Scholar 

  • Arakawa K, Mizuno K, Kishitani S, Takabe T. Immunological studies of betaine aldehyde dehydrogenase of barley. Plant Cell Physiol 1992; 33: 833–40.

    CAS  Google Scholar 

  • Aro E-M, Virgin I, Anderson B. Photoinhibition of photosystem II: inactivation, protein damage and turnover. Biochim Biophys Acta 1993; 1143: 113–34.

    Article  CAS  PubMed  Google Scholar 

  • Ashraf M, Foolad MR. Roles of glycinebetaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 2007; 59: 206–16.

    Article  CAS  Google Scholar 

  • Ashraf M, Nawaz K, Athar HUR, Raza SH. Growth enhancement in two potential cereal crops, maize and wheat, by exogenous application of glycinebetaine. In: Abdelly C, Ozturk M, Ashraf M, Grignon C, Eds. Biosaline Agriculture and High Salinity Tolerance. Birkhauser Verlag, Switzerland, 2008; pp. 21–35.

    Chapter  Google Scholar 

  • Athar HUR, Ashraf M, Wahid A, Jamil A. Inducing salt tolerance in canola (Brassica napus L.) by exogenous application of glycinebetaine and proline: responses at the initial growth stages. Pakistan J Bot 2009; 41: 1311–9.

    CAS  Google Scholar 

  • Baker NR. Possible role of photosystem II in environmental perturbations of photosynthesis. Physiol Plant 1991; 81: 563–70.

    Article  CAS  Google Scholar 

  • Ballantyne JS, Chamberlin ME. Regulation of cellular amino acid levels. In: Strange K, Ed. Cellular and Molecular Physiology of Cell Volume Regulation. CRC Press, Boca Raton, 1994; pp. 111–22.

    Google Scholar 

  • Bao Y, Zhao R, Li F, Tang W, Han L. Simultaneous expression of Spinacia oleracea chloroplast choline monooxygenase (CMO) and betaine aldehyde dehydrogenase (BADH) genes contribute to dwarfism in transgenic Lolium perenne. Plant Mol Biol Rep 2011; 29: 379–388.

    Article  CAS  Google Scholar 

  • Brouquisse R, Weigel P, Rhodes D, Yocum CF, Hanson AD. Evidence for a ferredoxin-dependent choline monooxygenase from spinach chloroplast stroma. Plant Physiol 1989; 90: 322–329.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burg SP, Thimann KV. The physiology of ethylene formation in apples. Proc Nat Acad Sci USA 1959; 45: 335–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Busheva M, Apostolova E. Influence of saccharides and glycine betaine on freezing of photosystem 2-enriched particles: a chlorophyll fluorescence study. Photosynthetica 1997, 34: 591–4.

    Article  CAS  Google Scholar 

  • Cha-Um S, Supaibulwatana K, Kirdmanee C. Glycinebetaine accumulation, physiological characterizations and growth efficiency in salt-tolerant and salt-sensitive lines of indica rice (Oryza sativa L. ssp. indica) in response to salt stress. J Agron Crop Sci 2007; 193: 157–66.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chen WP, Li PH, Chen THH. Glycinebetaine increases chilling tolerance and reduces chilling-induced lipid peroxidation in Zea mays L. Plant Cell Environ 2000; 23: 609–18.

    Article  CAS  Google Scholar 

  • Ciardi JA, Deikman J, Orzolek MD. Increased ethylene synthesis enhances chilling tolerance in tomato. Physiol Plant 1997; 101: 333–40.

    Article  CAS  Google Scholar 

  • Collins GG, Nie X, Saltveit ME. Heat shock increases chilling tolerance of mung bean hypocotyls tissues. Physiol Plant 1995; 89: 117–24.

    Article  Google Scholar 

  • Coughlan SJ, Heber U. The role of glycinebetaine in the protection of spinach thylakoids against freezing stress. Planta 1982; 156: 62–69.

    Article  CAS  PubMed  Google Scholar 

  • Davies PJ. The Plant Hormones: Their Nature, Occurrence, and Functions. In: Davies PJ, Ed. Plant Hormones: Biosynthesis, Signal Transduction and Action!, 3rd ed. Springer Science+Business Media B.V.: Dordrecht, The Netherlands, 2010; pp. 1–15.

    Chapter  Google Scholar 

  • Dawson RWC, Elliot WH, Jones KM. Data for Biochemical research. II. Clarendon Press, Oxford, 1969; p. 12.

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Demiral T, Turkan I. Does exogenous glycinebetaine affect antioxidative system of rice seedlings under NaCl treatment? J Plant Physiol 2004; 161: 1089–100.

    Article  CAS  PubMed  Google Scholar 

  • Diamant S, Eliahu N, Rosenthal D, Goloubinoff P. Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses. J Biol Chem 2001; 276: 39586–39591.

    Article  CAS  PubMed  Google Scholar 

  • Dodd IC. Hormonal interactions and stomatal responses. J Plant Growth Regul 2003; 22: 32–46.

    Article  CAS  Google Scholar 

  • Dodd IC, Davies WJ. Hormones and the regulation of water balance. In: Davies PJ, Ed. Plant Hormones: Biosynthesis, Signal Transduction and Action! (revised third edition). Springer Dordrecht Heidelberg London New York, 2010; pp. 241–61.

