Skip to main content
SpringerLink
Log in

Identification of Low Temperature Stress Regulated Transcript Sequences and Gene Families in Italian Cypress

  • Research
  • Published:
Molecular Biotechnology Aims and scope Submit manuscript

Abstract

Cold acclimation is a complex transcriptionally controlled process regulated by many different genes and genic-interactions in plants. The northward spreading of woody species is mainly limited by winter harshness. To increase our knowledge about the biological processes underlying cold acclimation, plants evolved in warmer climates can serve as models. In this work, a Suppression Subtractive Hybridization approach using PCR-select was used to isolate Italian cypress (Cupressus sempervirens L.) transcript sequences putatively expressed under low temperature stress. After assessing the reliability of the subtractive step, a total of 388 clones were selected and sequenced. Following sequence assembly and removal of the redundant cDNAs, 156 unique transcripts were identified and annotated in order to assign them a putative functional class. Most of the identified transcripts were functionally classified pertaining to stress in cellular and chloroplast membranes, which are previously known to be severely damaged by cold treatment. Among the identified functional gene families, the extensively represented ones were dehydrins, early light-inducible proteins, senescence-associated genes and oleosins. The last three gene families were further selected for phylogenetic analysis, with the corresponding protein sequences across the complete genomes of the model plants Populus trichocarpa, Vitis vinifera, Physcomitrella patens, and Arabidopsis thaliana. The relationship with the ortholog sequences coming from these species and their further implications are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Theocharis, A., Clement, C., & Barka, E. A. (2012). Physiological and molecular changes in plants grown at low temperatures. Planta, 235, 1091–1105.

    Article  CAS  Google Scholar 

  2. Hincha, D. K. (2002). Cryoprotectin: A plant lipid-transfer protein homologue that stabilizes membranes during freezing. Philosophical Transactions of the Royal Society of London. Series B, 357, 909–915.

    Article  CAS  Google Scholar 

  3. Yaish, M. W. F., Doxey, A. C., McConkey, B. J., Moffatt, B. A., & Griffith, M. (2006). Cold-active winter rye glucanases with ice-binding capacity. Plant Physiology, 141, 1459–1472.

    Article  CAS  Google Scholar 

  4. Welling, A., & Palva, E. T. (2006). Molecular control of cold acclimation in trees. Physiol Plantarum, 127, 167–181.

    Article  CAS  Google Scholar 

  5. Fernandez, O., Theocharis, A., Bordiec, S., Feil, R., Jacquens, L., Clement, C., et al. (2012). Acclimates grapevine to cold by modulating carbohydrate metabolism. Molecular Plant-Microbe Interactions, 25, 496–504.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. Bies-Etheve, N., Gaubier-Comella, P., Debures, A., Lasserre, E., Jobet, E., Raynal, M., et al. (2008). Inventory, evolution and expression profiling diversity of the LEA (late embryogenesis abundant) protein gene family in Arabidopsis thaliana. Plant Molecular Biology, 67, 107–124.

    Article  CAS  Google Scholar 

  8. Heddad, M., Noren, H., Reiser, V., Dunaeva, M., Andersson, B., & Adamska, I. (2006). Differential expression and localization of early light-induced proteins in Arabidopsis. Plant Physiology, 142, 75–87.

    Article  CAS  Google Scholar 

  9. Degenkolbe, T., Giavalisco, P., Zuther, E., Seiwert, B., Hincha, D. K., & Willmitzer, L. (2012). Differential remodeling of the lipidome during cold acclimation in natural accessions of Arabidopsis thaliana. The Plant Journal, 72, 972–982.

    CAS  Google Scholar 

  10. Mao, D., & Chen, C. (2012). Colinearity and similar expression pattern of rice DREB1 s reveal their functional conservation in the cold-responsive pathway. PLoS ONE, 7, e47275. doi:10.1371/journal.pone.0047275.

    Article  CAS  Google Scholar 

  11. Checker, V. G., Chhibbar, A. K., & Khurana, P. (2012). Stress-inducible expression of barley Hva1 gene in transgenic mulberry displays enhanced tolerance against drought, salinity and cold stress. Transgenic Research, 21, 939–957.

    Article  CAS  Google Scholar 

  12. Perdiguero, P., Barbero, M. C., Cervera, M. T., Soto, A., & Collada, C. (2012). Novel conserved segments are associated with differential expression patterns for Pinaceae dehydrins. Planta, 236, 1863–1874.

