Overexpression of a blueberry-derived CBF gene enhances cold tolerance in a southern highbush blueberry cultivar

Molecular Breeding

Volumn 30, Issue 3, 2012, Pages 1313-1323

  Walworth, Aaron E ^a   Rowland, Lisa J ^b   Polashock, James J ^b   Hancock, James F ^a   Song, Guo qing ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

C repeat binding factor (CBF) gene; Cold tolerance; Freezing tolerance; Transgenic plant; Vaccinium corymbosum; Woody plant

Indexed keywords

ELECTROLYTES; FREEZING; GENE ENCODING; PLANTS (BOTANY); TEMPERATURE; VIRUSES;

BINDING FACTORS; BLUEBERRY CULTIVARS; C-REPEAT BINDING FACTOR GENE; COLD TOLERANCE; FREEZING TOLERANCE; TRANSGENEIC PLANTS; TRANSGENIC LINES; TRANSGENICS; VACCINIUM CORYMBOSUM; WOODY PLANTS;

TRANSCRIPTION;

AGROBACTERIUM; CAULIFLOWER MOSAIC VIRUS; RHIZOBIUM; VACCINIUM; VACCINIUM CORYMBOSUM;

EID: 84866932498     PISSN: 13803743     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11032-012-9718-7     Document Type: Article

References (56)