    Google Scholar 

  • Farooq M, Aziz T, Hussain M, Rehman H, Jabran K, Khan MB. Glycinebetaine improves chilling tolerance in hybrid maize. J Agron Crop Sci 2008a; 194: 152–60.

    Article  CAS  Google Scholar 

  • Farooq M, Basra SMA, Wahid A, Cheema ZA, Khalid A. Physiological role of exogenously applied glycinebetaine to improve drought tolerance in fine grain aromatic rice (Oryza sativa L.). J Agron Crop Sci 2008b; 194: 325–33.

    Article  CAS  Google Scholar 

  • Farooq M, Wahid A, Lee D-J, Cheema SA, Aziz T. Comparative time course action of the foliar applied glycinebetaine, salicylic acid, nitrous oxide, brassinosteroids and spermine in improving drought resistance of rice. J Agron Crop Sci 2010; 196: 336–45.

    Article  CAS  Google Scholar 

  • Field RJ. The role of 1-aminocyclopropane-1-carboxylic acid in the control of low temperature induced ethylene production in leaf tissue of Phaseolus vulgaris L. Ann Bot 1984; 54: 61–7.

    Article  CAS  Google Scholar 

  • Franks PJ, Farquhar GD. The effect of exogenous abscisic acid on stomatal development, stomatal mechanics, and leaf gas exchange in Tradescantia virginiana. Plant Physiol 2001; 125: 935–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frederick JR, Alm DM, Hesketh JD. Leaf photosynthetic rates, stomatal resistances, and internal CO2 concentrations of soybean cultivars under drought stress. Photosynthetica 1989; 23: 575–84.

    Google Scholar 

  • Gadallah MAA. Effects of proline and glycinebetaine on Vicia faba responses to salt stress. Biol Plant 1999; 42: 249–57.

    Article  CAS  Google Scholar 

  • Gamble PE, Mullet JE. Inhibition of carotenoid accumulation and abscisic acid biosynthesis in fluridone-treated dark-grown barley. Eur J Biochem 1986; 160: 117–121.

    Article  CAS  PubMed  Google Scholar 

  • Goggin DE, Emery RJN, Kurepin LV, Powles SB. A potential role for endogenous microflora in dormancy release, cytokinin metabolism and the response to fluridone in Lolium rigidum seeds. Ann Bot 2015; 115: 293–301.

    Article  PubMed  Google Scholar 

  • Grote EM, Ejeta G, Rhodes D. Inheritance of glycinebetaine deficiency in sorghum. Crop Sci 1994; 34: 1217–20.

    Article  CAS  Google Scholar 

  • Hansen E. Quantitative study of ethylene production in apple varieties. Plant Physiol 1945; 20: 631–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hattori T, Mitsuya S, Fujiwara T, Jagendorf AT, Takabe T. Tissue specificity of glycinebetaine synthesis in barley. Plant Sci 2009; 176: 112–8.

    Article  CAS  Google Scholar 

  • Hayashi H, Alia, Mustardy L, Deshnium P, Ida M, Murata N. Transformation of Arabidopsis thaliana with the codA gene for choline oxidase: accumulation of glycinebetaine and enhanced tolerance to salt and cold stress. Plant J 1997; 12: 133–42.

    Article  CAS  PubMed  Google Scholar 

  • Hibino T, Waditee R, Araki E, Ishikawa H, Aoki K, Tanaka Y, Takabe T. Functional characterization of choline monooxygenase, an enzyme for betaine synthesis in plants. J Biol Chem 2002; 277: 41352–60.

    Article  CAS  PubMed  Google Scholar 

  • Hitz WD, Ladyman JAR, Hanson AD. Betaine synthesis and accumulation in barley during field water stress. Crop Sci 1982; 22: 47–54.

    Article  CAS  Google Scholar 

  • Holmstrom K-O, Somersalo S, Mandal A, Palva TE, Welin B. Improved tolerance to salinity and low temperature in transgenic tobacco producing glycinebetaine. J Exp Bot 2000; 51: 177–85.

    Article  CAS  PubMed  Google Scholar 

  • Hu LX, Hu T, Zhang XZ, Pang HC, Fu JM. Exogenous glycine betaine ameliorates the adverse effect of salt stress on perennial ryegrass. J Am Soc Hort Sci 2012; 137: 38–46.

    CAS  Google Scholar 

  • Huang J, Hirji R, Adam L, Rozwadowski KL, Hammerlindl JK, Keller WA, Selvaraj G. Genetic engineering of glycinebetaine production toward enhancing stress tolerance in plants: metabolic limitations. Plant Physiol 2000; 122: 747–56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hüner NPA, Maxwell DP, Gray GR, Savitch LV, Krol M, Ivanov AG, Falk S. Sensing environmental change: PSII excitation pressure and redox signalling. Physiol Plant 1996; 98: 358–364.

    Article  Google Scholar 

  • Hüner NPA, Oquist G, Sarhan F. Energy balance and acclimation to light and cold. Trends Plant Sci 1998; 3: 224–230.

    Article  Google Scholar 

  • Hüner NPA, Bode R, Dahal K, Hollis L, Rosso D, Krol M, Ivanov AG. Chloroplast redox imbalance governs phenotypic plasticity: the “grand design of photosynthesis” revisited. Front Plant Sci 2012; 3: 255.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hüner NPA, Dahal K, Kurepin LV, Savitch L, Singh J, Ivanov AG, Kane K, Sarhan F. Potential for increased photosynthetic performance and crop productivity in response to climate change: role of CBFs and gibberellic acid. Front Chem 2014; 2: 18.

