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Candidate gene expression profiling in two contrasting tomato cultivars under chilling stress

  • Original Papers
  • Published:
Biologia Plantarum

Abstract

Tomato (Solanum lycopersicum Mill.) is sensitive to chilling stress during all stages of plant development. Genetic variation for chilling tolerance exists between cultivated tomato and its related wild species, but intra-specific variation has not been thoroughly investigated so far. Seedlings of 63 tomato accessions were evaluated under low temperature and two contrasting cultivars were identified for the trait: Albenga and San Marzano, the former being more chillingtolerant. To clarify the molecular mechanisms of chilling tolerance in tomato, changes in candidate gene expressions in the two tomato genotypes were analysed, using quantitative RT-PCR. Candidate genes were chosen among those known to be induced by chilling and/or with putative roles in CBF/DREB and ROS-mediated pathways. Results show that besides a CBF regulon, whose function is conserved, ROS and C2H2-type zinc finger protein-mediated cold signalling pathways were also involved in chilling tolerance. Under the chilling stress, the up-regulation of respective transcripts was consistently higher in the chilling-tolerant genotype than in the chilling-sensitive ones.

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Abbreviations

ABA:

abscisic acid

AP2/ERF:

APETALA 2/ethylene response factor

Aux/IAA:

auxin/indole-3-acetic acid

bZIP:

basic region-leucine zipper

CBF/DREB:

C-repeat binding factor/dehydration-responsive element binding

COR:

cold-regulated

CRT/DRE:

C-repeat/dehydration responsive element

Ct:

cycle threshold

DHNs:

dehydrins

DMRT:

Duncan’s multiple range test

EAR-motif:

ERF-associated amphiphilic repression motif

EF-1-α:

elongation factor 1-α

EL:

electrolyte leakage

ERF:

ethylene response factor

FAD:

fatty acid desaturase

GLM:

generalized linear model

ILs:

introgression lines

LEA:

late embryogenesis abundant

MYB:

myeloblastosis

NLS:

nuclear localization signal

NTC:

no template control

RT-qPCR:

reverse transcription-quantitative PCR

RCBD:

randomized complete block design

REST©:

relative expression software tool©

ROS:

reactive oxygen species

SGN:

sol genomics network

TFs:

transcription factors

USP:

universal stress protein

WT:

wild type

References

  • Alam, B., Jacob, J.: Overproduction of photosynthetic electrons is associated with chilling injury in green leaves. — Photosynthetica 40: 91–95, 2002.

    Article  CAS  Google Scholar 

  • Apel, K., Hirt, H.: Reactive oxygen species: metabolism, oxidative stress, and signal transduction. — Annu. Rev. Plant Biol. 55: 373–399, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Asada, K., Takahashi, M.: Production and scavenging of active oxygen in photosynthesis. — In: Kyle, D.J., Osmond, C.B., Arntzen, C.J. (ed.): Photoinhibition: Topics in Photosynthesis. Pp. 227–287. Elsevier Scientific Publishers, Amsterdam 1987.

    Google Scholar 

  • Bloom, A.J., Zwieniecki, M.A., Passioura, J.B., Randall, L.B., Holbrook, N.M., St. Clair, D.A.: Water relations under root chilling in a sensitive and tolerant tomato species. — Plant Cell Environ. 27: 971–979, 2004.

    Article  Google Scholar 

  • Bravo, L.A., Gallardo, J., Navarrete, A., Olave, N., Martínez, J., Alberdi, M., Close, T.J., Corcuera, L.J.: Cryoprotective activity of a cold induced dehydrin purified from barley. — Physiol. Plant. 118: 262–269, 2003.

    Article  CAS  Google Scholar 

  • Breton, G., Danyluk, J., Charron, J.B., Sarhan, F.: Expression profiling and bioinformatic analyses of a novel stressregulated multispanning transmembrane protein family from cereals and Arabidopsis. — Plant Physiol. 132: 64–74, 2003.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Cheng, C., Yun, K.Y., Ressom, H., Mohanty, B., Bajic, V.B., Jia, Y., Yun, S.J., De los Reyes, B.G.: An early response regulatory cluster induced by low temperature and hydrogen peroxide in seedlings of chilling-tolerant japonica rice. — BMC Genomics 8: e175, 2007.

