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Transcriptomic analysis of cold response in tomato fruits identifies dehydrin as a marker of cold stress

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Abstract

Tomato is sensitive to cold during vegetative growth, fruit set, development, and ripening. We have characterized the effect of cold stress (6°C for up to 48 h) on the transcriptome of Micro-Tom tomato fruits during ripening by subtractive PCR. The cold stress caused modifications in gene expression of housekeeping genes. From a total of 38 genes up-regulated by cold, only one clone — a dehydrin homologue — was related to previously identified cold-stress genes. Phylogenetic analysis showed its clustering with other cold-induced dehydrins, and increased distances from dehydrins activated by abscisic acid. Quantitative expression analysis of tomato dehydrin showed it was activated by cold treatment in leaves and fruits. As dehydrin is a member of theSl-CBF1 regulon from tomato, we analyzed the cold-responsive transcription factorSl-CBF1 in mature leaves and ripening fruits stored at 6°C. Leaves of Micro-Tom showed high basal levels of the transcription factorSl-CBF1, compared to fruits. Cold treatment caused increased levels ofSl-CBF1 expression in leaves but not in fruits of Micro-Tom and Demisem (a commercial cultivar). Tomato dehydrin can be used as a transcriptional marker of cold stress in leaves and ripening fruits. However, our results indicate that the cold response activation of dehydrin gene in tomato fruits is the consequence of an alternative pathway, different from theSl-CBF1 regulon.

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References

  • Alonso-Blanco C, Gomez-Mena C, Llorente F, Koornneef M, Salinas J, Martinez-Zapater JM, 2005. Genetic and molecular analyses of natural variation indicateCBF2 as a candidate gene for underlying a freezing tolerance quantitative trait locus inArabidopsis. Plant Physiol 139: 1304–1312.

    Article  CAS  PubMed  Google Scholar 

  • Carbone F, Pizzichini D, Giuliano G, Rosati C, Perrotta G, 2005. Comparative profiling of tomato fruits and leaves evidences — a complex modulation of global transcript profiles. Plant Sci 169: 165–175.

    Article  CAS  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK, 2006. Gene regulation during cold acclimation in plants. Physiologia Plantarum 126: 52–61.

    Article  CAS  Google Scholar 

  • Choi DW, Zhu B, Close TJ, 1999. The barley (Hordeum vulgare L.) dehydrin multigene family: sequences, allele types, chromosome assignments, and expression characteristics of 11 Dhn genes of cv Dicktoo. Theor Appl Genet 98: 1234–1247.

    Article  CAS  Google Scholar 

  • Davies B, Egea-Cortines M, de Andrade SE, Saedler H, Sommer H, 1996. Multiple interactions amongst floral homeotic MADS box proteins. EMBO J 15: 4330–4343.

    CAS  PubMed  Google Scholar 

  • Diatchenko L, Lau Y-FC, Campbell AP, Chenchik A, Moqadam F, Huang B, et al. 1996. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93: 6025–6030.

    Article  CAS  PubMed  Google Scholar 

  • Egea-Cortines M, Cohen E, Arad S, Bagni N, Mizrahi Y, 1993. Polyamine levels in pollinated and auxin-induced fruit of tomato (Lycopersicon esculentum) during development. Physiol Plantarum 87: 14–20.

    Article  CAS  Google Scholar 

  • Fei ZJ, Tang X, Alba RM, White JA, Ronning CM, Martin GB, et al. 2004. Comprehensive EST analysis of tomato and comparative genomics of fruit ripening. Plant J 40: 47–59.

    Article  PubMed  Google Scholar 

  • Fernandez-Munoz R, Gonzalez-Fernandez JJ, Cuartero J, 1995. Variability of pollen tolerance to low temperatures in tomato and related wild species. J Hortic Sci 70: 41–49.

    Google Scholar 

  • Foolad MR, Lin GY, 2000. Relationship between cold tolerance during seed germination and vegetative growth in tomato: germplasm evaluation. J Am Soc Hortic Sci 125: 679–683.

    Google Scholar 

  • Foolad MR, Lin GY, 2001. Genetic analysis of cold tolerance during vegetative growth in tomato,Lycopersicon esculentum Mill. Euphytica 122: 105–111.