    PubMed  PubMed Central  Google Scholar 

  • Hussain M, Malik MA, Farooq M, Ashraf MY, Cheema MA. Improving drought tolerance by exogenous application of glycinebetaine and salicylic acid in sunflower. J Agron Crop Sci 2008; 194: 193–9.

    Article  CAS  Google Scholar 

  • Ibrahim M, Anjum A, Khaliq N, Iqbal M, Athar HUR. Four foliar applications of glycinebetaine did not alleviate adverse effects of slat stress on growth of sunflower. Pakistan J Bot 2006; 38: 1561–70.

    Google Scholar 

  • Ikuta S, Imamura S, Misaki H, Horiuti Y. Purification and characterization of choline oxidase from Arthrobacter globiformis. J Biochem 1977; 82: 1741–9.

    Article  CAS  PubMed  Google Scholar 

  • Iqbal N, Ashraf M, Ashraf MY. Glycinebetaine, an osmolyte of interest to improve water stress tolerance in sunflower (Helianthus annuus L.): water relations and yield. South Afr J Bot 2008; 74: 274–81.

    Article  CAS  Google Scholar 

  • Irigoyen JJ, Emerich DW, Sánchez-Díaz M. Alfalfa leaf senescence induced by drought stress: photosynthesis, hydrogen peroxide metabolism, lipid peroxidation and ethylene evolution. Physiol Plant 1992; 84: 67–72.

    Article  CAS  Google Scholar 

  • Ishitani M, Nakamura T, Han SY, Takabe T. Expression of the betaine aldehyde dehydrogenase gene in barley in response to osmotic stress and abscisic acid. Plant Mol Biol 1995; 27: 307–15.

    Article  CAS  PubMed  Google Scholar 

  • Ivanov AG, Morgan R, Gray GR, Velitchkova MY, Hüner NPA. Temperature/light dependent development of selective resistance to photoinhibition of photosystem I. FEBS Lett 1998; 430: 288–292

    Article  CAS  PubMed  Google Scholar 

  • Ivanov AG, Rosso D, Savitch LV, Stachula P, Rosembert M, Oquist G, Hurry V, Hüner NPA. Implications of alternative electron sinks in increased resistance of PSII and PSI photochemistry to high light stress in cold-acclimated Arabidopsis thaliana. Photosynth Res 2012a; 113:191–206.

    Article  CAS  PubMed  Google Scholar 

  • Ivanov AG, Allakhverdiev SI, Hüner NPA, Murata N. Genetic decrease in fatty acid unsaturation of phosphatidylglycerol increased photoinhibition of photosystem I at low temperature in tobacco leaves. Biochim Biophys Acta 2012b; 1817: 1374–1379.

    Article  CAS  PubMed  Google Scholar 

  • Jagendorf AT, Takabe T. Inducers of glycinebetaine synthesis in barley. Plant Physiol 2001; 127: 1827–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kacperska A. Plant responses to low temperature: signaling pathways involved in plant acclimation. In: Margesin R, Schinner F, Eds. Salicylic Acid: Plant Growth and Development. Springer-Verlag Berlin Heilderberg, Germany, 1999; pp. 79–104.

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kern AJ, Dyer WE. Glycine betaine biosynthesis is induced by salt stress but repressed by auxinic herbicides in Kochia scoparia. J Plant Growth Regul 2004; 23: 9–19.

    Article  CAS  Google Scholar 

  • Kiba T, Kudo T, Kojima M and Sakakibara H. Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. J Exp Bot 2011; 62: 1399–1409.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Korkmaz A, Sirikci R. Improving salinity tolerance of germinating seeds by exogenous application of glycinebetaine in pepper. Seed Sci Tech 2011; 39: 377–88.

    Article  Google Scholar 

  • Kurepin LV, Pharis RP. Light signaling and the phytohormonal regulation of shoot growth. Plant Sci 2014; 229: 280–289.

    Article  CAS  PubMed  Google Scholar 

  • Kurepin LV, Mancell L, Reid DM, Pharis RP, Chinnappa CC. Possible roles for ethylene and gibberellin in the phenotypic plasticity of an alpine population of Stellaria longipes. Botany 2006; 84: 1101–1109.

    CAS  Google Scholar 

  • Kurepin LV, Walton LJ, Reid DM. Interaction of red to far red light ratio and ethylene in regulating stem elongation of Helianthus annuus. Plant Growth Regul 2007; 51: 53–61.

    Article  CAS  Google Scholar 

  • Kurepin LV, Qaderi MM, Back TG, Pharis RP, Reid DM. A rapid effect of applied brassinolide on abscisic acid concentrations in Brassica napus leaf tissue subjected to short-term heat stress. Plant Growth Regul 2008a; 55: 165–7.

    Article  CAS  Google Scholar 

  • Kurepin LV, Emery RJN, Chinnappa CC, Reid DM. Light irradiance differentially regulates endogenous levels of cytokinins and auxin in alpine and prairie genotypes of Stellaria longipes. Physiol Plant 2008b; 134: 624–635.

