Molecular Biology Reports

, Volume 41, Issue 3, pp 1401–1410 | Cite as

Glycine betaine protects tomato (Solanum lycopersicum) plants at low temperature by inducing fatty acid desaturase7 and lipoxygenase gene expression

  • T. Karabudak
  • M. Bor
  • F. Özdemir
  • İ. Türkan


Cold stress is among the environmental stressors limiting productivity, yield and quality of agricultural plants. Tolerance to cold stress is associated with the increased unsaturated fatty acids ratio in the plant membranes which are also known to be substrates of octadecanoid pathway for jasmonate and other oxylipins biosynthesis. Accumulation of osmoprotectant, glycine betaine (GB) is well known to be effective in the protecting membranes and mitigating cold stress effects but, the mode of action is poorly understood. We studied the role of GB in cold stress responses of two tomato cultivated varieties; Gerry (cold stress sensitive) and T47657 (moderately cold stress tolerant) and compared the differences in lypoxygenase-13 (TomLOXF) and fatty acid desaturase 7 (FAD7) gene expression profiles and physiological parameters including relative growth rates, relative water content, osmotic potential, photosynthetic efficiency, membrane leakage, lipid peroxidation levels. Our results indicated that GB might have a role in inducing FAD7 and LOX expressions for providing protection against cold stress in tomato plants which could be related to the desaturation process of lipids leading to increased membrane stability and/or induction of other genes related to stress defense mechanisms via octadecanoid pathway or lipid peroxidation products.


Tomato Chilling stress FAD7 LOX Lipid peroxidation PUFAs 



This research was supported by Ege University Research Foundation with the grant number 2010-FEN-021. The authors are grateful to Tuna Saygan from Syngenta-Turkey for providing us Gerry and T47657 seeds and to Kera Yücel and Levent Soylu for their technical assistance.


