Functional characterization of two almond C-repeat-binding factors involved in cold response

Tree Physiology

Volumn 32, Issue 9, 2012, Pages 1113-1128

  Barros, Pedro M ^a,b   Gonçalves, Nuno ^a,b   Saibo, Nelson J M ^a,b   Margarida Oliveira, M ^a,b  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b IBET   (Portugal)

Author keywords

bin mapping; CBF transcription factors; Dehydrin1; gene expression; Prunus dulcis; transactivation

Indexed keywords

ABSCISIC ACID; DEHYDRIN PROTEINS, PLANT; DNA BINDING PROTEIN; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

ABSCISIC ACID; ACCLIMATION; ADAPTATION; CHEMICAL BINDING; CLIMATE CONDITIONS; DECIDUOUS TREE; DROUGHT; FRUIT; FUNCTIONAL ROLE; GENE EXPRESSION; GENETIC VARIATION; LIFE HISTORY TRAIT; LOW TEMPERATURE; PHYSIOLOGICAL RESPONSE; SHOOT GROWTH;

ACCLIMATIZATION; AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CHROMOSOME MAP; COLD; DEHYDRATION; DNA SEQUENCE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; PLANT; PROMOTER REGION; PROTEIN MOTIF; PRUNUS; QUANTITATIVE TRAIT LOCUS; SEQUENCE ALIGNMENT; TRANSCRIPTION INITIATION;

ABSCISIC ACID; ACCLIMATIZATION; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ARABIDOPSIS; BASE SEQUENCE; CHROMOSOME MAPPING; COLD TEMPERATURE; DEHYDRATION; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, PLANT; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT PROTEINS; PLANT SHOOTS; PROMOTER REGIONS, GENETIC; PRUNUS; QUANTITATIVE TRAIT LOCI; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

PRUNUS DULCIS;

EID: 84866390475     PISSN: 0829318X     EISSN: 17584469     Source Type: Journal    
DOI: 10.1093/treephys/tps067     Document Type: Article

References (85)