    Article  CAS  PubMed  Google Scholar 

  • Kurepin LV, Walton LJ, Reid DM, Chinnappa CC. Light regulation of endogenous salicylic acid levels in hypocotyls of Helianthus annuus seedlings. Botany 2010a; 88, 668–74.

    Article  CAS  Google Scholar 

  • Kurepin LV, Walton LJ, Yeung EC, Chinnappa CC, Reid DM. The interaction of light irradiance with ethylene in regulating growth of Helianthus annuus shoot tissues. Plant Growth Regul 2010b; 62: 43–50.

    Article  CAS  Google Scholar 

  • Kurepin LV, Yip WK, Fan R, Yeung EC, Reid DM. The roles and interactions of ethylene with gibberellins in the far-red enriched light-mediated growth of Solanum lycopersicum seedlings. Plant Growth Regul 2010c; 61: 215–22.

    Article  CAS  Google Scholar 

  • Kurepin LV, Walton LJ, Pharis RP, Emery RJN, Reid DM. Interactions of temperature and light quality on phytohormone-mediated elongation of Helianthus annuus hypocotyls. Plant Growth Regul 2011a; 64: 147–54.

    Article  CAS  Google Scholar 

  • Kurepin L, Haslam T, Lopez-Villalobos A, Oinam G, Yeung E. Adventitious root formation in ornamental plants: II. The role of plant growth regulators. Prop Ornam Plants 2011b; 11: 161–171.

    Google Scholar 

  • Kurepin LV, Walton LJ, Yeung EC, Reid DM. The interaction of light irradiance with auxin in regulating growth of Helianthus annuus shoots. Plant Growth Regul 2011c; 65: 255–262.

    Article  CAS  Google Scholar 

  • Kurepin LV, Walton LJ, Hayward A, Emery RJN, Reid DM, Chinnappa CC. Shade light interaction with salicylic acid in regulating growth of sun (alpine) and shade (prairie) ecotypes of Stellaria longipes. Plant Growth Regul 2012a; 68: 1–8.

    Article  CAS  Google Scholar 

  • Kurepin LV, Farrow S, Walton LJ, Emery RJN, Pharis RP, Chinnappa CC. Phenotypic plasticity of sun and shade ecotypes of Stellaria longipes in response to light quality signaling: Cytokinins. Environ Exp Bot 2012b; 84: 25–32.

    Article  Google Scholar 

  • Kurepin LV, Ozga JA, Zaman M, Pharis RP. The physiology of plant hormones in cereal, oilseed and pulse crops. Prairie Soils Crops 2013a; 6: 7–23.

    Google Scholar 

  • Kurepin LV, Dahal KP, Zaman M, Pharis RP. Interplay between environmental signals and endogenous salicylic acid concentration. In: Hayat S, Ahmad A, Alyemini MN, Eds. Salicylic Acid: Plant Growth and Development. Springer Science+Business Media B.V., Dordrecht, The Netherlands, 2013b; pp. 61–82.

    Chapter  Google Scholar 

  • Kurepin LV, Dahal KP, Savitch LV, Singh J, Bode R, Ivanov AG, Hurry V and Hüner NPA. Role of CBFs as integrators of chloroplast redox, phytochrome and plant hormone signaling during cold acclimation. Int J Mol Sci, 2013c; 14: 12729–63.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kurepin LV, Zaman M, Pharis RP. Phytohormonal basis for the plant growth promoting action of naturally occurring biostimulators. J Sci Food Agric 2014; 94: 1715–1722.

    Article  CAS  PubMed  Google Scholar 

  • Kurepin LV, Ivanov AG, Zaman M, Pharis RP, Allakhverdiev SI, Hurry V and Hüner NPA. Stress-related hormones and glycinebetaine interplay in protection of photosynthesis under abiotic stress conditions. Photosynth Res 2015a; 126: 221–235.

    Article  CAS  PubMed  Google Scholar 

  • Kurepin LV, Pharis RP, Emery RJN, Reid DM, Chinnappa CC. Phenotypic plasticity of sun and shade ecotypes of Stellaria longipes in response to light quality signaling, gibberellins and auxin. Plant Physiol Biochem 2015b; 94: 174–180.

    Article  CAS  PubMed  Google Scholar 

  • Kurepin LV, Yeung EC, Reid DM, Pharis RP. Light signaling regulates tulip organ growth and ethylene production in a tissue-specific manner. Inter J Plant Sci 2016; DOI: 10.1086/684947.

    Google Scholar 

  • Landfald B, Strom AR. Choline-glycine betaine pathway confers a high level of osmotic tolerance in Escherichia coli. J Bacteriol 1986; 165: 849–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SH, Reid DM. The role of endogenous ethylene in the expansion of Helianthus annuus leaves. Can J Bot 1997; 78: 501–508.

    Article  Google Scholar 

  • Liu Y, Bolen DW. The peptide backbone plays a dominant role in protein stabilization by naturally occurring osmolytes. Biochemistry 1995; 34: 12884–91.

    Article  CAS  PubMed  Google Scholar 

  • Long SP, Humphries S, Falkowski PG. Photoinhibition of photosystem in nature. Ann Rev Plant Physiol Plant Mol Biol 1994; 45: 633–62.