  1. 1.
    Yu C, Wang HS, Yang S, Tang XF, Duan M, Meng QW (2009) Overexpression of endoplasmic reticulum omega-3 fatty acid desaturase gene improves chilling tolerance in tomato. Plant Physiol Biochem 47:1102–1112PubMedCrossRefGoogle Scholar
  2. 2.
    Liu XY, Li B, Yang JH, Sui N, Yang XM, Meng QW (2008) Overexpression of tomato chloroplast omega-3 fatty acid desaturase gene alleviates the photoinhibition of photosystems 2 and 1 under chilling stress. Photosynthesis 46(2):185–192CrossRefGoogle Scholar
  3. 3.
    Wallis JG, Watts JL, Browse J (2002) Polysaturated fatty acid synthesis: what will they think of next? Trends Biochem Sci 27(9):463–467CrossRefGoogle Scholar
  4. 4.
    Wasternack C, Stenzel I, Hause B, Hause G, Kutter C, Maucher H, Neumerkel J, Feussner I, Miersch O (2006) The wound response in tomato-role of jasmonic acid. J Plant Physiol 163:297–306PubMedCrossRefGoogle Scholar
  5. 5.
    Franklin-Torres ML, Repellin A, Van-Biet H, Agnes d’Arcy L, Zuily-Fodil Y, Pham-Thi AT (2009) Omega-3 fatty acid desaturase (FAD3, FAD7, FAD8) gene expression and linolenic acid content in cowpea leaves submitted to drought and after rehydration. Environ Exp Bot 65:162–169CrossRefGoogle Scholar
  6. 6.
    Sakurai I, Hagio M, Gombos Z, Tyystjarvi T, Paakkarinen V, Aro EM, Wada H (2003) Requirement of phosphatidyl-glycerol for maintenance of photosynthetic machinery. Plant Physiol 133:1376–1384PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Feussner I, Wasternack C (2002) The lipoxygenase pathway. Ann Rev Plant Biol 53:275–297CrossRefGoogle Scholar
  8. 8.
    Weber H (2002) Fatty acid-derived signals in plants. Trends Plant Sci 7:217–224PubMedCrossRefGoogle Scholar
  9. 9.
    Laxalt AM, Munnik T (2002) Phospholipid signalling in plant defence. Curr Opin Plant Biol 5:1–7CrossRefGoogle Scholar
  10. 10.
    Shi Y, An L, Li X, Huang C, Chen G (2011) The octadecanoid signaling pathway participates in the chilling-induced transcription of ω-3 fatty acid desaturases in Arabidopsis. Plant Physiol Biochem 49:208–215PubMedCrossRefGoogle Scholar
  11. 11.
    Dave A, Graham A (2012) Oxylipin signaling: a distinct role for the jasmonic acid precursor cis-(+)-12-Oxo-phytodienoic acid (cis-OPDA). Front Plant Sci 3(42):1–6Google Scholar
  12. 12.
    Avila CA, Arevalo-Soliz LM, Jia L, Navarre DA, Chen Z, Howe GA, Meng QW, Smith JE, Goggin FL (2012) Loss of function of fatty acıd desaturase7 in tomato enhances basal aphid resistance in a salicylate-dependent manner. Plant Physiol 158(4):2028–2041PubMedCentralPubMedCrossRefGoogle Scholar
  13. 13.
    Khodakovskaya M, McAvoy R, Peters J, Wu H, Li Y (2006) Enhanced cold tolerance in transgenic tobacco expressing a chloroplast omega 3 fatty acid desaturase gene under the control of a cold inducible promoter. Planta 223:1090–1100PubMedCrossRefGoogle Scholar
  14. 14.
    Wang J, Ming F, Pittman J, Han Y, Hu J, Guo B, Shen D (2006) Characterization of a rice (Oryza sativa L.) gene encoding a temperature-dependent chloroplast omega-3 fatty acid desaturase. Biochem Biophys Res Commun 340:1209–1216PubMedCrossRefGoogle Scholar
  15. 15.
    Zhou Z, Wang MJ, Zhao ST, Hu JJ, Lu MZ (2010) Changes in freezing tolerance in hybrid poplar caused by up- and down-regulation of PtFAD2 gene expression. Trans Res 19:647–654CrossRefGoogle Scholar
  16. 16.
    Nishiuchi T, Hamada T, Kodama H, Iba K (1997) Wounding changes the spatial expression pattern of the Arabidopsis plastid v-3 fatty acid desaturase gene (FAD7) through different signal transduction pathways. Plant Cell 9:1701–1712PubMedCentralPubMedGoogle Scholar
  17. 17.
    Sun JQ, Jiang HL, Li CY (2011) Systemin mediated systemic defense signaling in tomato. Mol Plant 4:607–615PubMedCrossRefGoogle Scholar