1. Alonso, J.M., J.M. Ansón, M.T. Espiau and R. Socias i Company. 2005. Determination of endodormancy break in almond flower buds by a correlation model using the average temperature of different day intervals and its application to the estimation of chill and heat requirements and blooming date. J. Am. Soc. Hort. Sci. 130:308-318.
2. Anthony, R.G., R. Henriques, A. Helfer, et al. 2004. A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J. 23:572-581.
3. Artlip, T.S., A.M. Callahan, C.L. Bassett and M.E. Wisniewski. 1997. Seasonal expression of a dehydrin gene in sibling deciduous and evergreen genotypes of peach (Prunus persica [L.] Batsch). Plant Mol. Biol. 33:61-70.
4. Arús, P., T. Gradziel, M.M. Oliveira and R. Tao. 2009. Genomics of almond. In Plant Genetics and Genomics: Crops and Models. Vol. 6-Genetics and Genomics of Rosaceae. Eds. K.M. Folta and S.E. Gardiner. Springer, New York, pp 187-219.
5. Badawi, M., J. Danyluk, B. Boucho, M. Houde and F. Sarhan. 2007. The CBF gene family in hexaploid wheat and its relationship to the phylogenetic complexity of cereal CBFs. Mol. Genet. Genomics 277:533-554.
6. Baldwin, B.D., M.S. Bandara and K.K. Tanino. 1998. Is tissue culture a viable system with which to examine environmental and hormonal regulation of cold acclimation in woody plants? Physiol. Plant. 102:201-209.
7. Barros, P.M., N. Gonçalves, N.J.M. Saibo, M.M. Oliveira. 2012. Cold acclimation and floral development in almond bud break: insights into the regulatory pathways. J. Exp. Bot. Epub ahead of print. doi:10.1093/jxb/ers144.
8. Bassett, C.L., M.E. Wisniewski, T.S. Artlip, J.L. Norelli and R.E. Farrell. 2006. Global analysis of genes regulated by low temperature and photoperiod in peach bark. J. Am. Soc. Hortic. Sci. 131:551-563.
9. Bassett, C.L., M.E. Wisniewski, T.S. Artlip, G. Richart, J.L. Norelli and R.E. Farrell. 2009. Comparative expression and transcript initiation of three peach dehydrin genes. Planta 230:107-118.
10. Bekman, E.P., N.J.M. Saibo, A. Di Cataldo, A.P. Regalado, C.P. Ricardo and C. Rodrigues-Pousada. 2000. Differential expression of four genes encoding 1-aminocyclopropane-1-carboxylate synthase in Lupinus albus during germination, and in response to indole-3-acetic acid and wounding. Planta 211:663-672.
11. Benedict, C., J.S. Skinner, R. Meng, Y. Chang, R. Bhalerao, N.P.A. Huner, C.E. Finn, T.H.H. Chen and V. Hurry. 2006. The CBF1-dependent low temperature signalling pathway, regulon and increase in freeze tolerance are conserved in Populus spp. Plant Cell Environ. 29:1259-1272.
12. Bieniawska, Z., C. Espinoza, A. Schlereth, R. Sulpice, D.K. Hincha and M.A. Hannah. 2008. Disruption of the Arabidopsis circadian clock is responsible for extensive variation in the cold-responsive transcriptome. Plant Physiol. 147:263-279.
13. Borson, N.D., W.L. Salo and L.R. Drewes. 1992. A lock-docking oligo(dT) primer for 5′ and 3′ RACE PCR. Genome Res. 2:144-148.
14. Carvallo, M.A., M.-T. Pino, Z. Jeknic, C. Zou, C.J. Doherty, S.H. Shiu, T.H.H. Chen and M.F. Thomashow. 2011. A comparison of the low temperature transcriptomes and CBF regulons of three plant species that differ in freezing tolerance: Solanum commersonii, Solanum tuberosum and Arabidopsis thaliana. J. Exp. Bot 62:3807-3819.
15. Cellier, F., G. Conéjéro and F. Casse. 2000. Dehydrin transcript fluctuations during a day/night cycle in drought-stressed sunflower. J. Exp. Bot. 51:299-304.
16. Champ, K.I., V.J. Febres and G.A. Moore. 2007. The role of CBF transcriptional activators in two Citrus species (Poncirus and Citrus) with contrasting levels of freezing tolerance. Physiol. Plant. 129:529-541.
17. Chang, W.-C., T.-Y. Lee, H.-D. Huang, H.-Y. Huang and R.-L. Pan. 2008. PlantPAN: Plant promoter analysis navigator, for identifying combinatorial cis-regulatory elements with distance constraint in plant gene groups. BMC Genomics 9:561.
18. Chinnusamy, V., M. Ohta, S. Kanrar, B.-H. Lee, X. Hong, M. Agarwal and J.-K. Zhu. 2003. ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev. 17:1043-1054.
