Advertisement

Planta

, Volume 218, Issue 1, pp 65–70 | Cite as

A survey of genes differentially expressed during long-term heat-induced chilling tolerance in citrus fruit

  • María Teresa Sanchez-Ballesta
  • Yolanda Lluch
  • María José Gosalbes
  • Lorenzo Zacarias
  • Antonio Granell
  • María Teresa LafuenteEmail author
Original Article

Abstract

Long-term storage at low, non-freezing, temperature (1.5 °C) induces chilling injury in fruit of Fortune mandarin (Citrus clementina Hort. Ex Tanaka × Citrus reticulata, Blanco), manifested as pitting and brown depressed areas that may end up with local cell death. Pre-conditioning of fruit for 3 days at 37 °C prevented chilling injury. The use of suppression subtractive hybridization permitted the isolation of genes differentially expressed in heat-conditioned fruit exposed to chilling conditions, which may be candidates for heat-induced chilling tolerance. Northern blot analysis revealed that some genes were up-regulated by prolonged heat (3 days/37 °C) and their expression persisted in fruit cells upon subsequent chilling exposure. The expression of other genes was specifically induced by the combination of heat and cold. Among the putative tolerance-associated genes, we identified two transcription factors of the WRKY family and one TFIIB factor. Heat conditioning also altered the expression of genes encoding proteins involved in secondary metabolism, cell wall modification, oxidative damage and other stress-responsive proteins. These results illustrate the complexity of molecular mechanisms operating during heat-induced chilling tolerance in citrus fruit.

Keywords

Chilling Citrus fruit Gene expression Heat conditioning Suppression subtractive hybridization Transcription factors 

Abbreviations

CI

chilling injury

HICT

heat-induced chilling tolerance

HSP

heat-shock protein

SSH

suppression subtractive hybridization

Notes

Acknowledgments

We thank Dr. L. González-Candelas and Dr. J.F. Marcos (IATA–CSIC) for discussion and advice. This work was supported by a research grant FAIR-CT98-4096 from the EU.