    Article  Google Scholar 

  • Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF, 1998. Lowtemperature regulation of theArabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16: 433–442.

    Article  CAS  PubMed  Google Scholar 

  • Giovannoni J, Yen H, Shelton B, Miller S, Vrebalov J, Kannan P, et al. 1999. Genetic mapping of ripening and ethylene-related loci in tomato. Theor Appl Genet 98: 1005–1013.

    Article  CAS  Google Scholar 

  • Gomez di Marco P, Ferrer MA, Fernandez-Trujillo JP, Calderon AA, Artes F, Egea-Cortines M et al 2009. Structural changes, chemical composition and antioxidant activity of cherry tomato fruits (cv. Micro-Tom) stored under optimal and chilling conditions. Journal of the Science of Food and Agriculture DOI: 10.1002/jsfa.3622.

  • Hara M, Terashima S, Fukaya T, Kuboi T, 2003. Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta 217: 290–298.

    CAS  PubMed  Google Scholar 

  • Hsieh TH. Lee JT, Yang PT, Chiu LH, Charng YY, Wang YC, Chan MT, 2004. Heterology expression of theArabidopsis c-repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. Plant Physiol 135: 1145–1145.

    Article  CAS  Google Scholar 

  • Jackman RL, Yada RY, Marangoni AG, Parkin KL, Stanley DW, 1989. Chilling injury: a review of quality aspects. J Food Quality 11: 253–278.

    Article  Google Scholar 

  • Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF, 1998.Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280: 104–106.

    Article  CAS  PubMed  Google Scholar 

  • Jones A, 2000. Does the plant mitochondrion integrate cellular stress and regulate programmed cell death? Trends Plant Sci 5: 225–230.

    Article  CAS  PubMed  Google Scholar 

  • Kader A, 1992. Postharvest technology of horticultural crops. 2nd edn. Davis: University of California.

    Google Scholar 

  • Kiyosue T, Yamaguchishinozaki K, Shinozaki K, 1994. Characterization of 2 cDNAs (Erd10 and Erd14) corresponding to genes that respond rapidly to dehydration stress inArabidopsis thaliana. Plant Cell Physiol 35: 225–231.

    CAS  PubMed  Google Scholar 

  • Kosova K, Vitamvas P, Prasil IT, 2007. The role of dehydrins in plant response to cold. Biol Plant 51: 601–617.

    Article  CAS  Google Scholar 

  • Kovacs D, Kalmar E, Torok Z, Tompa P, 2008. Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiol 147: 381–390.

    Article  CAS  PubMed  Google Scholar 

  • Lozano R, Angosto T, Gomez P, Payan C, Capel J, Huijser P, et al. 1998. Tomato flower abnormalities induced by low temperatures are associated with changes of expression of MADS-box genes. Plant Physiol 117: 91–100.

    Article  CAS  PubMed  Google Scholar 

  • Lukyanov K, Diatchenko L, Chenchik A, Nanisetti A, Siebert P, Usman N, et al. 1997. Construction of cDNA libraries from small amounts of total RNA using the suppression PCR effect. Biochem Bioph Res Comm 230: 285–288.

    Article  CAS  Google Scholar 

  • Malacrida C, Valle EM, Boggio SB, 2006. Postharvest chilling induces oxidative stress response in the dwarf tomato cultivar Micro-Tom. Physiol Plantarum 127: 10–18.

    Article  CAS  Google Scholar 

  • Manchado-Rojo M, Weiss J, Egea-Cortines M, 2008. Using 23 rDNA to identify contaminations ofE. coli inAgrobacterium tumefaciens cultures. Anal Biochem 372: 253–254.

    Article  CAS  PubMed  Google Scholar 

  • Meissner R, Chague V, Zhu Q, Emmanuel E, Elkind Y, Levy AA, 2000. Technical advance: a high throughput system for transposon tagging and promoter trapping in tomato. Plant J 22: 265–274.

    Article  CAS  PubMed  Google Scholar 

  • Naik D, Dhanaraj AL, Arora R, Rowland LJ, 2007. Identification of genes associated with cold acclimation in blueberry (Vaccinium corymbosum L.) using a subtractive hybridization approach. Plant Sci 173: 213–222.