    Article  CAS  Google Scholar 

  • Christie, P.J., Alfenito, M.R., Walbot, V.: lmpact of low temperature stress on general phenylpropanoid and anthocyanin pathways: enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings. — Planta 194: 541–549, 1994.

    Article  CAS  Google Scholar 

  • Close, T.J.: Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. — Physiol. Plant. 97: 795–803, 1996.

    Article  CAS  Google Scholar 

  • Close, T.J.: Dehydrins: a commonality in the response of plants to dehydration and low temperature. — Physiol. Plant. 100: 291–296, 1997.

    Article  CAS  Google Scholar 

  • Cook, D., Fowler, S., Fiehn, O., Thomashow, M.F.: A prominent role for the CBF cold response pathway in configuring the low temperature metabolome of Arabidopsis. — Proc. nat. Acad. Sci. USA 101: 15243–15248, 2004.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Crifò, T., Puglisi, I., Petrone, G., Recupero, R., Piero, A.R.L.: Expression analysis in response to low temperature stress in blood oranges: implication of the flavonoid biosynthetic pathway. — Gene 476: 1–9, 2011.

    Article  PubMed  CAS  Google Scholar 

  • Desikan, R., Mackerness, S.A.H., Hancock, J.T., Neill, S.J.: Regulation of the Arabidopsis transcriptome by oxidative stress. — Plant Physiol. 127: 159–172, 2001.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Elizondo, R., Oyanedel, E.: Field testing of tomato chilling tolerance under varying light and temperature conditions. — Chil. J. agr. Res. 70: 552–558, 2010.

    Article  Google Scholar 

  • Eriksson, S.K., Kutzer, M., Procek, J., Grobner, G., Harryson, P.: Tunable membrane binding of the intrinsically disordered dehydrin Lti30, a cold-induced plant stress protein. — Plant Cell 23: 2391–2404, 2011.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fernandez, P., Rienzo, J.D., Fernandez, L., Hopp, H.E., Paniego, N., Heinz, R.A.: Transcriptomic identification of candidate genes involved in sunflower responses to chilling and salt stresses based on cDNA microarray analysis. — BMC Plant Biol. 8: 11, 2008.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Foolad, M.R., Lin, G.Y.: Relationship between cold tolerance during seed germination and vegetative growth in tomato: Germplasm evaluation. — J. amer. Soc. hort. Sci. 125: 679–683, 2000.

    Google Scholar 

  • Fowler, S., Thomashow, M.F.: Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. — Plant Cell 14:1675–1690, 2002.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gilmour, S.J., Sebolt, A.M., Salazar, M.P., Everard, J.D., Thomashow, M.F.: Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. — Plant Physiol. 124: 1854–1865, 2000.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Goodstal, F.J., Kohler, G.R., Randall, L.B., Bloom, A.J., St Clair, D.A.: A major QTL introgressed from wild Lycopersicon hirsutum confers chilling tolerance to cultivated tomato (Lycopersicon esculentum). — Theor. appl Genet. 111: 898–905, 2005.

    Article  CAS  Google Scholar 

  • Gupta, N., Rathore, M., Goyary, D., Khare, N., Anandhan, S., Pande, V., Ahmed, Z.: Marker-free transgenic cucumber expressing Arabidopsis cbf1 gene confers chilling stress tolerance. — Biol. Plant. 56: 57–63, 2012.

    Article  CAS  Google Scholar 

  • He, L.G., Wang, H.L., Liu, D.C., Zhao, Y.J., Xu, M., Zhu, M., Wei, G.Q., Sun Z.H.: Isolation and expression of a coldresponsive gene PtCBF in Poncirus trifoliata and isolation of citrus CBF promoters. — Biol. Plant. 56: 484–492, 2012.

    Article  CAS  Google Scholar 

  • Jaglo, K.R., Kleff, S., Amundsen, K.L., Zhang, X., Haake, V., Zhang, J.Z., Deits, T., Thomashow, M.F.: Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. — Plant Physiol. 127: 910–917, 2001.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jaglo-Ottosen, K.R., Gilmour, S.J., Zarka, D.G., Schabenberger, O., Thomashow, M.F.: Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. — Science 280:104-106, 1998.