  18. 18.
    Li C, Liu G, Xu C, Lee GI, Bauer P, Ling HQ, Gana MW, Howe GA (2003) The tomato suppressor of prosystemin-mediated responses2 gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemic wound signal for defense gene expression. Plant Cell 15:1646–1661PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu Rev Plant Physiol Plant Mol Biol 44:357–384CrossRefGoogle Scholar
  20. 20.
    Park EJ, Jeknic Z, Chen THH (2006) Exogenous application of glycinebetaine ıncreases chilling tolerance in tomato plants. Plant Cell Physiol 47(6):706–714PubMedCrossRefGoogle Scholar
  21. 21.
    Chen WP, Li PH, Chen THH (2000) Glycinebetaine increases chilling tolerance and reduces chilling-induced lipid peroxidation in Zea mays L. Plant Cell Environ 23:609–618CrossRefGoogle Scholar
  22. 22.
    Allard F, Houde M, Krol M, Ivanov A, Hunner NPA, Sarhan F (1998) Betaine improves freezing tolerance in wheat. Plant Cell Physiol 39:1194–1202CrossRefGoogle Scholar
  23. 23.
    Hunt R, Causton DR, Shipley B, Askew P (2002) A modern tool for classical plant growth analysis. Ann Bot 90:485–488PubMedCrossRefGoogle Scholar
  24. 24.
    Madhava Rao KV, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeon pea (Cajanus cajan L. Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128PubMedCrossRefGoogle Scholar
  25. 25.
    Santa-Cruz MM, Martinez-Rodriguez F, Perez-Alfocea R, Romero-Aranda R, Bolarin MC (2002) The rootstock effect on the tomato salinity response depends on the shoot genotype. Plant Sci 162:825–831CrossRefGoogle Scholar
  26. 26.
    Smart RE, Bingham GE (1974) Rapid estimates of relative water content. Plant Physiol 53:258–260PubMedCentralPubMedCrossRefGoogle Scholar
  27. 27.
    Scotti CP, Thu Pham Thi A (1997) Effects of abscisic acid pretreatment on membrane leakage and lipid composition of Vigna unguiculata leaf discs subjected to osmotic stres. Plant Sci 130:11–18CrossRefGoogle Scholar
  28. 28.
    Subbarao GV, Wheeler RM, Stutte GW, Levine LH (1999) How far can sodium substitute for potassium in red beet? J Plant Nutr 22:1745–1761PubMedCrossRefGoogle Scholar
  29. 29.
    Bessieres MA, Gibbon Y, Lefeuvre JC, Larher F (1999) A single-step purification for glycine betaine determination in plant extracts by ısocratic HPLC. J Agric Food Chem 47(12):5297PubMedCrossRefGoogle Scholar
  30. 30.
    Murata N, Mohanty PS, Hayashi H, Papageorgiou GC (1992) Glycinebetaine stabilizes the association of extrinsic proteins with the photosynthetic oxygen-evolving complex. FEBS Lett 296:187–189PubMedCrossRefGoogle Scholar
  31. 31.
    Wolter FP, Schmidt R, Heinz E (1992) Chilling sensitivity of Arabidopsis thaliana with genetically engineered membrane lipids. EMBO J 11:4685–4692PubMedGoogle Scholar
  32. 32.
    Yokoi S, Higashi S, Kishitani S, Murata N, Toriyama K (1998) Introduction of the cDNA for Arabidopsis glycerol-3-phosphate acyltransferase (GPAT) confers unsaturation of fatty acids and chilling tolerance of photosynthesis on rice. Mol Breed 4:269–275CrossRefGoogle Scholar
  33. 33.
    Kaniuga Z, Saczynska V, Miskiewicz E (1998) Galactolipase activity but not the level of high melting point phosphatidylglycerol is related to chilling tolerance in differentially sensitive Zea mays inbred lines. Plant Cell Rep 17:897–901CrossRefGoogle Scholar
  34. 34.
    Ariizumi T, Kishitani S, Inatsugi R, Nishida I, Murata N, Toriyama K (2002) An increase in unsaturation of fatty acids in phosphatidylglycerol from leaves improves the rates of photosynthesis and growth at low temperatures in transgenic rice seedlings. Plant Cell Physiol 43:751–758PubMedCrossRefGoogle Scholar
  35. 35.