19. Church, G.M. and W. Gilbert. 1984. Genomic sequencing. Proc. Natl Acad. Sci. USA 81:1991-1995.
20. Dirlewanger, E., A. Moing, C. Rothan, L. Svanella, V. Pronier, A. Guye, C. Plomion and R. Monet. 1999. Mapping QTLs controlling fruit quality in peach (Prunus persica (L.) Batsch). Theor. Appl. Genet. 98:18-31.
21. Druart, N., A. Johansson, K. Baba, et al. 2007. Environmental and hormonal regulation of the activity-dormancy cycle in the cambial meristem involves stage-specific modulation of transcriptional and metabolic networks. Plant J. 50:557-573.
22. Dubouzet, J.G., Y. Sakuma, Y. Ito, M. Kasuga, E.G. Dubouzet, S. Miura, M. Seki, K. Shinozaki and K. Yamaguchi-Shinozaki. 2003. OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt-and cold-responsive gene expression. Plant J. 33:751-763.
23. El Kayal, W., M. Navarro, G. Marque, G. Keller, C. Marque and C. Teulieres. 2006. Expression profile of CBF-like transcriptional factor genes from Eucalyptus in response to cold. J. Exp. Bot. 57:2455-2469.
24. Fan, S., D.G. Bielenberg, T.N. Zhebentyayeva, G.L. Reighard, W.R. Okie, D. Holland and A.G. Abbott. 2010. Mapping quantitative trait loci associated with chilling requirement, heat requirement and bloom date in peach (Prunus persica). New Phytol. 185:917-930.
25. Figueiredo, D.D., P.M. Barros, A.M. Cordeiro, T. Serra, T. Lourenço, S. Chander, M.M. Oliveira and N.J.M. Saibo. 2012. Seven zinc finger transcription factors are novel regulators of the stress responsive gene OsDREB1B. J. Exp. Bot. 63:3643-3656.
26. Fowler, D.B., G. Breton, A.E. Limin, S. Mahfoozi and F. Sarhan. 2001. Photoperiod and temperature interactions regulate low-temperatureinduced gene expression in barley. Plant Physiol. 127:1676-1681.
27. Fowler, S.G., D. Cook and M.F. Thomashow. 2005. Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol. 137:961-968.
28. Franklin, K.A. and G.C. Whitelam. 2007. Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nat. Genet. 39:1410-1413.
29. Frohman, M.A., M.K. Dush and G.R. Martin. 1988. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc. Natl Acad. Sci. USA 85:8998-9002.
30. Gamboa, M.C., S. Rasmussen-Poblete, P.D.T. Valenzuela and E. Krauskopf. 2007. Isolation and characterization of a cDNA encoding a CBF transcription factor from E. globulus. Plant Physiol. Biochem. 45:1-5.
31. Gao, M.J., G. Allard, L. Byass, A.M. Flanagan and J. Singh. 2002. Regulation and characterization of four CBF transcription factors from Brassica napus. Plant Mol. Biol. 49:459-471.
32. Garcia-Bañuelos, M.L., A.A. Gardea, J.J. Winzerling and L. Vazquez-Moreno. 2009. Characterization of a midwinter-expressed dehydrin (DHN) gene from apple trees (Malus domestica). Plant Mol. Biol. Rep. 27:476-487.
33. Gilmour, S.J., D.G. Zarka, E.J. Stockinger, M.P. Salazar, J.M. Houghton and M.F. Thomashow. 1998. Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J. 16:433-442.
34. Hannah, M.A., D. Wiese, S. Freund, O. Fiehn, A.G. Heyer and D.K. Hincha. 2006. Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiol. 142:98-112.
35. Higo, K., Y. Ugawa, M. Iwamoto and T. Korenaga. 1999. Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res. 27:297-300.
36. Howad, W., T. Yamamoto, E. Dirlewanger, et al. 2005. Mapping with a few plants: using selective mapping for microsatellite saturation of the Prunus reference map. Genetics 171:1305-1309.
37. Jaglo-Ottosen, K.R., S.J. Gilmour, D.G. Zarka, O. Schabenberger and M.F. Thomashow. 1998. Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104-106.
38. Jefferson, R.A., T.A. Kavanagh and M.W. Bevan. 1987. GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6:3901-3907.
39. Karimi, M., D. Inzé and A. Depicker. 2002. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant. Sci. 7:193-195.
40. Kidokoro, S., K. Maruyama, K. Nakashima, et al. 2009. The phytochrome-interacting factor PIF7 negatively regulates DREB1 expression under circadian control in Arabidopsis. Plant Physiol. 151:2046-2057.
41. Kitashiba, H., T. Ishizaka, K. Isuzugawa, K. Nishimura and T. Suzuki. 2004. Expression of a sweet cherry DREB1/CBF ortholog in Arabidopsis confers salt and freezing tolerance. J. Plant Physiol. 161:1171-1176.