    Google Scholar 

  • Jakoby, M., Weisshaar, B., Droge-Laser, W., Vicente-Carbajosa, J., Tiedemann, J., Kroj, T., Parcy, F.: bZIP transcription factors in Arabidopsis. — Trends Plant Sci. 7: 106–111, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Kasuga, M., Kiu, Q., Miura, S., Yamaguchi-Shinozaki, K., Shinozaki, K.: Improving plant drought, salt and freezing tolerance by gene transfer of a single stress-inducible transcription factor. — Nat. Biotechnol. 17: 287–291, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Kiełbowicz-Matuk, A.: Involvement of plant C2H2-type zinc finger transcription factors in stress responses. — Plant Sci. 185-186: 78–85, 2012.

    Article  PubMed  CAS  Google Scholar 

  • Kodama, H., Hamada, T., Horiguchi, G., Nishimura, M., Iba, K.: Genetic enhancement of cold tolerance by expression of a gene for chloroplast v-3 fatty acid desaturase in transgenic tobacco. — Plant Physiol. 105: 601–605, 1994.

    PubMed Central  PubMed  CAS  Google Scholar 

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

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kusano, T., Berberich, T., Harada, M., Suzuki, N., Sugawara, K.: A maize DNA-binding factor with a bZIP motif is induced by low temperature. — Mol. Genet. Genomics 248: 507–517, 1995.

    Article  CAS  Google Scholar 

  • Larkindale, J., Knight, M.R.: Protection against heat stress induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. — Plant Physiol. 128: 682–695, 2002.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Leyva, A., Jarillo, J.A., Salinas, J., Martinez-Zapater, J.I.M.: Low temperature induces the accumulation of phenylalanine ammonia-lyase and chalcone synthase mRNAs of Arabidopsis thaliana in a light-dependent manner. — Plant Physiol. 108: 39–46, 1995.

    PubMed Central  PubMed  CAS  Google Scholar 

  • Lin, Y.H., Hwang, S.Y., Hsu, P.Y., Chiang, Y.C., Huang, C.L., Wang, C.N., Lin, T.P.: Molecular population genetics and gene expression analysis of duplicated CBF genes of Arabidopsis thaliana. — BMC Plant Biol. 8: 111, 2008.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Liu, H., Ouyang, B., Zhang, J., Wang, T., Li, H., Zhang, Y., Yu, C., Ye, Z.: Differential modulation of photosynthesis, signaling, and transcriptional regulation between tolerant and sensitive tomato genotypes under cold stress. — PLoS One 7: e50785, 2012.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Liu, X.Y., Yang, J.H., Li, B., Yang, X.M., Meng, Q.W.: Antisense-mediated depletion of tomato chloroplast omega-3 fatty acid desaturase enhances thermal tolerance. — J. Integr. Plant Biol. 48: 1096–1107, 2006.

    Article  CAS  Google Scholar 

  • Liu, X.Y., Li, B., Yang, J.H., Sui, N., Yang, X.M., Meng, Q.W.: Overexpression of tomato chloroplast omega-3 fatty acid desaturase gene alleviates the photoinhibition of photosystems 2 and 1 under chilling stress. — Photosynthetica 46: 185–192, 2008.

    Article  CAS  Google Scholar 

  • Løvdal, T., Lillo, C.: Reference gene selection for quantitative real-time PCR normalization in tomato subjected to nitrogen, cold, and light stress. — Anal. Biochem. 387: 238–242, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Lyons, J.M.: Chilling injury in plants. — Annu. Rev. Plant Physiol. 24: 445–466, 1973.

    Article  CAS  Google Scholar 

  • Mantyla, E., Lang, V., Palva, E.T.: Role of abscisic acid in drought induced freezing tolerance, cold acclimation, and accumulation of LTl78 and RABl8 proteins in Arabidopsis thaliana. — Plant Physiol. 107: 141–148, 1995.