    Article  CAS  Google Scholar 

  • Lopez CML, Takahashi H, Yamazaki S. Plant-water relations of kidney bean plants treated with NaCl and foliarly applied glycinebetaine. J Agron Crop Sci 2002; 188: 73–80.

    Article  CAS  Google Scholar 

  • Low PS. Molecular basis of the biological compatibility of nature's osmolytes. In: Gilles R, Gilles-Baillien M, Eds. Transport Processes, Iono- and Osmoregulation. Springer-Verlag, Berlin, 1985; pp. 469–77.

    Chapter  Google Scholar 

  • Ma Q-Q, Wang W, Lib Y-H, Lib D-Q, Zou Q. Alleviation of photoinhibition in drought-stressed wheat (Triticum aestivum) by foliar-applied glycinebetaine. J Plant Physiol 2006; 163: 165–75.

    Article  CAS  PubMed  Google Scholar 

  • Ma XL, Wang YJ, Xie SL, Wang C, Wang W. Glycinebetaine application ameliorates negative effects of drought stress in tobacco. Rus J Plant Physiol 2007; 54: 472–9.

    Article  CAS  Google Scholar 

  • Machacckova I, Hanisova A, Krekule J. Levels of ethylene, ACC, MACC, ABA and proline as indicators of cold hardening and frost resistance in winter wheat. Physiol Plant 1989; 76: 603–7.

    Article  Google Scholar 

  • Mahmood T, Ashraf M, Shahbaz M. Does exogenous application of glycinebetaine as a pre-sowing seed treatment improve growth and regulate some key physiological attributes in wheat plants grown under water deficit conditions? Pakistan J Bot 2009; 41: 1291–302.

    CAS  Google Scholar 

  • Makela P, Peltonen-Sainio P, Jokinen K, Pehu E, Setala H, Hinkkanen R, Somersalo S. Uptake and translocation of foliar-applied glycinebetaine in crop plants. Plant Sci 1996a; 121: 221–30.

    Article  Google Scholar 

  • Makela P, Mantila J, Hinkkanen R, Pehu E, Peltonen-Sainio P. Effect of foliar applications of glycinebetaine on stress tolerance, growth, and yield of spring cereals and summer turnip rape in Finland. J Agric Crop Sci 1996b; 176: 223–34.

    Article  CAS  Google Scholar 

  • Makela P, Kleemola J, Jokinen K, Mantila J, Pehu E, Peltonen-Sainio P. Growth response of pea and summer turnip rape to foliar application of glycinebetaine. Acta Agric Scan 1997; 47: 168–75.

    CAS  Google Scholar 

  • Mamedov M, Hayashi H, Murata N. Effects of glycinebetaine and unsaturation of membrane lipids on heat stability of photosynthetic electron-transport and phosphorylation reactions in Synechocystis PCC6803. Biochim Biophys Acta 1993; 1142: 1–5.

    Article  CAS  Google Scholar 

  • McDonnell E, Wyn Jones RG. Glycinebetaine biosynthesis and accumulation in unstressed and salt-stressed wheat. J Exp Bot 1988; 39: 421–30.

    Article  CAS  Google Scholar 

  • McNeil SD, Nuccio ML, Ziemak MJ, Hanson AD. Enhanced synthesis of choline and glycine betaine in transgenic tobacco plants that overexpress phosphoethanolamine N-methyltransferase. Proc Nat Acad Sci USA 2001; 98: 10001–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mickelbart MV, Peel G, Joly RJ, Rhodes D, Ejeta G, Goldsbrough PB. Development and characterization of near-isogenic lines of sorghum segregating for glycinebetaine accumulation. Physiol Plant 2003; 118: 253–61.

    Article  CAS  Google Scholar 

  • Mohanty A, Kathuria H, Ferjani A, Sakamoto A, Mohanty P, Murata N, Tyagi AK. Transgenics of an elite indica rice variety Pusa Basmati 1 harbouring the codA gene are highly tolerant to salt stress. Theor Appl Gen 2002; 106: 51–7.

    Article  CAS  Google Scholar 

  • Morgan PW, Drew MC. Ethylene and plant responses to stress. Physiol Plant 1997; 100: 620–30.

    Article  CAS  Google Scholar 

  • Muchow RC, Sinclair TR, Bennett JM, Hammond LC. Response of leaf growth, leaf nitrogen, and stomatal conductance to water deficits during vegetative growth of field-grown soybean. Crop Sci 1986; 26: 1190–5.

    Article  CAS  Google Scholar 

  • Murata N, Mohanty PS, Hayashi H, Papageorgiou GC. Glycinebetaine stabilizes the association of extrinsic proteins with the photosynthetic oxygen-evolving complex. FEBS Lett 1992; 296: 187–9.

    Article  CAS  PubMed  Google Scholar 

  • Murata N, Allakhverdiev SI, Nishiyama Y. The mechanism of photoinhibition in vivo: Re-evaluation of the roles of catalase, α-tocopherol, non-photochemical quenching, and electron transport. Biochim Biophys Acta 2012; 1817: 1127–1133.

    Article  CAS  PubMed  Google Scholar 

  • Nawaz K, Ashraf M. Improvement in salt tolerance of maize by exogenous application of glycinebetaine: growth and water relations. Pakistan J Bot 2007; 39: 1647–53.

    Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N. A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim. Biophys. Acta 2006; 1757: 742–749.