42. Knight, H., D.G. Zarka, H. Okamoto, M.F. Thomashow and M.R. Knight. 2004. Abscisic acid induces CBF gene transcription and subsequent induction of cold-regulated genes via the CRT promoter element. Plant Physiol. 135:1710-1717.
43. Larkin, M.A., G. Blackshields, N.P. Brown, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
44. Levitt, J. 1980. Responses of plants to environmental stresses: chilling, freezing, and high temperature stresses. Academic Press, New York, 698 p.
45. Liu, Q., M. Kasuga, Y. Sakuma, H. Abe, S. Miura, K. Yamaguchi-Shinozaki and K. Shinozaki. 1998. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought-and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391-406.
46. Martínez-García, J.F., E. Huq and P.H. Quail. 2000. Direct targeting of light signals to a promoter element-bound transcription factor. Science 288:859-863.
47. Martins, M., R. Tenreiro and M.M. Oliveira. 2003. Genetic relatedness of Portuguese almond cultivars assessed by RAPD and ISSR markers. Plant Cell Rep. 22:71-78.
48. Mathur, J. and C. Koncz. 1998. PEG-mediated protoplast transformation with naked DNA. Methods Mol. Biol. 82:267-276.
49. Medina, J., R. Catalá and J. Salinas. 2011. The CBFs: three Arabidopsis transcription factors to cold acclimate. Plant Sci. 180:3-11.
50. Metzger, J.D. 1996. A physiological comparison of vernalization and dormancy chilling requirement. In Plant Dormancy: Physiology, Biochemistry and Molecular Biology. Ed. G.A. Lang. CAB International, New York, pp. 147-155.
51. Miguel, C.M., P. Druart and M.M. Oliveira. 1996. Shoot regeneration from adventitious buds induced on juvenile and adult almond (Prunus dulcis Mill.) explants. In Vitro Cell. Dev. Plant 32:148-153.
52. Nakano, T., K. Suzuki, T. Fujimura and H. Shinshi. 2006. Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol. 140:411-432.
53. Nakashima, K. and K. Yamaguchi-Shinozaki. 2006. Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Physiol. Plant. 126:62-71.
54. Natali, L., T. Giordani, B. Lercari, P. Maestrini, R. Cozza, T. Pangaro, P. Vernieri, F. Martinelli and A. Cavallini. 2007. Light induces expression of a dehydrin-encoding gene during seedling de-etiolation in sunflower (Helianthus annuus L.). J. Plant Physiol. 164:263-273.
55. Navarro, M., G. Marque, C. Ayax, G. Keller, J.P. Borges, C. Marque and C. Teulières. 2009. Complementary regulation of four Eucalyptus CBF genes under various cold conditions. J. Exp. Bot. 60:2713-2724.
56. Ochman, H., A.S. Gerber and D.L. Hartl. 1988. Genetic applications of an inverse polymerase chain reaction. Genetics 120:621-623.
57. Ohno, R., S. Takumi and C. Nakamura. 2003. Kinetics of transcript and protein accumulation of a low-molecular-weight wheat LEA D-11 dehydrin in response to low temperature. J. Plant Physiol. 160:193-200.
58. Panta, G.R., M.W. Rieger and L.J. Rowland. 2001. Effect of cold and drought stress on blueberry dehydrin accumulation. J. Hortic. Sci. Biotech. 76:549-556.
59. Polashock, J.J., R. Arora, Y. Peng, D. Naik and L.J. Rowland. 2010. Functional identification of a C-repeat binding factor transcriptional activator from blueberry associated with cold acclimation and freezing tolerance. J. Am. Soc. Hortic. Sci 135:40-48.
60. Puhakainen, T., C. Li, M. Boije-Malm, J. Kangasjärvi, P. Heino and E.T. Palva. 2004. Short-day potentiation of low temperature-induced gene expression of a C-repeat-binding factor-controlled gene during cold acclimation in silver birch. Plant Physiol. 136:4299-4307.
61. Qin, F., Y. Sakuma, J. Li, Q. Liu, Y.Q. Li, K. Shinozaki and K. Yamaguchi-Shinozaki. 2004. Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol. 45:1042-1052.
62. Rorat, T. 2006. Plant dehydrins-tissue location, structure and function. Cell. Mol. Biol. Lett. 11:536-556.
63. Rushton, D.L., P. Tripathi, R.C. Rabara, et al. 2011. WRKY transcription factors: key components in abscisic acid signalling. Plant. Biotechnol. J. 10:2-11.
64. Sambrook, J., E.F. Fritsch and T. Maniatis. 1989. Molecular cloning: a laboratory manual. 2nd edn. Cold Spring Harbor, New York.