    PubMed Central  PubMed  Google Scholar 

  • Mao, D., Chen, C.: Colinearity and similar expression pattern of rice DREB1s reveal their functional conservation in the cold-responsive pathway. — PLoS One 7: e47275, 2012.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mboup, M., Fischer, I., Lainer, H., Stephan, W.: Trans-species polymorphism and allele-specific expression in the CBF gene family of wild tomatoes. — Mol. Biol. Evol. 29: 3641–3652, 2012.

    Article  PubMed  CAS  Google Scholar 

  • McKhann, H.I., Gery, C., Bérard, A., Lévêque, S., Zuther, E., Hincha, D.K., De Mita, S., Brunel, D., Teoule, E.: Natural variation in CBF gene sequence, gene expression and freezing tolerance in the Versailles core collection of Arabidopsis thaliana. — BMC Plant Biol. 8: 105, 2008.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mittler, R.: Oxidative stress, antioxidants and stress tolerance. — Trends Plant Sci. 7: 405–410, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Mittler, R., Vanderauwera, S., Gollery, M., Van Breusegem, F.: Reactive oxygen gene network of plants. — Trends Plant Sci. 9: 490–498, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Miura, K., Shiba, H., Ohta, M., Kang, S.W., Sato, A., Yuasa, T., Iwaya-Inoue, M., Kamada, H., Ezura, H.: SlICE1 encoding a MYC-type transcription factor controls cold tolerance in tomato, Solanum lycopersicum. — Plant Biotechnol. 29: 253–260, 2012.

    Article  CAS  Google Scholar 

  • Morsy, M.R., Almutairi, A.M., Gibbons, J., Yun, S.J., De los Reyes, B.G.: The OsLti6 genes encoding low-molecularweight membrane proteins are differentially expressed in rice cultivars with contrasting sensitivity to low temperature. — Gene 344: 171–180, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Movahedi, S., Sayed Tabatabaei, B.E., Alizade, H., Ghobadi, C., Yamchi, A., Khaksar, G.: Constitutive expression of Arabidopsis DREB1B in transgenic potato enhances drought and freezing tolerance. — Biol. Plant. 56: 37–42, 2012.

    Article  CAS  Google Scholar 

  • Neill, S., Desikan, R., Hancock, J.: Hydrogen peroxide signaling. — Curr. Opin. Plant Biol. 5: 388–395, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Okawa, K., Nakayama, K., Kakizaki, T., Yamashita, T., Inaba, T.: Identification and characterization of Cor413im proteins as novel components of the chloroplast inner envelope. — Plant Cell Environ. 31: 1470–1483, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Orino, K., Lehman, L., Tsuji, Y., Ayaki, H., Torti, S.V., Torti, F.M.: Ferritin and the response to oxidative stress. — Biochem. J. 357: 241–247, 2001.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Orlova, I.V., Serebriiskaya, T.S., Popov, V., Merkulova, N., Nosov, A.M., Trunova, T.I., Tsydendambaev, V.D., Los, D.A.: Transformation of tobacco with a gene for the thermophylic acyl-lipid desaturase enhances the chilling tolerance of plants. — Plant Cell Physiol. 44: 447–450, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Pan, Y., Seymour, G.B., Lu, C., Hu, Z., Chen, X., Chen, G.: An ethylene response factor (ERF5) promoting adaptation to drought and salt tolerance in tomato. — Plant Cell Rep. 31: 349–360, 2012.

    Article  PubMed  CAS  Google Scholar 

  • Pennycooke, J.C., Cox, S., Stushnoff, C.: Relationship of cold acclimation, total phenolic content and antioxidant capacity with chilling tolerance in petunia (Petunia × hybrida). — Environ. exp. Bot. 53: 225–232, 2005.

    Article  CAS  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Prasad, T.K.: Mechanisms of chilling-induced oxidative stress injury and tolerance in developing maize seedlings: changes in antioxidant system, oxidation of proteins and lipids and protease activities. — Plant J. 10: 1017–1026, 1996.