    Article  CAS  PubMed  Google Scholar 

  • Nomura M, Hibino T, Takabe T, Sugiura T, Yokota A, Miyake H, Takabe T. Transgenically produced glycinebetaine protects ribulose 1,5-bisphosphate carboxylase/oxygenase from inactivation in Synechococcus sp. PCC7942 under salt stress. Plant Cell Physiol 1998; 39: 425–32.

    Article  CAS  Google Scholar 

  • Nuccio ML, Russell BL, Nolte KD, Rathinasabapathi B, Gage DA, Hanson AD. The endogenous choline supply limits glycine betaine synthesis in transgenic tobacco expressing choline monooxygenase. Plant J 1998; 16: 487–96.

    Article  CAS  PubMed  Google Scholar 

  • Nyyssola A, Kerovuo J, Kaukinen P, von Weymarn N, Reinikainen T. Extreme halophiles synthesize betaine from glycine by methylation. J Biol Chem 2000; 275: 22196–201.

    Article  CAS  PubMed  Google Scholar 

  • Ohnishi N, Murata N. 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 2006; 141: 758–765.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oinam G, Yeung E, Kurepin L, Haslam T, Villalobos AL. Adventitious root formation in ornamental plants: I. General overview and recent successes. Prop Ornam Plants 2011; 11: 78–90.

    Google Scholar 

  • Papageorgiou GC, Murata N. The unusually strong stabilizing effects of glycine betaine on the structure and function of the oxygen-evolving photosystem II complex. Photosyn Res 1995; 44: 243–52.

    Article  CAS  PubMed  Google Scholar 

  • Papageorgiou GC, Fujimura Y, Murata N. protection of the oxygen evolving Photosystem II complex by glycinebetaine. Biochim Biophys Acta 1991; 1057: 361–366.

    Article  CAS  Google Scholar 

  • Park EJ, Jeknic Z, Sakamoto A, DeNoma J, Yuwansiri R, Murata N, Chen THH. Genetic engineering of glycinebetaine synthesis in tomato protects seeds, plants, and flowers from chilling damage. Plant J 2004; 40: 474–87.

    Article  CAS  PubMed  Google Scholar 

  • Park EJ, Jeknic Z, Chen THH. Exogenous application of glycinebetaine increases chilling tolerance in tomato plants. Plant Cell Physiol 2006; 47: 706–14.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Park EJ, Lee WY, Kurepin LV, Zhang R, Janzen L, Pharis RP. Plant hormone-assisted early family selection in Pinus densiflora via a retrospective approach. Tree Physiol 2015; 35: 86–94.

    Article  PubMed  Google Scholar 

  • Peleg Z, Blumwald E. Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 2011; 14: 290–295.

    Article  CAS  PubMed  Google Scholar 

  • Prasad KVSK, Saradhi PP. Enhanced tolerance to photoinhibition in transgenic plants through targeting of glycinebetaine biosynthesis into the chloroplasts. Plant Sci 2004; 166: 1197–212.

    Article  CAS  Google Scholar 

  • Qaderi MM, Kurepin LV, Reid DM. Effects of temperature and watering regime on growth, gas exchange and abscisic acid content of canola (Brassica napus) seedlings. Environ Exp Bot 2012; 75: 107–13.

    Article  CAS  Google Scholar 

  • Qin X, Zeevaart JAD. Overexpression of a 9-cis-epoxycarotenoid dioxygenase gene in Nicotiana plumbaginifolia increases abscisic acid and phaseic acid levels and enhances drought tolerance. Plant Physiol 2002; 128: 544–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quan R, Shang M, Zhang H, Zhao Y, Zhang J. Improved chilling tolerance by transformation with betA gene for the enhancement of glycinebetaine synthesis in maize. Plant Sci 2004a; 166: 141–9.

    Article  CAS  Google Scholar 

  • Quan R, Shang M, Zhang H, Zhao Y, Zhang J. Engineering of enhanced glycine betaine synthesis improves drought tolerance in maize. Plant Biotech J 2004b; 2: 477–86.

    Article  CAS  Google Scholar 

  • Rahman S, Miyake H, Takeoka Y. Effects of exogenous glycinebetaine on growth and ultrastructure of salt-stressed rice seedlings (Oryza sativa L.). Plant Prod Sci 2002; 5: 33–44.

    Article  CAS  Google Scholar 

  • Rajagopal S, Carpentier R. Retardation of photo-induced changes in Photosystem I submembrane particles by glycinebetaine and sucrose. Photosyn Res 2003; 78: 77–85.

    Article  CAS  PubMed  Google Scholar 

  • Rajasekaran LR, Kriedemann PE, Aspinall D, Paleg LG. Physiological significance of proline and glycinebetaine: Maintaining photosynthesis during NaCl stress in wheat. Photosynthetica 1997; 34: 357–66.

    Article  CAS  Google Scholar 

  • Rapacz M, Waligórski P, Janowiak F. ABA and gibberellin-like substances during prehardening, cold acclimation, de- and reacclimation of oilseed rape. Acta Physiol Plant 2003; 25: 151–161.

    Article  CAS  Google Scholar 

  • Rathinasabapathi B, Burnet M, Russel BL, Gage DA, Liao P-C, Nye GJ, Scott P, Golbeck JH, Hanson AD. 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 1997; 94: 3454–3458.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rhodes D, Hanson AD. Quaternary ammonium and tertiary sulfonium compounds in higher plants. Ann Rev Plant Physiol Plant Mol Biol 1993; 44: 357–84.