References

  1. Baldwin DA, Gurley WB (1996) Isolation and characterization of cDNAs encoding transcription factor IIB from Arabidopsis and soybean. Plant J 10:561–568CrossRefPubMedGoogle Scholar
  2. Belles-Boix E, Babiychuk E, Van Montagu M, Inze D, Kushnir S (2000) CEO1, a new protein from Arabidopsis thaliana, protects yeast against oxidative damage. FEBS Lett 482:19–24CrossRefPubMedGoogle Scholar
  3. Cathala G, Savanret JF, Mendez B, West BL, Karon M, Martial J, Baxter J (1983) A method for isolation of intact, translationally active ribonucleic acid. DNA 2:324–335Google Scholar
  4. Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025–6030PubMedGoogle Scholar
  5. Dong J, Chen C, Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51:21–37CrossRefPubMedGoogle Scholar
  6. Ernst D, Schraudner M, Langebartels D, Sandermann H Jr (1992) Ozone-induced changes of mRNA levels of beta-1,3-glucanase, chitinase and 'pathogenesis-related' protein 1b in tobacco plants. Plant Mol Biol 20:673–682PubMedGoogle Scholar
  7. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206PubMedGoogle Scholar
  8. Gonzalez-Aguilar GA, Zacarias L, Lafuente MT (1998) Ripening affects high-temperature-induced polyamines and their changes during cold storage of hybrid 'Fortune' mandarins. J Agric Food Chem 46:3503–3508CrossRefGoogle Scholar
  9. Györgyey J, Németh K, Magyar Z, Kelemen Z, Alliotte T, Inzé D, Dudits D (1997) Expression of a novel-type small proline-rich protein gene of alfalfa is induced by 2,4-dichlorophenoxiacetic acid in dedifferentiated callus cells. Plant Mol Biol 34:593–602CrossRefPubMedGoogle Scholar
  10. Hara K, Yagi M, Kusano T, Sano H (2000) Rapid systemic accumulation of transcripts encoding a tobacco WRKY transcription factor upon wounding. Mol Gen Genet 263:30–37PubMedGoogle Scholar
  11. Hauschild MZ (1993) Putrescine (1,4-diaminobutane) as an indicator of pollution-induced stress in higher plants: barley and rape stressed with Cr(III) or Cr(VI). Ecol Environ Saf 26:228–247CrossRefGoogle Scholar
  12. Hinderhofer K, Zentgraf U (2001) Identification of a transcription factor specifically expressed at the onset of leaf senescence. Planta 213:469–473PubMedGoogle Scholar
  13. Kurth J, Varotto C, Pesaresi P, Biehl A, Richly E, Salamini F, Leister D (2002) Gene-sequence tag-expression analyses of 1,800 genes related to chloroplast functions. Planta 215:101–109CrossRefPubMedGoogle Scholar
  14. Lafuente MT, Belver A, Guye MG, Saltveit ME Jr (1991) Effect of temperature conditioning on chilling injury of cucumber cotyledons. Possible role of abscisic acid and heat shock proteins. Plant Physiol 95:443–449Google Scholar
  15. Lafuente MT, Martínez-Téllez MA, Zacarias L (1997) Abscisic acid in the response of Fortune mandarins to chilling. Effect of maturity and high-temperature conditioning. J Sci Food Agric 73:494–502CrossRefGoogle Scholar
  16. Lee JE, Vogt T, Hause B, Lobler M (1997) Methyl jasmonate induces an O-methyltransferase in barley. Plant Cell Physiol 38:851–862Google Scholar
  17. Lee JH, Van Montagu M, Verbruggen N (1999) A highly conserved kinase is an essential component for stress tolerance in yeast and plant cells. Proc Natl Acad Sci USA 96:5873–5877CrossRefPubMedGoogle Scholar
  18. Lurie S (1998) Postharvest heat treatments. Postharv Biol Technol 14:257–269CrossRefGoogle Scholar
  19. Orth K, Xu Z, Mudgett MB, Bao ZQ, Palmer LE, Bliska JB, Mangel WF, Staskawicz B, Dixon JE (2000) Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290:1594–1597CrossRefPubMedGoogle Scholar
  20. Pan S, Czarnecka-Verner E, Gurley WB (2000) Role of the TATA binding protein-transcription factor IIB interaction in supporting basal and activated transcription in plant cells. Plant Cell 12:125–136CrossRefPubMedGoogle Scholar
  21. Porat R, Vinokur V, Holland D, McCollum TG, Droby S (2001) Isolation of a citrus chitinase cDNA and characterization of its expression in response to elicitation of fruit pathogen resistance. J Plant Physiol 158:1585–1590Google Scholar
  22. Porat R, Pavoncello D, Ben-Hayyim G, Lurie S (2002a) A heat treatment induced the expression of a Na+/H+ antiport gene (cNHX1) in citrus fruit. Plant Sci 162:957–963CrossRefGoogle Scholar
  23. Porat R, Pavoncello D, Lurie S, McCollum TG (2002b) Identification of a grapefruit cDNA belonging to a unique class of citrus dehydrins and characterization of its expression patterns under temperature stress conditions. Physiol Plant 115:598–603CrossRefPubMedGoogle Scholar
  24. Sabehat A, Lurie S, Weiss D (1998) Expression of small heat-shock proteins at low temperatures. A possible role in protecting against chilling injuries. Plant Physiol 117:651–658PubMedGoogle Scholar
  25. Sala JM, Lafuente MT (1999) Catalase in the heat-induced chilling tolerance of cold-stored hybrid Fortune mandarin fruits. J Agric Food Chem 47:2410–2414CrossRefPubMedGoogle Scholar
  26. Sanz A, Moreno JI, Castresana C (1998) PIOX, a new pathogen-induced oxygenase with homology to animal cyclooxygenase. Plant Cell 10:1523–1537CrossRefPubMedGoogle Scholar
  27. Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13:61–72PubMedGoogle Scholar
  28. Szederkenyi J, Komor E, Schobert C (1997) Cloning of the cDNA for glutaredoxin, an abundant sieve-tube exudate protein from Ricinus communis L. and characterisation of the glutathione-dependent thiol-reduction system in sieve tubes. Planta 202:349–356CrossRefPubMedGoogle Scholar
  29. Thomashow MF (2001) So what's new in the field of plant cold acclimation? Lots! Plant Physiol 125:89–93Google Scholar
  30. Thompson DK, Palmer JR, Daniels CJ (1999) Expression and heat-responsive regulation of a TFIIB homologue from the archaeon Haloferax volcanii. Mol Microbiol 33:1081–1092CrossRefPubMedGoogle Scholar
  31. Thomsen J, De Biase A, Kaczanowski S, Macario AJL, Thomm M, Zielenkiewicz P, MacColl R, Conway de Macario E (2001) The basal transcription factors TBP and TFB from the mesophilic archaeon Methanosarcina mazeii: Structure and conformational changes upon interaction with stress-gene promoters. J Mol Biol 309:589–603CrossRefPubMedGoogle Scholar
  32. Wang CY, Bowen JH, Weir IE, Allan AC, Ferguson IB (2001) Heat-induced protection against death of suspension-cultured apple fruit cells exposed to low temperature. Plant Cell Environ 24:1199–1207CrossRefGoogle Scholar
  33. Woolf AB, Watkins CB, Bowen JH, Lay-Yee M, Maindonal JH, Ferguson B (1995) Reducing external chilling injury in stored 'Hass' avocados with dry heat treatments. J Am Soc Hort Sci 120:1050–1056Google Scholar
  34. Yasuda E, Ebinuma H, Wabiko H (1997) A novel glycine-rich/hydrophobic 16 kda polypeptide gene from tobacco: similarity to proline-rich protein genes and its wound-inducible and developmentally regulated expression. Plant Mol Biol 33:667–678CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • María Teresa Sanchez-Ballesta
    • 1
  • Yolanda Lluch
    • 2
  • María José Gosalbes
    • 1
  • Lorenzo Zacarias
    • 1
  • Antonio Granell
    • 2
  • María Teresa Lafuente
    • 1
    Email author
  1. 1.Instituto de Agroquímica y Tecnología de Alimentos (IATA)Consejo Superior de Investigaciones Científicas (CSIC)BurjassotSpain
  2. 2.Instituto de Biología Molecular y Celular de Plantas (IBMCP), Consejo Superior de Investigaciones Científicas (CSIC)Universidad Politécnica de ValenciaValenciaSpain

Personalised recommendations