    Article  CAS  Google Scholar 

  • Natali L, Giordani T, Lercari B, Maestrini P, Cozza R, Pangaro T, et al. 2007. Light induces expression of a dehydrin-encoding gene during seedling de-etiolation in sunflower (Helianthus annuus L.). J Plant Physiol 164: 263–273.

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW, 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucl. Acids Res. 29: e45.

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW, Horgan GW, Dempfle L, 2002. Relative expression software tool (REST(C)) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucl. Acids Res. 30: e36.

    Article  PubMed  Google Scholar 

  • Porat R, Pasentsis K, Rozentzvieg D, Gerasopoulos D, Falara V, Samach A, et al. 2004. Isolation of a dehydrin cDNA from orange and grapefruit citrus fruit that is specifically induced by the combination of heat followed by chilling temperatures. Physiol Plantarum 120: 256–264.

    Article  CAS  Google Scholar 

  • Sanchez-Ballesta MT, Rodrigo MJ, LaFuente MT, Granell A, Zacarias L, 2004. Dehydrin from citrus, which confers in vitro dehydration and freezing protection activity, is constitutive and highly expressed in the flavedo of fruit but responsive to cold and water stress in leaves. J Agr Food Chem 52: 1950–1957.

    Article  CAS  Google Scholar 

  • Smith MAL, Spomer LA, Shibli RA, Knight SL, 1992. Effects of NaCl salinity on miniature dwarf tomato Micro-Tom. Part 2. Shoot and root-growth responses, fruit production, and osmotic adjustment. J Plant Nutr 15: 2329–2341.

    Article  CAS  Google Scholar 

  • Stockinger EJ, Gilmour SJ, Thomashow MF, 1997.Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94: 1035–1040.

    Article  CAS  PubMed  Google Scholar 

  • Thomashow MF, 1999. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol and Plant Mol Biol 50: 571–599.

    Article  CAS  Google Scholar 

  • an Berkel J, Salamini F, Gebhardt C, 1994. Transcripts accumulating during cold storage of potato (Solanum tuberosum L.) tubers are sequence related to stress-responsive genes. Plant Physiol 104: 445–452.

    Article  PubMed  Google Scholar 

  • Venema JH, Linger P, van Heusden AW, van Hasselt PR, Bruggemann W, 2005. The inheritance of chilling tolerance in tomato (Lycopersicon spp.). Plant Biology 7: 118–130.

    Article  CAS  PubMed  Google Scholar 

  • Yang TW, Zhang LJ, Zhang TG, Zhang H, Xu SJ, An LZ, 2005. Transcriptional regulation network of cold-responsive genes in higher plants. Plant Sci 169: 987–995.

    Article  CAS  Google Scholar 

  • Yano K, Aoki K, Suda K, Suzuki T, Sakurai N, Narita T, et al. 2007. KaFTom: Full-length cDNA Database of a miniature tomato cultivar Micro-Tom. Plant Cell Physiol 48: S255-S255.

    Google Scholar 

  • Yano K, Watanabe M, Yamamoto N, Maeda F, Tsugane T, Shibata D, 2005. Expressed sequence tags (EST) database of a miniature tomato cultivar, Micro-Tom. Plant Cell Physiol 46: S139-S139.

    Google Scholar 

  • Yin ZM, Rorat T, Szabala BM, Ziolkowska A, Malepszy S, 2006. Expression of aSolanum sogarandinum SK3-type dehydrin enhances cold tolerance in transgenic cucumber seedlings. Plant Sci 170: 1164–1172.

    Article  CAS  Google Scholar 

  • Zhang X, Fowler SG, Cheng HM, Lou YG, Rhee SY, Stockinger EJ, 2004. Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerantArabidopsis. Plant J 39: 905–919.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to M. Egea-Cortines.

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Weiss, J., Egea-Cortines, M. Transcriptomic analysis of cold response in tomato fruits identifies dehydrin as a marker of cold stress. J Appl Genet 50, 311–319 (2009). https://doi.org/10.1007/BF03195689

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