    Article  CAS  Google Scholar 

  13. Dauwe, R., Holliday, J. A., Aitken, S. N., & Mansfield, S. D. (2012). Metabolic dynamics during autumn cold acclimation within and among populations of Sitka spruce (Picea sitchensis). New Phytologist, 194, 192–205.

    Article  CAS  Google Scholar 

  14. D’Angeli, S., Falasca, G., Matteucci, M., & Altamura, M. M. (2013). Cold perception and gene expression differ in Olea europaea seed coat and embryo during drupe cold acclimation. New Phytologist, 197, 123–138.

    Article  Google Scholar 

  15. Larcher, W. (2001). Ökophysiologie der Pflanzen: (S. E. Ulmer) ed (p. 302). Stuttgart: Eugen Ulmer.

    Google Scholar 

  16. Bagnoli, F., Vendramin, G. G., Buonamici, A., Doulis, A. G., Gonzalez-Martinez, S. C., La Porta, N., et al. (2009). Is Cupressus sempervirens native in Italy? An answer from genetic and palaeobotanical data. Molecular Ecology, 18, 2276–2286.

    Article  CAS  Google Scholar 

  17. Baldi, P., Muthuchelian, K., & La Porta, N. (2012). Leaf plasticity to light intensity in Italian cypress (Cupressus sempervirens L.): Adaptability of a Mediterranean conifer cultivated in the Alps. Journal of Photochemistry and Photobiology B: Biology, 117, 61–69.

    Article  CAS  Google Scholar 

  18. Zorer, R., Eccel, E., Tognetti, R., & La Porta, N. (2014). A Mediterranean conifer under vegetation shift: Seasonal changes of photochemical activity in Cupressus sempervirens (L.) and evidence of correlation with temperature models. Italian Journal of Agrometeorology, 1, 29–40.

    Google Scholar 

  19. La Porta, N., Bertamini, M., Nedunchezhian, N., Raddi, P., & Muthuchelian, K. (2005). Photoinhibition of photosynthesis in needles of two cypress (Cupressus sempervirens L.) clones. Tree Physiology, 25, 1033–1039.

    Article  Google Scholar 

  20. Weger, H. G., Silim, S. N., & Guy, R. D. (1993). Photosynthetic acclimation to low temperature by western red cedar seedlings. Plant, Cell and Environment, 16, 711–717.

    Article  CAS  Google Scholar 

  21. La Porta, N., Bertamini, M., Nedunchezhian, N., & Muthuchelian, K. (2006). Photosynthetic changes that occur during aging of cypress (Cupressus sempervirens L.) needles. Photosynthetica, 44, 555–560.

    Article  CAS  Google Scholar 

  22. Muthuchelian, K., La Porta, N., Bertamini, M., & Nedunchezhian, N. (2005). Cypress canker induced inhibition of photosynthesis in field grown cypress (Cupressus sempervirens L.) needles. Physiological and Molecular Plant Pathology, 67, 33–39.

    Article  CAS  Google Scholar 

  23. Muthuchelian, K., Bertamini, M., La Porta, N., & Nedunchezhian, N. (2005). Photoinhibition and recovery of photosynthesis in canker-susceptible and resistant needles of cypress (Cupressus sempervirens L.). J. Phytopath., 153, 337–343.

    Article  CAS  Google Scholar 

  24. Zocca, A., Zanini, C., Aimi, A., Frigimelica, G., La Porta, N., & Battisti, A. (2008). Spread of a plant pathogen and associated insect vectors at the northern range margin of cypress (Cupressus sempervirens). Acta Oecologica, 33, 307–313.

    Article  Google Scholar 

  25. Oshlack, A., Robinson, M. D., & Young, M. D. (2010). From RNA-seq reads to differential expression results. Genome Biology, 11, 220.

    Article  CAS  Google Scholar 

  26. Gu, R. S., Fonseca, S., Puskas, L. G., Hackler, L., Zvara, A., Dudits, D., & Pais, M. S. (2004). Transcript identification and profiling during salt stress and recovery of Populus euphratica. Tree Physiology, 24, 265–276.

    Article  CAS  Google Scholar 

  27. Yakovlev, I. A., Fossdal, C. G., Johnsen, O., Junttila, O., & Skroppa, T. (2006). Analysis of gene expression during bud burst initiation in Norway spruce via ESTs from subtracted cDNA libraries. Tree Genetics and Genomes, 2, 39–52.