    Article  CAS  Google Scholar 

  • Sahu BB, Shaw BP. Isolation, identification and expression analysis of salt-induced genes in Suaeda maritima, a natural halophyte using PCR-based suppression subtractive hybridization. BMC Plant Biol 2009; 9: 69.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sakamoto A, Murata N. Metabolic engineering of rice leading to biosynthesis of glycinebetaine and tolerance to salt and cold. Plant Mol Biol 1998; 38: 1011–9.

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto A, Murata N. The role of glycinebetaine in the protection of plants from stress: clue from transgenic plants. Plant Cell Environ 2002; 25: 63–71.

    Article  Google Scholar 

  • Saneoka H, Nagasaka C, Hahn DT, Yang WJ, Premachandra GS, Joly RJ, Rhodes D. Salt tolerance of glycinebetaine-deficient and -containing maize lines. Plant Physiol 1995; 107: 631–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saneoka H, Ishiguro S, Moghaieb REA. Effect of salinity and abscisic acid on accumulation of glycinebetaine and betaine aldehyde dehydrogenase mRNA in Sorghum leaves (Sorghum bicolor). J Plant Physiol 2001; 158: 853–9.

    Article  CAS  Google Scholar 

  • Scheller H, Haldrup A. Photoinhibition of photosystem I. Planta 2005; 221: 5–8.

    Article  CAS  PubMed  Google Scholar 

  • Schwartz SH, Zeevaart JAD. Abscisic acid biosynthesis and metabolism. In: Davies PJ, Ed. Plant Hormones: Biosynthesis, Signal Transduction and Action! (revised third edition). Springer Dordrecht Heidelberg London New York, 2010; pp. 137–55.

    Chapter  Google Scholar 

  • Scott IM, Clarke SM, Wood JE, Mur LAJ. Salicylate accumulation inhibits growth at chilling temperature in Arabidopsis. Plant Physiol 2004; 135: 1040–1049.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shahbaz M, Zia B. Does exogenous application of glycinebetaine through rooting medium alter rice (Oryza sativa L.) mineral nutrient status under saline conditions? J Appl Bot Food Qual 2011; 84: 54–60.

    CAS  Google Scholar 

  • Shirasawa K, Takabe T, Takabe T, Kishitani S. Accumulation of glycinebetaine in rice plants that overexpress choline monooxygenase from spinach and evaluation of their tolerance to abiotic stress. Ann Bot 2006; 98: 565–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinclair TR, Muchow RC, Ludlow MM, Leach GJ, Lawn RJ, Foale MA. Field and model analysis of the effect of water deficits on carbon and nitrogen accumulation by soybean, cowpea and black gram. Field Crop Res 1987; 17: 121–40.

    Article  Google Scholar 

  • Sonoike K. Photoinhibition of photosystem I: its physiological significance in the chilling sensitivity of plants. Plant Cell Physiol 1996; 37: 239–247

    Article  CAS  Google Scholar 

  • Takahashi W, Oishi H, Ebina M, Komatsu T, Takamizo T. Production of transgenic Italian ryegrass expressing the betaine aldehyde dehydrogenase gene of zoysiagrass. Breed Sci 2010; 60: 279–85.

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Thompson AJ, Jackson AC, Symonds RC, Mulholland BJ, Dadswell AR, Blake PS, Burbidge A, Taylor IB. Ectopic expression of a tomato 9-cis-epoxycarotenoid dioxygenase gene causes over-production of abscisic acid. Plant J 2000; 23: 363–74.

    Article  CAS  PubMed  Google Scholar 

  • Turnbull MH, Pharis RP, Kurepin LV, Sarfati M, Mander LN, Kelly D. Flowering in snow tussock (Chionochloa spp.) is influenced by temperature and hormonal cues. Funct Plant Biol 2012; 39: 38–50.

    Article  CAS  Google Scholar 

  • Wahid A, Shabbir A. Induction of heat stress tolerance in barley seedlings by pre-sowing seed treatment with glycinebetaine. Plant Growth Regul 2005; 46: 133–41.

    Article  CAS  Google Scholar 

  • Walton LJ, Kurepin LV, Reid DM, Chinnappa CC. Stem and leaf growth of alpine sun and prairie shade ecotypes of Stellaria longipes under different photoperiods: role of ethylene. Botany 2006; 84: 1496–1502.

    CAS  Google Scholar 

  • Walton LJ, Kurepin LV, Reid DM, Chinnappa CC. Narrow-band light regulation of ethylene and gibberellin levels in hydroponically-grown Helianthus annuus hypocotyls and roots. Plant Growth Regul 2010; 61: 53–59.

    Article  CAS  Google Scholar 

  • Walton LJ, Kurepin LV, Yeung EC, Shah S, Emery RJN, Reid DM, Pharis RP. Ethylene involvement in silique and seed development of canola (Brassica napus L.). Plant Physiol Biochem 2012; 58: 142–50.