    Kaur G, Kumar S, Nayyar H, Upadhyaya HD (2008) Cold stress injury during the pod filling phase in chickpea (Cicer arietinum L.): effects on quantitative and qualitative components of seeds. J Agric Crop Sci 194:457–464Google Scholar
  36. 36.
    Holmström KO, Somersalo S, Mandal A, Palva TE, Welin B (2000) Improved tolerance to salinity and low temperature in transgenic tobacco producing glycine betaine. J Exp Bot 51(343):177–185PubMedCrossRefGoogle Scholar
  37. 37.
    Venema JH, Postumus F, De Vries M, Van Hasselt PR (1999) Differential response of domestic and wild Lycopersicon species to chilling under low light: growth, carbohydrate content, photosynthesis and the xanthophylls cycle. Physiol Plant 105:81–88CrossRefGoogle Scholar
  38. 38.
    Gibon Y, Bessieres MA, Larher F (1997) Is glycine betaine a non-compatible solute in higher plants that do not accumulate it? Plant Cell Environ 20:329–340CrossRefGoogle Scholar
  39. 39.
    Makela P, Jokinen K, Kontturi M, Peltonen-Sainio P, Pehu E, Somersalo S (1998) Foliar application of glycinebetaine—a novel product from sugar beet- as an approach to increase tomato yield. Ind Crop Prod 7:139–148CrossRefGoogle Scholar
  40. 40.
    Sakamoto A, Alia A, Murata N (1998) Metabolic engineering of rice leading to biosynthesis of glycinebetaine and tolerance to salt and cold. Plant Mol Biol 38:1011–1019PubMedCrossRefGoogle Scholar
  41. 41.
    Demiral T, Turkan I (2004) Does exogenous glycinebetaine affect antioxidative system of rice seedlings under NaCl treatment? J Plant Physiol 161:1089–1100PubMedCrossRefGoogle Scholar
  42. 42.
    Zhao Y, Aspinall D, Paleg LG (1992) Protection of Membrane Integrity in Medicago sativa L. by glycinebetaine against the effects of freezing. J Plant Physiol 140:541–543CrossRefGoogle Scholar
  43. 43.
    Marocco A, Lorenzoni C, Fracheboud Y (2005) Chilling stress in maize. Maydica 50:571–580Google Scholar
  44. 44.
    Naidu BP, Paleg LG, Aspinall D, Jennings AC, Jones GP (1991) Amino acid and glycine betaine accumulation in cold stressed wheat seedlings. Phytochemistry 30(2):407–409CrossRefGoogle Scholar
  45. 45.
    Farmer EE, Almeras E, Krishnamurthy V (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr Opin Plant Biol 6:372–378PubMedCrossRefGoogle Scholar
  46. 46.
    Almeras E, Stolz S, Vollenweider S, Reymond P, Mene-Saffrane L, Farmer EE (2003) Reactive electrophile species activate defense gene expression in Arabidopsis. Plant J 34:205–216PubMedCrossRefGoogle Scholar
  47. 47.
    Weber H, Che ´telat A, Reymond P, Farmer EE (2004) Selective and powerful stress gene expression in Arabidopsis in response to malondialdehyde. Plant J 37:877–888PubMedCrossRefGoogle Scholar
  48. 48.
    Mene-Saffrane L, Dubugnon L, Che ´telat A, Stolz S, Gouhier-Darimont C, Farmer EE (2009) Nonenzymatic oxidation of trienoic fatty acids contributes to reactive oxygen species management in Arabidopsis. J Biol Chem 284:1702–1708PubMedCrossRefGoogle Scholar
  49. 49.
    Orlova IV, Serebriiskaya TS, Popov V, Merkulova N, Nosov AM, Trunova TI, Tsydendambaev VD, Los DA (2003) Transformation of tobacco with a gene fort he thermophylic acyl-lipid desaturase enhances the chilling tolerance of plants. Plant Cell Physiol 44:447–450PubMedCrossRefGoogle Scholar
  50. 50.
    Holley SR, Yalamanchili RD, Moura DS, Ryan CA, Stratmann JW (2003) Convergence of signalling pathways induced by systemin, oligosaccharide elicitors and ultraviolet B radiation at the level of MAPKs in Lycopersicon peruvianum suspension cultured cells. Plant Phyisol 132:1728–1732CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • T. Karabudak
    • 1
  • M. Bor
    • 1
  • F. Özdemir
    • 1
  • İ. Türkan
    • 1
  1. 1.Department of Biology, Science FacultyEge UniversityIzmirTurkey

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