    Article  Google Scholar 

  28. Pedron, L., Baldi, P., Hietala, A. M., & La Porta, N. (2009). Genotype-specific regulation of cold-responsive genes in cypress (Cupressus sempervirens L.). Gene, 437, 45–53.

    Article  CAS  Google Scholar 

  29. Xu, L., Yuan, Y., Zhang, L., Wan, L., Zheng, Y., Zhou, P., & Li, D. (2011). Identification and characterization of differential gene expression in the mesocarp and kernel of oil palm nuts using suppression subtractive hybridization. Tree Genetics and Genomes, 7, 999–1010.

    Article  Google Scholar 

  30. La Porta, N., Battisti, A., & Raddi, P. (2005). Ecological assessment and sustainable management of cypress under climate change conditions in the Italian Alps. International Forest Review, 7(5), 82.

    Google Scholar 

  31. Moser, C., Gatto, P., Moser, M., Pindo, M., & Velasco, R. (2004). Isolation of functional RNA from small amounts of different grape and apple tissues. Molecular Biotechnology, 26, 95–99.

    Article  CAS  Google Scholar 

  32. Simon, N., Campbell, L., Ornolfsdottir, E., Groben, R., Guillou, L., Lange, M., & Medlin, L. K. (2000). Oligonucleotide probes for the identification of three algal groups by dot blot and fluorescent whole-cell hybridization. Journal of Eukaryotic Microbiology, 47, 76–84.

    Article  CAS  Google Scholar 

  33. Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.

    Article  CAS  Google Scholar 

  34. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.

    Article  CAS  Google Scholar 

  35. Huang, X., & Madan, A. (1999). CAP3: A DNA sequence assembly program. Genome Research, 9, 868–877.

    Article  CAS  Google Scholar 

  36. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., et al. (2000). Gene ontology: Tool for the unification of biology. The Gene Ontology Consortium. Nat Genet, 25, 25–29.

    CAS  Google Scholar 

  37. Schiex, T., Gouzy, J., Moisan, A., & De Oliveira, Y. (2003). FrameD: A flexible program for quality check and gene prediction in prokaryotic genomes and noisy matured eukaryotic sequences. Nucleic Acids Research, 31, 3738–3741.

    Article  CAS  Google Scholar 

  38. Simkin, A. J., Qian, T., Caillet, V., Michoux, F., Ben Amor, M., Lin, C., et al. (2006). Oleosin gene family of Coffea canephora: Quantitative expression analysis of five oleosin genes in developing and germinating coffee grain. Journal of Plant Physiology, 163, 691–708.

    Article  CAS  Google Scholar 

  39. Peng, Y., Lin, W., Wei, H., Krebs, S. L., & Arora, R. (2008). Phylogenetic analysis and seasonal cold acclimation-associated expression of early light-induced protein genes of Rhododendron catawbiense. Physiologia Plantarum, 132, 44–52.

    CAS  Google Scholar 

  40. Palmé, A. E., Pyhäjärvi, T., Wachowiak, W., & Savolainen, O. (2009). Selection on nuclear genes in a Pinus phylogeny. Molecular Biology and Evolution, 26, 893–905.

    Article  Google Scholar 

  41. Thomashow, M. F. (1999). Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 571–599.

    Article  CAS  Google Scholar 

  42. Wang, Y. Q., Shen, J. K., Berglund, T., Ohlsson, A. B., Tang, X. F., Zhou, Z. K., et al. (2010). Analysis of expressed sequence tags from Ginkgo mature foliage in China. Tree Genetics and Genomes, 6, 357–365.

    Article  Google Scholar 

  43. Ujino-Ihara, T., Kanamori, H., Yamane, H., Taguchi, Y., Namiki, N., Mukai, Y., et al. (2005). Comparative analysis of expressed sequence tags of conifers and angiosperms reveals sequences specifically conserved in conifers. Plant Molecular Biology, 59, 895–907.

    Article  CAS  Google Scholar 

  44. Mishra, S., Srivastava, S., & Nautiyal, C. S. (2014). Differential gene expression profile in Pseudomonas putida NBRIC19-treated wheat (Triticum aestivum) plants subjected to biotic stress of Parthenium hysterophorus. Molecular Biology Reports, 41, 1385–1399.

