Plant Growth Regulation

, Volume 55, Issue 1, pp 1–10 | Cite as

Salicylic acid activates phenylalanine ammonia-lyase in grape berry in response to high temperature stress

  • Peng-Fei Wen
  • Jian-Ye Chen
  • Si-Bao Wan
  • Wei-Fu Kong
  • Ping Zhang
  • Wei Wang
  • Ji-Cheng Zhan
  • Qiu-Hong Pan
  • Wei-Dong Huang
Original Paper

Abstract

Our previous work has indicated that salicylic acid (SA) is involved in the development of pea plant thermotolerance and induces the gene expression of phenylalanine ammonia-lyase (PAL; EC 4.3.1.5), a key enzyme in phenylpropanoid metabolism of grape berry. However, the relationship between SA and PAL during high temperature stress remains obscure. The present experiment, using the technique of in vivo incubation of the grape berry (Vitis vinifera L. cv. Cabernet Sauvignon) tissue in the SA-contained medium, the effects of exogenous SA on the gene expression of PAL and the accumulation of polyphenols during high temperature stress were investigated. The results showed that SA could induce the accumulation of PAL mRNA and the synthesis of new PAL protein, and increase the activity under high temperature stress. A significant accumulation of phenolics was also observed in the SA-treated berries. But, the activation of PAL by SA could be blocked by the pretreatments of berry tissues with the protein synthesis inhibitor cycloheximide, and mRNA transcription inhibitor, actinomycin D, respectively. It is thus speculated that SA may induce the activation of PAL and the accumulation of pheonlics leading to the development of thermotolerance.

Keywords

Grape berry Salicylic acid Phenylalanine ammonia-lyase Phenolics High temperature stress 