65. Schrader, J., R. Moyle, R. Bhalerao, M. Hertzberg, J. Lundeberg, P. Nilsson and R.P. Bhalerao. 2004. Cambial meristem dormancy in trees involves extensive remodelling of the transcriptome. Plant J. 40:173-187.
66. Shinwari, Z.K., K. Nakashima, S. Miura, M. Kasuga, M. Seki, K. Yamaguchi-Shinozaki and K. Shinozaki. 1998. An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. Biochem. Biophys. Res. Commun. 250:161-170.
67. Socias i Company, R. and A.J. Felipe. 1992. Almond: a diverse germplasm. HortScience 27:718-863.
68. Stockinger, E.J., S.J. Gilmour and M.F. Thomashow. 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.
69. Tamura, K., J. Dudley, M. Nei and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
70. Tanino, K.K., L. Kalcsits, S. Silim, E. Kendall and G.R. Gray. 2010. Temperature-driven plasticity in growth cessation and dormancy development in deciduous woody plants: a working hypothesis suggesting how molecular and cellular function is affected by temperature during dormancy induction. Plant Mol. Biol. 73:49-65.
71. Thomashow, M.F. 1999. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Phys. 50:571-599.
72. Weiser, C.J. 1970. Cold resistance and injury in woody plants: knowledge of hardy plant adaptations to freezing stress may help us to reduce winter damage. Science 169:1269-1278.
73. Welling, A. and E.T. Palva. 2006. Molecular control of cold acclimation in trees. Physiol. Plant. 127:167-181.
74. Welling, A. and E.T. Palva. 2008. Involvement of CBF transcription factors in winter hardiness in birch. Plant Physiol. 147:1199-1211.
75. Welling, A., P. Rinne, A. Viherä-Aarnio, S. Kontunen-Soppela, P. Heino and E.T. Palva. 2004. Photoperiod and temperature differentially regulate the expression of two dehydrin genes during overwintering of birch (Betula pubescens Ehrh.). J. Exp. Bot. 55:507-516.
76. Wisniewski, M., R. Webb, R. Balsamo, T.J. Close, X.-M. Yu and M. Griffith. 1999. Purification, immunolocalization, cryoprotective, and antifreeze activity of PCA60: a dehydrin from peach (Prunus persica). Physiol. Plant. 105:600-608.
77. Wisniewski, M., J. Norelli, C. Bassett, T. Artlip and D. Macarisin. 2011. Ectopic expression of a novel peach (Prunus persica) CBF transcription factor in apple (Malus x domestica) results in short-day induced dormancy and increased cold hardiness. Planta 233:971-983.
78. Wisniewski, M.E., C.L. Bassett, J. Renaut, R. Farrell, T. Tworkoski and T.S. Artlip. 2006. Differential regulation of two dehydrin genes from peach (Prunus persica) by photoperiod, low temperature and water deficit. Tree Physiol. 26:575-584.
79. Xiao, H., M. Siddiqua, S. Braybrook and A. Nassuth. 2006. Three grape CBF/DREB1 genes respond to low temperature, drought and abscisic acid. Plant Cell Environ. 29:1410-1421.
80. Xiao, H., E.A.R. Tattersall, M.K. Siddiqua, G.R. Cramer and A. Nassuth. 2008. CBF4 is a unique member of the CBF transcription factor family of Vitis vinifera and Vitis riparia. Plant Cell Environ. 31:1-10.
81. Yamaguchi-Shinozaki, K. and K. Shinozaki. 2006. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 57:781-803.
82. Yamane, H., Y. Kashiwa, T. Ooka, R. Tao and K. Yonemori. 2008. Suppression subtractive hybridization and differential screening reveals endodormancy-associated expression of an SVP/AGL24-type MADS-box gene in lateral vegetative buds of Japanese apricot. J. Am. Soc. Hortic. Sci. 133:708-716.
83. Yang, W., X.D. Liu, X.J. Chi, et al. 2011. Dwarf apple MbDREB1 enhances plant tolerance to low temperature, drought, and salt stress via both ABA-dependent and ABA-independent pathways. Planta 233:219-29.
84. Zarka, D.G., J.T. Vogel, D. Cook and M.F. Thomashow. 2003. Cold induction of Arabidopsis CBF genes involves multiple ICE (inducer of CBF expression) promoter elements and a cold-regulatory circuit that is desensitized by low temperature. Plant Physiol. 133:910-918.
85. Zhang, X., S.G. Fowler, H. Cheng, Y. Lou, S.Y. Rhee, E.J. Stockinger and M.F. Thomashow. 2004. Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis. Plant J. 39:905-19.