    Article  CAS  Google Scholar 

  45. Fan, Q. J., Yan, F. X., Qiao, G., Zhang, B. X., & Wen, X. P. (2014). Identification of differentially-expressed genes potentially implicated in drought response in pitaya (Hylocereus undatus) by suppression subtractive hybridization and cDNA microarray analysis. Gene, 533, 322–331.

    Article  CAS  Google Scholar 

  46. Kaplan, F., Kopka, J., Sung, D. Y., Zhao, W., Popp, M., Porat, R., & Guy, C. L. (2007). Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. The Plant Journal, 50, 967–981.

    Article  CAS  Google Scholar 

  47. Purdy, S. J., Bussell, J. D., Nunn, C. P., & Smith, S. M. (2013). Leaves of the Arabidopsis maltose exporter1 mutant exhibit a metabolic profile with features of cold acclimation in the warm. PLoS One, 8, e79412. doi:10.1371/journal.pone.0079412.

    Article  CAS  Google Scholar 

  48. Lee, J. H., Yu, D. J., Kim, S. J., Choi, D., & Lee, H. J. (2012). Intraspecies differences in cold hardiness, carbohydrate content and beta-amylase gene expression of Vaccinium corymbosum during cold acclimation and deacclimation. Tree Physiology, 32, 1533–1540.

    Article  CAS  Google Scholar 

  49. Ito, A., Sugiura, T., Sakamoto, D., & Moriguchi, T. (2013). Effects of dormancy progression and low-temperature response on changes in the sorbitol concentration in xylem sap of Japanese pear during winter season. Tree Physiology, 33, 398–408.

    Article  Google Scholar 

  50. Secchi, F., & Zwieniecki, M. A. (2012). Analysis of xylem sap from functional (non-embolized) and nonfunctional (embolized) vessels of Populus nigra: Chemistry of refilling. Plant Physiology, 160, 955–964.

    Article  CAS  Google Scholar 

  51. Riikonen, J., Kontunen-Soppela, S., Vapaavuori, E., Tervahauta, A., Tuomainen, M., & Oksanen, E. (2013). Carbohydrate concentrations and freezing stress resistance of silver birch buds grown under elevated temperature and ozone. Tree Physiology, 33, 311–319.

    Article  CAS  Google Scholar 

  52. Boneh, U., Biton, I., Schwartz, A., & Ben-Ari, G. (2012). Characterization of the ABA signal transduction pathway in Vitis vinifera. Plant Science, 187, 89–96.

    Article  CAS  Google Scholar 

  53. Mittler, R. (2006). Abiotic stress, the field environment and stress combination. Trends in Plant Science, 11, 15–19.

    Article  CAS  Google Scholar 

  54. Mao, X., Chen, S., Li, A., Zhai, C., & Jing, R. (2014). Novel NAC transcription factor TaNAC67 confers enhanced multi-abiotic stress tolerances in Arabidopsis. PLoS One, 9, e84359. doi:10.1371/journal.pone.0084359.

    Article  Google Scholar 

  55. Baldi, P., Pedron, L., Hietala, A. M., & La Porta, N. (2011). Cold tolerance in cypress (Cupressus sempervirens L.): A physiological and molecular study. Tree Genetics and Genomes, 7, 79–90.

    Article  Google Scholar 

  56. Uemura, M., Tominaga, Y., Nakagawara, C., Shigematsu, S., Minami, A., & Kawamura, Y. (2006). Responses of the plasma membrane to low temperatures. Physiologia Plantarum, 126, 81–89.

    Article  CAS  Google Scholar 

  57. Kazemi Shahandashti, S. S., Maali Amiri, R., Zeinali, H., & Ramezanpour, S. S. (2013). Change in membrane fatty acid compositions and cold-induced responses in chickpea. Molecular Biology Reports, 40, 893–903.

    Article  CAS  Google Scholar 

  58. Abdrakhamanova, A., Wang, Q. Y., Khokhlova, L., & Nick, P. (2003). Is microtubule disassembly a trigger for cold acclimation? Plant and Cell Physiology, 44, 676–686.

    Article  CAS  Google Scholar 

  59. Kosova, K., Vitamvas, P., & Prasil, I. T. (2007). The role of dehydrins in plant response to cold. Biologia Plantarum, 51, 601–617.