    Article  CAS  PubMed  Google Scholar 

  • Wang LJ, Huang WD, Liu YP, Zhan JC. Changes in salicylic and abscisic acid contents during heat treatment and their effect on thermotolerance of grape plants. Russ J Plant Physiol 2005; 52: 516–520.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Weisz PR, Denison RF, Sinclair TR. Response to drought stress of nitrogen fixation (acetylene reduction) rates by field-grown soybeans. Plant Physiol 1985; 78: 525–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson KE, Ivanov AG, Öquist G, Grodzinski B, Sarhan F, Huner NPA. Energy balance, organellar redox status and acclimation to environmental stress. Can J Bot 2006; 84 1355–1370.

    Article  CAS  Google Scholar 

  • Wu L, Zu X, Wang X, Sun A, Zhang J, Wang S, Chen Y. Comparative proteomic analysis of the effects of salicylic acid and abscisic acid on maize (Zea mays L.) leaves. Plant Mol Biol Rep 2013; 31: 507–16.

    Article  CAS  Google Scholar 

  • Wyn Jones RG, Storey R, Leigh RA, Ahmad N, Pollard A. A hypothesis on cytoplasmic osmoregulation. In: Marre E, Cifferi O, Eds. Regulation of Cell Membrane Activities in Plants. Elsevier, Amsterdam, 1977; pp. 121–36.

    Google Scholar 

  • Xing W, Rajashekar CB. Glycine betaine involvement in freezing tolerance and water stress in Arabidopsis thaliana. Environ Exp Bot 2001; 46: 21–8.

    Article  CAS  PubMed  Google Scholar 

  • Yalpani N, Enyedi AJ, Leon J, Raskin I. Ultraviolet light and ozone stimulate accumulation of salicylic acid, pathogenesis related proteins and virus resistance in tobacco. Planta 1994; 193: 372–376.

    Article  CAS  Google Scholar 

  • Yang X, Liang Z, Lu C. Genetic engineering of the biosynthesis of glycinebetaine enhances photosynthesis against high temperature stress in transgenic tobacco plants. Plant Physiol 2005; 138: 2299–309.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang X, Liang Z, Wen X, Lu C. Genetic engineering of the biosynthesis of glycinebetaine leads to increased tolerance of photosynthesis to salt stress in transgenic tobacco plants. Plant Mol Biol 2008; 66: 73–86.

    Article  CAS  PubMed  Google Scholar 

  • Yu Y-B, Adams DO, Yanf SF. Inhibition of ethylene production by 2, 4-dinitrophenol and high temperature. Plant Physiol 1980; 66: 286–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaman M, Ghani A, Kurepin LV, Pharis RP, Khan S, Smith TJ. Improving ryegrass-clover pasture dry matter yield and urea efficiency with gibberellic acid. J Sci Food Agricul 2014; 94: 2521–2528.

    Article  CAS  Google Scholar 

  • Zaman M, Kurepin LV, Catto W, Pharis RP. Enhancing crop yield with the use of N-based fertilizers co-applied with plant hormones or growth regulators. J Sci Food Agric 2015; 95: 1777–1785.

    Article  CAS  PubMed  Google Scholar 

  • Zaman M, Kurepin LV, Catto W, Pharis RP. Evaluating the use of plant hormones and biostimulators in forage pastures to enhance shoot dry biomass production by perennial ryegrass (Lolium perenne L.). J Sci Food Agric 2016; 96: 715–726.

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Huang R. Enhanced tolerance to freezing in tobacco and tomato overexpressing transcription factor TERF2/LeERF2 is modulated by ethylene biosynthesis. Plant Mol Biol 2010; 73: 241–9.

    Article  CAS  PubMed  Google Scholar 

  • Zhang LX, Li SX, Liang ZS. Differential plant growth and osmotic effects of two maize (Zea mays L.) cultivars to exogenous glycinebetaine application under drought stress. Plant Growth Regul 2009; 58: 297–305.

    Article  CAS  Google Scholar 

  • Zhang L, Gao M, Hu J, Zhang X, Wang K, Ashraf M. Modulation role of abscisic acid (ABA) on growth, water relations and glycinebetaine metabolism in two maize (Zea mays L.) cultivars under drought stress. Int J Mol Sci 2012; 13: 3189–202.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao X-X, Ma Q-Q, Liang C, Fang Y, Wang YQ, Wang W. Effect of glycinebetaine on function of thylakoid membranes in wheat flag leaves under drought stress. Biol Plant 2007; 51: 584–8.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. Shazia Zaman for drawing the chemical structures of glycine betaine, abscisic acid and salicylic acid. We would also like to acknowledge the financial support from the Ballance Agri-Nutrients, New Zealand (MZ, LVK, RPP), KEMPE Foundation, Sweden (VMH, LVK, NPAH), Natural Sciences and Engineering Research Council of Canada (NPAH) , the Canada Research Chairs Program (NPAH) and the Canada Foundation for Innovation (NPAH).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Leonid V. Kurepin or Alexander G. Ivanov .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Kurepin, L.V., Ivanov, A.G., Zaman, M., Pharis, R.P., Hurry, V., Hüner, N.P.A. (2017). Interaction of Glycine Betaine and Plant Hormones: Protection of the Photosynthetic Apparatus During Abiotic Stress. In: Hou, H., Najafpour, M., Moore, G., Allakhverdiev, S. (eds) Photosynthesis: Structures, Mechanisms, and Applications. Springer, Cham. https://doi.org/10.1007/978-3-319-48873-8_9

Download citation

Publish with us

Policies and ethics