Abbreviations

MDA

Malondialdehyde

PAL

Phenylalanine ammonia-lyase

SA

Salicylic acid

References

  1. Anderson MD, Prasad TK, Martin BA, Steward CR (1994) Differential gene expression in chilling acclimated maize seedlings and evidence for the involvement of abcisic acid in chilling tolerance. Plant Physiol 105:331–339PubMedGoogle Scholar
  2. Bolwell GP (1992) A role for phosphorylation in the down regulation of phenylalanine ammonia-lyase in suspension cultured cells of French bean. Phytochemistry 31:4081–4086CrossRefGoogle Scholar
  3. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Bichem 72:248–254CrossRefGoogle Scholar
  4. Campos-Vargas R, Nonogaki H, Suslow T, Saltveit ME (2005) Heat shock treatments delay the increase in wound-induced phenylalanine ammonia-ammonia-lyase activity by altering its expression, not its induction in Romaine lettuce (Lactuca sativa) tissue. Physiol Plant 132:82–91CrossRefGoogle Scholar
  5. Chen JY, Wen PF, Kong WF, Pan QH, Zhan JC, Li JM, Wan SB, Huang WD (2006) Effect of salicylic acid on phenylpropanoids and phenylalanine ammonia-lyase in harvested grape berries. Postharvest Biol Technol 40:64–72CrossRefGoogle Scholar
  6. Cheng S, Purgear J, Cairney JA (1993) Simple and efficient method for isolation RNA from pine trees. Plant Mol Biol Rep 11:113–116CrossRefGoogle Scholar
  7. Clarke SM, Mur LAJ, Wood JE, Scott IM (2004) Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. Plant J 38:432–447PubMedCrossRefGoogle Scholar
  8. Crosby JS, Vayda ME (1991) Stress-induced translational control in potato tubers may be mediated by polysome-associated proteins. Plant Cell 3:1013–1023PubMedCrossRefGoogle Scholar
  9. Dat JF, Lopez-Delgado H, Foyer CH, Scott IM (1998) Parallel change in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116:1351–1357PubMedCrossRefGoogle Scholar
  10. Ding CK, Wang CY, Gross KC (2002) Jasmonate and salicylate induce the expression of pathogenesis-related-protein genes and increase resistance to chilling injury in tomato fruit. Planta 214:895–901PubMedCrossRefGoogle Scholar
  11. Dixon RA, Achnine L, Kota P, Liu CJ, Srinivasa MS, Wang LJ (2002) The phenylpropanoid pathway and plant defence-a genomics perspective. Mol Plant Pathol 3:371–390CrossRefGoogle Scholar
  12. Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097PubMedCrossRefGoogle Scholar
  13. Fraissinet-Tachet L, Baltz R, Chong J, Kauffmann S, Fritig B, Saindrenan P (1998) Two tobacco genes induced by infection, elicitor and salicylic acid encode glucosyltransferases acting on phenylpropanoids and benzoic acid derivatives, including salicylic acid. FEBS Lett 437:319–323PubMedCrossRefGoogle Scholar
  14. Grace SC, Logan BA, Adams WW (1998) Seasonal differences in foliar content of chlorogenic acid, a phenylpropanoid antioxidant, in Mahonia repens. Plant Cell Environ 21:513–521CrossRefGoogle Scholar
  15. Janas KM, Cvikrová M, Palagiewicz A, Szafranska K, Posmyk MM (2002) Constitutive elevated accumulation of phenylpropanoids in soybean roots at low temperature. Plant Sci 163:369–373CrossRefGoogle Scholar
  16. Jones DH (1984) Phenylalanine ammonia-lyase: regulation of its induction, and role in plant development. Phytochemistry 23:1349–1359CrossRefGoogle Scholar
  17. Laemmli UK (1970) Cleavage of structural protein during the assembly of the head of bacteriophage T4. Nature 227:680–685PubMedCrossRefGoogle Scholar
  18. Lafuente MT, Zacarias L, Martinez-Telez MA, Sanchez-Ballesta MT, Granell A (2003) Phenylalanine ammonia-lyase and ethylene in relation to chilling injury as affected by fruit age in citrus. Postharvest Biol Technol 29:308–317CrossRefGoogle Scholar
  19. Lafuente MT, Sala JM, Zacarias L (2004) Active oxygen detoxifying enzymes and phenylalanine ammonia-lyase in the ethylene-induced chilling tolerance in citrus fruit. J Agric Food Chem 52:3606–3611PubMedCrossRefGoogle Scholar
  20. Larkindale J, Knight MR (2002) Protection against heat stress induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:682–695PubMedCrossRefGoogle Scholar
  21. Larkindale J, Huang BR (2004) Thermotolerance and antioxidant systems in Agrostis stolonifera: involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene. J Plant Physiol 161:405–413PubMedCrossRefGoogle Scholar
  22. Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593PubMedCrossRefGoogle Scholar
  23. Leyva A, Jarillo JA, Salinas J, Martinez-Zapater JM (1995) Low temperature induces the accumulation of phenylalanine ammonialyase and chalcone synthase mRNA of Arabidopsis thaliana in a light-dependent manner. Plant Physiol 108:39–46PubMedGoogle Scholar