    Article  CAS  Google Scholar 

  60. Sandve, S. R., Kosmala, A., Rudi, H., Fjellheim, S., Rapacz, M., Yamada, T., & Rognli, O. A. (2011). Molecular mechanisms underlying frost tolerance in perennial grasses adapted to cold climates. Plant Science, 180, 69–77.

    Article  CAS  Google Scholar 

  61. La Porta, N., Bertamini, M., Nedunchezhian, N., & Muthuchelian, K. (2004). High irradiance induced changes on photosystem 2 in young and mature needles of cypress (Cupressus sempervirens L.). Photosynthetica, 42, 263–271.

    Article  Google Scholar 

  62. Bascunan-Godoy, L., Sanhueza, C., Cuba, M., Zuniga, G. E., Corcuera, L. J., & Bravo, L. A. (2012). Cold-acclimation limits low temperature induced photoinhibition by promoting a higher photochemical quantum yield and a more effective PSII restoration in darkness in the Antarctic rather than the Andean ecotype of Colobanthus quitensis Kunt Bartl (Cariophyllaceae). BMC Plant Biology, 12, 114.

    Article  CAS  Google Scholar 

  63. Nylander, M., Svensson, J., Palva, E. T., & Welin, B. V. (2001). Stress-induced accumulation and tissue-specific localization of dehydrins in Arabidopsis thaliana. Plant Molecular Biology, 45, 263–279.

    Article  CAS  Google Scholar 

  64. Rorat, T. (2006). Plant dehydrins-tissue location, structure and function. Cellular & Molecular Biology Letters, 11, 536–556.

    Article  CAS  Google Scholar 

  65. Yang, Y., He, M., Zhu, Z., Li, S., Xu, Y., Zhang, C., et al. (2012). Identification of the dehydrin gene family from grapevine species and analysis of their responsiveness of various forms of abiotic and biotic stress. BMC Plant Biology, 54, 743–753.

    Google Scholar 

  66. Hanin, M., Brini, F., Ebel, E., Toda, Y., Takeda, S., & Masmoudi, K. (2011). Plant dehydrins and stress tolerance: Versatile proteins for complex mechanisms. Plant Signaling & Behavior, 6, 1503–1509.

    Article  CAS  Google Scholar 

  67. Adamska, I., & Kloppstech, K. (1991). Evidence for an association of the early light-inducible protein (ELIP) of pea with photosystem II. Plant Molecular Biology, 16, 209–223.

    Article  CAS  Google Scholar 

  68. Hutin, C., Nussaume, L., Moise, N., Moya, I., Kloppstech, K., & Havaux, M. (2003). Early light-induced proteins protect Arabidopsis from photooxidative stress. Proceedings of the National Academy of Sciences of the United States of America, 100, 4921–4926.

    Article  CAS  Google Scholar 

  69. Zarter, C. R., Adams, W. W, 3rd, Ebbert, V., Adamska, I., Jansson, S., & Demmig-Adams, B. (2006). Winter acclimation of PsbS and related proteins in the evergreen Arctostaphylos uva-ursi as influenced by altitude and light environment. Plant, Cell and Environment, 29, 869–878.

    Article  CAS  Google Scholar 

  70. Rossini, S., Casazza, A. P., Engelmann, E. C., Havaux, M., Jennings, R. C., & Soave, C. (2006). Suppression of both ELIP1 and ELIP2 in Arabidopsis does not affect tolerance to photoinhibition and photooxidative stress. Plant Physiology, 141, 1264–1273.

    Article  CAS  Google Scholar 

  71. Zhou, C. G. S. (2009). Senescence. In D. M. Pua EC (Ed.), Plant developmental biology: Biotechnological perspectives (pp. 151–169). Berlin: Springer.

    Google Scholar 

  72. Guo, Y., & Gan, S. S. (2012). Convergence and divergence in gene expression profiles induced by leaf senescence and 27 senescence-promoting hormonal, pathological and environmental stress treatments. Plant, Cell and Environment, 35, 644–655.

    Article  CAS  Google Scholar 

  73. Zhao, L., Zhang, H., Zhang, B., Bai, X., & Zhou, C. (2012). Physiological and molecular changes of detached wheat leaves in responding to various treatments. Journal of Integrative Plant Biology, 54, 567–576.