    Article  CAS  Google Scholar 

  • Puhakainen, T., Hess, M.W., Mäkelä, P., Svensson, J., Heino, P., Palva, E.T.: Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. — Plant mol. Biol. 54: 743–753, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Raison, J.K., Lyons, J.M.: Chilling injury: a plea for uniform terminology. — Plant Cell Environ. 9: 685–686, 1986.

    Article  Google Scholar 

  • Rice-Evans, C.A., Miller, N.J., Paganga, G.: Antioxidant properties of phenolic compounds. — Trends Plant Sci. 2: 152–159, 1997.

    Article  Google Scholar 

  • Rizza, F., Crosatti, C., Stanca, A.M., Cattivelli, L.: Studies for assessing the influence of hardening on cold tolerance of barley genotypes. — Euphytica 75: 131–138, 1994.

    Article  Google Scholar 

  • Sauter, M., Rzewuski, G., Marwedel, T., Lorbiecke, R.: The novel ethylene regulated gene OsUsp1 from rice encodes a member of a plant protein family related to prokaryotic universal stress proteins. — J. exp. Bot. 53: 2325–2331, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Scott, S.J., Jones, R.A.: Low temperature seed germination of Lycopersicon species evaluated by survival analysis. — Euphytica 31: 869–883, 1982.

    Article  Google Scholar 

  • Seong, E.S., Kwon, S.S., Ghimire, B.K., Yu, C.Y., Cho, D.H., Lim, J.D., Kim, K.S., Heo, K., Lim, E.S., Chung, I.M., Kim, M.J., Lee, Y.S.: LebZIP2 induced by salt and drought stress and transient overexpression by Agrobacterium. — BMB Rep. 41: 693–698, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Sharma, M.K., Kumar, R., Solanke, A.U., Sharma, R., Tyagi, A.K., Sharma, A.K.: Identification, phylogeny, and transcript profiling of ERF family genes during development and abiotic stress treatments in tomato. — Mol. Genet. Genomics 284: 455–475, 2010.

    Article  PubMed  CAS  Google Scholar 

  • Somerville, C., Browse, J.: Plant lipids: metabolism, mutants, and membranes. — Science 252: 80–87, 1991.

    Article  PubMed  CAS  Google Scholar 

  • Tanaka, Y., Sasaki, N., Ohmiya, A.: Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. — Plant J. 54: 733–749, 2008.

    Article  PubMed  CAS  Google Scholar 

  • The Tomato Genome Consortium: the tomato genome sequence provides insights into fleshy fruit evolution. — Nature 485: 635–641, 2012.

    Article  CAS  Google Scholar 

  • Theocharis, A., Clément, C., Barka, E.A.: Physiological and molecular changes in plants grown at low temperatures. — Planta 235: 1091–1105, 2012.

    Article  PubMed  CAS  Google Scholar 

  • Thomashow, M.F.: Plant cold acclimation: freezing tolerances genes and regulatory mechanisms. — Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 571–599, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Thomashow, M.F.: So what’s new in the field of plant cold acclimation? Lots! — Plant Physiol. 125: 89–93, 2001.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Thomashow, M.F.: Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. — Plant Physiol. 154: 571–577, 2010.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Torres, M.A., Dangl, J.L.: Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. — Curr. Opin. Plant Biol. 8: 397–403, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Truco, M.J., Randall, L.B., Bloom, A.J., St. Clair, D.A.: Detection of QTLs associated with shoot wilting and root ammonium uptake under chilling temperatures in an interspecific backcross population from Lycopersicon esculentum X L. hirsutum. — Theor. appl. Genet. 101: 1082–1092, 2000.

    Article  CAS  Google Scholar 

  • Vallejos, C.E., Pearcy, R.W.: Differential acclimation potential to low temperature in two species of Lycopersicon: photosynthesis and growth. — Can. J. Bot. 65: 1303–1307, 1987.

    Article  Google Scholar 

  • Vannini, C., Iriti, M., Bracale, M., Locatelli, F., Faoro, F., Croce, P., Pirona, R., Di Maro, A., Coraggio, I., Genga, A.: The ectopic expression of the rice Osmyb4 gene in Arabidopsis increases tolerance to abiotic, environmental and biotic stresses. — Physiol. mol. Plant Pathol. 69: 26–42, 2006.