  24. Liang X, Dron M, Schimd J, Dixon RA, Lamb CJ (1989) Development and environmental regulation of a phenylalanine ammonia-lyase-β-glucuronidase gene fusion in transgenic tobacco plants. Proc Natl Aca Sci USA 86:9284–9288CrossRefGoogle Scholar
  25. Liu HT, Liu YY, Pan QH, Yang HR, Zhan JC, Huang WD (2006) Novel interrelationship between salicylic acid, abscisic acid, and PIP2-specific phospholipase C in heat acclimation-induced thermotolerance in pea leaves. J Exp Bot 57:3337–3347PubMedCrossRefGoogle Scholar
  26. Lopez-Delgado H, Dat JF, Foyer CH, Scott IM (1998) Induction of thermotolerance in potato microplants by acetyl salicylic acid and H2O2. J Exp Bot 49:713–720CrossRefGoogle Scholar
  27. Lyons JM (1973) Chilling injury in plants. Annu Rev Plant Physiol 24:445–466CrossRefGoogle Scholar
  28. Paliyath G, Pinhero RG, Rao MV, Murr DP, Fletcher RA (1997) Changes in activities of antioxidant enzymes and their relationship to genetic and paclobutrazol-induced chilling tolerance in maize seedlings. Plant Physiol 114:695–704PubMedGoogle Scholar
  29. Pan QH, Zhan JC, Liu HT, Zhang JH, Chen JY, Wen PF, Huang WD (2006) Salicylic acid synthesized by benzoic acid 2-hydroxylase participates in the development of thermotolerance in pea plants. Plant Sci 171:226–233CrossRefGoogle Scholar
  30. Prasad TK, Anderson MD, Martin BA, Steward CR (1994a) Evidence for chilling-induce oxidative stress in maize seedlings and a regulatory role of hydrogen peroxide. Plant Cell 6:65–74PubMedCrossRefGoogle Scholar
  31. Prasad TK, Anderson MD, Steward CR (1994b) Acclimation, hydrogen peroxide and abcisic acid protect mitochondria against irreversible chilling injury in maize seedlings. Plant Physiol 105:619–627PubMedGoogle Scholar
  32. Rivero RM, Ruiz JM, García PC, López-Lefebre LR, Sánchez E, Romero L (2001) Resistance to cold and heat stress: accumulation of phenolic compounds in tomato and watermelon plants. Plant Sci 160:315–321PubMedCrossRefGoogle Scholar
  33. Sanchez-Ballesta MT, Zacarias L, Granell A, Lafuente MT (2000) Accumulation of PAL transcript and PAL activity as affected by heat-conditioning and low-temperature storage and its relation to chilling sensitivity in mandarin fruits. J Agric Food Chem 48:2726–2731PubMedCrossRefGoogle Scholar
  34. Senaratna TD, Touchell EB, Dixon K (2000) Acetyl salicylic acid (aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Regul 30:157–161CrossRefGoogle Scholar
  35. Sgarbi E, Fornasiero RB, Lins AP, Bonatti PM (2003) Phenol metabolism is differentially affected by ozone in two cell lines from grape (Vitis vinifera L.) leaf. Plant Sci 165:951–957CrossRefGoogle Scholar
  36. Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158Google Scholar
  37. Solecka D, Kacperska A (2003) Phenylpropanoid deficiency affects the course of plant acclimation to cold. Physiol Plant 119:253–262CrossRefGoogle Scholar
  38. Teklemariam TA, Blake TJ (2004) Phenylalanine ammonia-lyase-induced freezing tolerance in jack pine (Pinus banksiana) seedlings treated with low, ambient levels of ultraviolet-B radiation. Physiol Plant 122:244–253CrossRefGoogle Scholar
  39. Thulke O, Conrath U (1998) Salicylic acid has a dual role in the activation of defence-related genes in parsley. Plant J 14:35–42PubMedCrossRefGoogle Scholar
  40. Wang CY (1982) Physiological and biochemical response of plant to chilling stress. HortScience 17:173–186Google Scholar
  41. Wen PF, Chen JY, Kong WF, Pan QH, Wan SB, Huang WD (2005) Salicylic acid induced the expression of phenylalanine ammonia-lyase gene in grape berry. Plant Sci 169:928–934CrossRefGoogle Scholar
  42. Zhu Q, Dabi T, Beeche A, Yamamoto R, Lawton MA, Lamb C (1995) Cloning and properties of a rice gene encoding phenylalanine ammonia-lyase. Plant Mol Biol 29:535–550PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Peng-Fei Wen
    • 1
    • 2
  • Jian-Ye Chen
    • 3
  • Si-Bao Wan
    • 1
  • Wei-Fu Kong
    • 1
  • Ping Zhang
    • 1
  • Wei Wang
    • 1
  • Ji-Cheng Zhan
    • 1
  • Qiu-Hong Pan
    • 1
  • Wei-Dong Huang
    • 1
  1. 1.College of Food Science and Nutritional EngineeringChina Agricultural UniversityBeijingP.R. China
  2. 2.College of HorticultureShanXi Agricultural UniversityTaiguP.R. China
  3. 3.Guangdong Key Laboratory for Postharvest Science, College of HorticultureSouth China Agricultural UniversityGuangzhouP.R. China

Personalised recommendations