    Article  CAS  Google Scholar 

  74. Lim, P. O., Kim, H. J., & Nam, H. G. (2007). Leaf senescence. Annual Review of Plant Biology, 58, 115–136.

    Article  CAS  Google Scholar 

  75. Shimada, T. L., Shimada, T., Takahashi, H., Fukao, Y., & Hara-Nishimura, I. (2008). A novel role for oleosins in freezing tolerance of oilseeds in Arabidopsis thaliana. The Plant Journal, 55, 798–809.

    Article  CAS  Google Scholar 

  76. Tanaka, H., Osakabe, Y., Katsura, S., Mizuno, S., Maruyama, K., Kusakabe, K., et al. (2012). Abiotic stress-inducible receptor-like kinases negatively control ABA signaling in Arabidopsis. The Plant Journal, 70, 599–613.

    Article  CAS  Google Scholar 

  77. Xue-Xuan, X., Hong-Bo, S., Yuan-Yuan, M., Gang, X., Jun-Na, S., Dong-Gang, G., & Cheng-Jiang, R. (2010). Biotechnological implications from abscisic acid (ABA) roles in cold stress and leaf senescence as an important signal for improving plant sustainable survival under abiotic-stressed conditions. Critical Reviews in Biotechnology, 30, 222–230.

    Article  CAS  Google Scholar 

  78. Huang, G. T., Ma, S. L., Bai, L. P., Zhang, L., Ma, H., Jia, P., et al. (2012). Signal transduction during cold, salt, and drought stresses in plants. Molecular Biology Reports, 39, 969–987.

    Article  Google Scholar 

  79. Tzen, J. T., Lai, Y. K., Chan, K. L., & Huang, A. H. (1990). Oleosin isoforms of high and low molecular weights are present in the oil bodies of diverse seed species. Plant Physiology, 94, 1282–1289.

    Article  CAS  Google Scholar 

  80. Kim, H. U., Hsieh, K., Ratnayake, C., & Huang, A. H. (2002). A novel group of oleosins is present inside the pollen of Arabidopsis. Journal of Biological Chemistry, 277, 22677–22684.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Dr. Paolo Raddi, Mr. Vincenzo Di Lonardo, and Dr. Roberto Danti (IPP-CNR, Florence, Italy) who kindly supplied the selected cypress genotypes used in the experiments. We gratefully thank also Mr. Federico Piccirillo (Montemagno Resource Inc.), Mr. Emanuel Endrizzi and Dr. Luca Pedron (Fondazione Edmund Mach) for the technical assistance in the laboratory and field and Mrs. Tessa Say for the useful English corrections. The authors acknowledge the two anonymous reviewers and the editor for the appreciated constructive comments and suggestions which have helped to improve the manuscript. This work is part of the project ECOCYPRE (Ecological assessment and sustainable managements of cypress in the landscape of Trentino) that was funded to Dr. Nicola La Porta by the Provincia autonoma di Trento through Grant No. 437.

Author information

Authors and Affiliations

  1. IASMA Research and Innovation Centre, Fondazione Edmund Mach (FEM), Via E. Mach 1, 38010, San Michele all’Adige, Trento, Italy

    Nicola La Porta, Gaurav Sablok, Paolo Fontana, Emilio Potenza & Paolo Baldi

  2. MOUNTFOR Project Centre, European Forest Institute, Via E. Mach 1, 38010, San Michele all’Adige, Trento, Italy

    Nicola La Porta

  3. Plant Functional Biology and Climate Change Cluster (C3), University of Technology Sydney, PO Box 123, Broadway, NSW, 2007, Australia

    Gaurav Sablok

  4. Trees and Timber Institute (IVALSA), National Research Council (CNR), Via Madonna del Piano 10, 50019, Sesto Fiorentino, Firenze, Italy

    Giovanni Emilliani & Alessio Giovannelli

  5. The Norwegian Forest and Landscape Institute, Høgskoleveien 8, Pb. 115, 1432, Ås, Norway

    Ari M. Hietala

Authors
  1. Nicola La Porta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gaurav Sablok
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Giovanni Emilliani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ari M. Hietala
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alessio Giovannelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Paolo Fontana
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Emilio Potenza
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Paolo Baldi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nicola La Porta.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 257 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

La Porta, N., Sablok, G., Emilliani, G. et al. Identification of Low Temperature Stress Regulated Transcript Sequences and Gene Families in Italian Cypress. Mol Biotechnol 57, 407–418 (2015). https://doi.org/10.1007/s12033-014-9833-2

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12033-014-9833-2

Keywords

Search

Navigation