    Article  CAS  Google Scholar 

  • Venema, J.H., Posthumus, F., De Vries, M., Van Hasselt, P.R.: Differential response of domestic and wild Lycopersicon species to chilling under low light: growth, carbohydrate content, photosynthesis and the xanthophyll cycle. — Physiol. Plant. 105: 81–88, 1999.

    Article  CAS  Google Scholar 

  • Venema, J.H., Linger, P., Van Heusden, A.W., Van Hasselt, P.R., Bruggemann, W.: The inheritance of chilling tolerance in tomato (Lycopersicon spp.). — Plant Biol. 7: 118–130, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Weiss, J., Egea-Cortines, M.: Transcriptomic analysis of cold response in tomato fruits identifies dehydrin as a marker of cold stress. — J. appl. Genetics 50: 311–319, 2009.

    Article  CAS  Google Scholar 

  • Wolf, S., Yakir, D., Stevens, M.A., Rudich, J.: Cold temperature tolerance of wild tomato species. — J. amer. Soc. hort. Sci. 111: 960–964, 1986.

    Google Scholar 

  • Xiao, H., Tattersall, E.A., Siddiqua, M.K., Cramer, G.R., Nassuth, A.: CBF4 is a unique member of the CBF transcription factor family of Vitis vinifera and Vitis riparia. — Plant Cell Environ. 31: 1–10, 2008.

    PubMed  CAS  Google Scholar 

  • Yu, C., Wang, H.S., Yang, S., Tang, X.F., Duan, M., Meng, Q.W.: Overexpression of endoplasmic reticulum omega-3 fatty acid desaturase gene improves chilling tolerance in tomato. — Plant Physiol. Biochem. 47: 1102–1112, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Yun, K.Y., Park, M.R., Mohanty, B., Herath, V., Xu, F., Mauleon, R., Wijaya, E., Bajic, V.B., Bruskiewich, R., De los Reyes, B.: Transcriptional regulatory network triggered by oxidative signals configures the early response mechanisms of japonica rice to chilling stress. — BMC Plant Biol. 10: e16, 2010.

    Article  CAS  Google Scholar 

  • Zhang, T., Zhao, X., Wang, W., Pan, Y., Huang, L., Liu, X., Zong, Y., Zhu, L., Yang, D., Fu, B.: Comparative transcriptome profiling of chilling stress responsiveness in two contrasting rice genotypes. — PLoS One 7: e43274, 2012.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhang, X., Fowler, S.G., Cheng, H., Lou, Y., Rhee, S.Y., Stockinger, E.J., Thomashow, M.F.: Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis. — Plant J. 39: 905–919, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, X., Guo, X., Lei, C., Cheng, Z., Lin, Q., Wang, J., Wu, F., Wang, J., Wan, J.: Overexpression of SlCZFP1, a novel TFIIIA-type zinc finger protein from tomato, confers enhanced cold tolerance in transgenic Arabidopsis and rice. — Plant mol. Biol. Rep. 29: 185–196, 2011.

    Article  CAS  Google Scholar 

  • Zhao, H.X., Li, Q., Li, G., Du, Y.: Differential gene expression in response to cold stress in Lepidium apetalum during seedling emergence. — Biol. Plant. 56: 64–70, 2012.

    Article  CAS  Google Scholar 

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Correspondence to A. Caffagni.

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Acknowledgments: The authors thank to the C.M. Rick Tomato Genetics Resource Center, Department of Plant Sciences, University of California, Davis, USA and Dr. Nazareno Acciarri (the CRA-ORA Research Unit for Vegetable Crops, Monsampolo del Tronto, Italy) for providing seeds of 37 and 26 tomato accessions, respectively. We also wish to thank Dr. Fulvia Rizza for her excellent technical assistance in the phenotypic examination of the plants. Authors acknowledge partial support of PRIN2006, the TomANTHO Project of the Italian Ministry of University and Research (MiUR).

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Caffagni, A., Pecchioni, N., Francia, E. et al. Candidate gene expression profiling in two contrasting tomato cultivars under chilling stress. Biol Plant 58, 283–295 (2014). https://doi.org/10.1007/s10535-014-0403-z

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