Biologia plantarum 2014, 58:283-295 | DOI: 10.1007/s10535-014-0403-z

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

A. Caffagni1,*, N. Pecchioni1,2, E. Francia1,2, D. Pagani3, J. Milc1,2
1 Interdepartmental Research Centre BIOGEST-SITEIA, University of Modena and Reggio Emilia, Reggio Emilia, Italy
2 Department of Life Sciences, University of Modena and Reggio Emilia, Reggio Emilia, Italy
3 Genomics Research Centre, Fiorenzuola d'Arda, Italy

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.

Keywords: C2H2-type zinc finger protein; CBF, DREB pathway; ROS-mediated pathway; Solanum lycopersicum
Subjects: temperature - low; C2H2-type zinc finger protein; CBF/DREB pathway; reactive oxygen specied; electrolyte leakage; gene expression; tomato
Species: Solanum lycopersicum

Received: September 11, 2013; Revised: November 7, 2013; Accepted: November 18, 2013; Published: June 1, 2014Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Caffagni, A., Pecchioni, N., Francia, E., Pagani, D., & Milc, J. (2014). Candidate gene expression profiling in two contrasting tomato cultivars under chilling stress. Biologia plantarum, 58(2), 283-295. doi: 10.1007/s10535-014-0403-z.
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)

    • Open full article

    Supplementary files

    Download filebpl-201402-0010_S1.pdf

    File size: 408.79 kB

    Download filebpl-201402-0010_S2.pdf

    File size: 111.69 kB

    References

    1. Alam, B., Jacob, J.: Overproduction of photosynthetic electrons is associated with chilling injury in green leaves. - Photosynthetica 40: 91-95, 2002. Go to original source...
    2. Apel, K., Hirt, H.: Reactive oxygen species: metabolism, oxidative stress, and signal transduction. - Annu. Rev. Plant Biol. 55: 373-399, 2004. Go to original source...
    3. 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.
    4. 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. Go to original source...
    5. 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. Go to original source...
    6. 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. Go to original source...
    7. 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. Go to original source...
    8. 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. Go to original source...
    9. Close, T.J.: Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. - Physiol. Plant. 97: 795-803, 1996. Go to original source...
    10. Close, T.J.: Dehydrins: a commonality in the response of plants to dehydration and low temperature. - Physiol. Plant. 100: 291-296, 1997. Go to original source...
    11. 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. Go to original source...
    12. 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. Go to original source...
    13. 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. Go to original source...
    14. Elizondo, R., Oyanedel, E.: Field testing of tomato chilling tolerance under varying light and temperature conditions. - Chil. J. agr. Res. 70: 552-558, 2010. Go to original source...
    15. 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. Go to original source...
    16. 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. Go to original source...
    17. 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. Go to original source...
    18. 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. Go to original source...
    19. 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.
    20. 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. Go to original source...
    21. 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. Go to original source...
    22. 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. Go to original source...
    23. 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. Go to original source...
    24. 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. Go to original source...
    25. 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. Go to original source...
    26. 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. Go to original source...
    27. Kiełbowicz-Matuk, A.: Involvement of plant C2H2-type zinc finger transcription factors in stress responses. - Plant Sci. 185-186: 78-85, 2012. Go to original source...
    28. 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. Go to original source...
    29. 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. Go to original source...
    30. 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. Go to original source...
    31. 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. Go to original source...
    32. 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. Go to original source...
    33. 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. Go to original source...
    34. 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. Go to original source...
    35. 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. Go to original source...
    36. 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. Go to original source...
    37. 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. Go to original source...
    38. Lyons, J.M.: Chilling injury in plants. - Annu. Rev. Plant Physiol. 24: 445-466, 1973. Go to original source...
    39. 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. Go to original source...
    40. 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. Go to original source...
    41. 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. Go to original source...
    42. 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. Go to original source...
    43. Mittler, R.: Oxidative stress, antioxidants and stress tolerance. - Trends Plant Sci. 7: 405-410, 2002. Go to original source...
    44. Mittler, R., Vanderauwera, S., Gollery, M., Van Breusegem, F.: Reactive oxygen gene network of plants. - Trends Plant Sci. 9: 490-498, 2004. Go to original source...
    45. 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. Go to original source...
    46. 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. Go to original source...
    47. 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. Go to original source...
    48. Neill, S., Desikan, R., Hancock, J.: Hydrogen peroxide signaling. - Curr. Opin. Plant Biol. 5: 388-395, 2002. Go to original source...
    49. 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. Go to original source...
    50. 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. Go to original source...
    51. 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. Go to original source...
    52. 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. Go to original source...
    53. 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. Go to original source...
    54. 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. Go to original source...
    55. 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. Go to original source...
    56. 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. Go to original source...
    57. Raison, J.K., Lyons, J.M.: Chilling injury: a plea for uniform terminology. - Plant Cell Environ. 9: 685-686, 1986. Go to original source...
    58. Rice-Evans, C.A., Miller, N.J., Paganga, G.: Antioxidant properties of phenolic compounds. - Trends Plant Sci. 2: 152-159, 1997. Go to original source...
    59. 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. Go to original source...
    60. 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. Go to original source...
    61. Scott, S.J., Jones, R.A.: Low temperature seed germination of Lycopersicon species evaluated by survival analysis. - Euphytica 31: 869-883, 1982. Go to original source...
    62. 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. Go to original source...
    63. 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. Go to original source...
    64. Somerville, C., Browse, J.: Plant lipids: metabolism, mutants, and membranes. - Science 252: 80-87, 1991. Go to original source...
    65. Tanaka, Y., Sasaki, N., Ohmiya, A.: Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. - Plant J. 54: 733-749, 2008. Go to original source...
    66. The Tomato Genome Consortium: the tomato genome sequence provides insights into fleshy fruit evolution. - Nature 485: 635-641, 2012. Go to original source...
    67. Theocharis, A., Clément, C., Barka, E.A.: Physiological and molecular changes in plants grown at low temperatures. - Planta 235: 1091-1105, 2012. Go to original source...
    68. Thomashow, M.F.: Plant cold acclimation: freezing tolerances genes and regulatory mechanisms. - Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 571-599, 1999. Go to original source...
    69. Thomashow, M.F.: So what's new in the field of plant cold acclimation? Lots! - Plant Physiol. 125: 89-93, 2001. Go to original source...
    70. Thomashow, M.F.: Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. - Plant Physiol. 154: 571-577, 2010. Go to original source...
    71. 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. Go to original source...
    72. 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. Go to original source...
    73. 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. Go to original source...
    74. 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. Go to original source...
    75. 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. Go to original source...
    76. 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. Go to original source...
    77. 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. Go to original source...
    78. 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.
    79. 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.
    80. 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. Go to original source...
    81. 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. Go to original source...
    82. 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. Go to original source...
    83. 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. Go to original source...
    84. 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. Go to original source...
    85. 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. Go to original source...

    Return to the content