1. An G, Ebert PR, Mitra A, Ha SB (1988) Binary vectors. In: Gelvin SB, Shilperoort RA (eds) Plant molecular biology manual. Martinus Nijhoff, Dordrecht, pp A3: 1-19.
2. Arora R, Rowland LJ, Lehman JS, Lim CC, Panta GR, Vorsa N (2000) Genetic analysis of freezing tolerance in blueberry (Vaccinium section Cyanococcus). Theor Appl Genet 100: 690-696.
3. Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24: 701-713.
4. Benedict C, Skinner JS, Meng R, Chang YJ, Bhalerao R, Huner NPA, Finn CE, Chen THH, Hurry V (2006) The CBF1-dependent low temperature signaling pathway, regulon and increase in freeze tolerance are conserved in Populus spp. Plant, Cell Environ 29: 1259-1272.
5. Bhat SR, Srinivasan S (2002) Molecular and genetic analyses of transgenic plants: considerations and approaches. Plant Sci 163: 673-681.
6. Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11: 113-116.
7. Choi DW, Rodriguez EM, Close TJ (2002) Barley Cbf3 gene identification, expression pattern, and map location. Plant Physiol 129: 1781-1787.
8. Dhanaraj AL, Slovin JP, Rowland LJ (2005) Isolation of a cDNA clone and characterization of expression of the highly abundant, cold acclimation-associated 14 kDa dehydrin of blueberry. Plant Sci 168: 949-957.
9. Dhanaraj AL, Alkharouf NW, Beard HS, Chouikha IB, Matthews BF, Wei H, Arora R, Rowland LJ (2007) Major differences observed in transcript profiles of blueberry during cold acclimation under field and cold room conditions. Planta 225: 735-751.
10. Doyle JJ, Doyle JL (1987) A rapid DNA isolation precedure for small quantities of fresh leaf tissue. Phytochem Bull 19: 11-15.
11. Ehlenfeldt MK, Rowland LJ, Arora R (2003) Bud hardiness and deacclimation in blueberry cultivars with varying species ancestry: flowering time may not be a good indicator of deacclimation. Acta Hort 626: 39-44.
12. El Kayal W, Navarro M, Marque G, Keller G, Marque C, Teulieres C (2006) Expression profile of CBF-like transcriptional factor genes from Eucalyptus in response to cold. J Exp Bot 57: 2455-2469.
13. Gao MJ, Allard G, Byass L, Flanagan AM, Singh J (2002) Regulation and characterization of four CBF transcription factors from Brassica napus. Plant Mol Biol 49: 459-471.
14. Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (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.
15. Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124: 1854-1865.
16. Guy CL, Niemi KJ, Brambl R (1985) Altered gene expression during cold acclimation of spinach. Proc Natl Acad Sci USA 82: 3673-3677.
17. Hancock JF, Goulart BL, Erb WA, Scheerens JC (1997) Blueberry hybrids with complex genetic backgrounds evaluated on mineral soils: cold hardiness as influenced by parental species and location. Acta Hort 446: 389-395.
18. Hanson EJ, Berkheimer SF, Hancock JF (2007) Seasonal changes in the cold hardiness of the flower buds of highbush blueberry with varying species ancestry. J Am Pomol Soc 61: 14-18.
19. Hicklenton PR, Reekie JYC, MacKenzie K, Ryan D, Eaton LJ, Havard P (2002) Freeze damage and frost tolerance thresholds for flowers of the lowbush blueberry (Vaccinium angustifolium Ait). Acta Hort 574: 193-201.
20. Hood EE, Gelvin SB, Melchers LS, Hoekema A (1993) New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res 2: 208-218.
21. Jaglo KR, Kleff S, Amundsen KL, Zhang X, Haake V, Zhang JZ, Deits T, Thomashow MF (2001) 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.
22. Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280: 104-106.
23. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901-3907.
24. Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17: 287-291.
25. Kitashiba H, Ishizaka T, Isuzugawa K, Nishimura K, Suzuki T (2004) Expression of a sweet cherry DREB1/CBF ortholog in Arabidopsis confers salt and freezing tolerance. J Plant Physiol 161: 1171-1176.
26. Levi A, Panta GR, Parmentier CM, Muthalif MM, Arora R, Shanker S, Rowland LJ (1999) Complementary DNA cloning, sequencing and expression of an unusual dehydrin from blueberry floral buds. Physiol Plant 107: 98-109.
27. Lin W, Pliszka K (2003) Comparison of spring frost tolerance among different highbush blueberry (Vaccinium corymbosum L.) cultivars. Acta Hort 626: 337-341.
28. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (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: 1391-1406.
29. Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H, Shimada Y, Yoshida S, Shinozaki K, Yamaguchi-Shinozaki K (2004) Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J 38: 982-993.
30. Muthalif MM, Rowland LJ (1994) Identification of dehydrin-like proteins responsive to chilling in floral buds of blueberry (Vaccinium, section Cyanococcus). Plant Physiol 104: 1439-1447.
31. Naik D, Dhanaraj AL, Arora R, Rowland LJ (2007) Identification of genes associated with cold acclimation in blueberry (Vaccinium corymbosum L.) using a subtractive hybridization approach. Plant Sci 173: 213-222.
32. Navarro M, Ayax C, Martinez Y, Laur J, El Kayal W, Marque C, Teulieres C (2011) Two EguCBF1 genes overexpressed in Eucalyptus display a different impact on stress tolerance and plant development. Plant Biotechnol J 9: 50-63.
33. Norvell DJ, Moore JN (1982) An evaluation of chilling models for estimating rest requirements of highbush blueberries (Vaccinium corymbosum L). J Am Soc Hort Sci 107: 54-56.
34. Owens CL, Thomashow MF, Hancock JF, Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologous expression of CBF1 in strawberry. J Am Soc Hort Sci 127: 489-494.
35. Pino MT, Skinner JS, Jeknic Z, Hayes PM, Soeldner AH, Thomashow MF, Chen TH (2008) Ectopic AtCBF1 over-expression enhances freezing tolerance and induces cold acclimation-associated physiological modifications in potato. Plant, Cell Environ 31: 393-406.
36. Polashock JJ, Arora R, Peng Y, Naik D, Rowland LJ (2010) Functional identification of a C-repeat binding factor transcriptional activator from blueberry associated with cold acclimation and freezing tolerance. J Am Soc Hort Sci 135: 40-48.
37. Qin F, Sakuma Y, Li J, Liu Q, Li YQ, Shinozaki K, Yamagushi-Shinozaki KY (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.
38. Serres R, McCown B, Zeldin E (1997) Detectable β-glucuronidase activity in transgenic cranberry is affected by endogenous inhibitors and plant development. Plant Cell Rep 16: 641-646.
39. Siddiqua M, Nassuth A (2011) Vitis CBF1 and Vitis CBF4 differ in their effect on Arabidopsis abiotic stress tolerance, development and gene expression. Plant, Cell Environ 34: 1345-1359.
40. Song G-Q, Sink KC (2004) Agrobacterium tumefaciens-mediated transformation of blueberry (Vaccinium corymbosum L.). Plant Cell Rep 23: 475-484.
41. Song G-Q, Sink KC (2006) Agrobacterium-mediated transformation of highbush blueberry (Vaccinium corymbosum L.) cultivars. In: Wang K (ed) Agrobacterium protocols: methods in molecular biology 344, 2nd edn. Humana Press, Totowa, pp 263-272.
42. Stam M, Mol JNM, Kooter JM (1997) The silence of genes in transgenic plants. Ann Bot 79: 3-12.
43. Steponkus PL, Uemura M, Joseph RA, Gilmour SJ, Thomashow MF (1998) Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana. Proc Natl Acad Sci USA 95: 14570-14575.
44. Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94: 1035-1040.
45. Takuhara Y, Kobayashi M, Suzuki S (2011) Low-temperature-induced transcription factors in grapevine enhance cold tolerance in transgenic Arabidopsis plants. J Plant Physiol 168: 967-975.
46. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50: 571-599.
47. Thomashow MF (2010) Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol 154: 571-577.
48. Tillett RL, Wheatley MD, Tattersall EA, Schlauch KA, Cramer GR, Cushman JC (2012) The Vitis vinifera C-repeat binding protein 4 (VvCBF4) transcriptional factor enhances freezing tolerance in wine grape. Plant Biotechnol J 10: 105-124. doi: 10. 1111/j. 1467-7652. 2011. 00648. x.
49. USDA-ERS (2010) U. S. Blueberry Industry Dataset http://usda. mannlib. cornell. edu/MannUsda/viewDocumentInfo. do?documentID=1765. Accessed 8 June 2011.
50. Vogel JT, Zarka DG, van Buskirk HA, Fowler SG, Thomashow MF (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41: 195-211.
51. Walworth AE, Warner RM (2009) Differential cold acclimation ability of Petunia spp. HortScience 44: 1219-1222.
52. Wisniewski M, Norelli J, Bassett C, Artlip T, Macarisin D (2011) Ectopic expression of a novel peach (Prunus persica) CBF transcription factor in apple (Malus × domestica) results in short-day induced dormancy and increased cold hardiness. Planta 233: 971-983.
53. Xiao H, Siddiqua M, Braybrook S, Nassuth A (2006) Three grape CBF/DREB1 genes respond to low temperature, drought and abscisic acid. Plant, Cell Environ 29: 1410-1421.
54. Xiao H, Tattersall EA, Siddiqua MK, Cramer GR, Nassuth A (2008) CBF4 is a unique member of the CBF transcription factor family of Vitis vinifera and Vitis riparia. Plant, Cell Environ 31: 1-10.
55. Yang W, Liu XD, Chi XJ, Wu CA, Li YZ, Song LL, Liu XM, Wang YF, Wang FW, Zhang C, Liu Y, Zong JM, Li HY (2011) Dwarf apple MbDREB1 enhances plant tolerance to low temperature, drought, and salt stress via both ABA-dependent and ABA-independent pathways. Planta 233: 219-229.
56. Zhang X, Fowler SG, Cheng HM, Lou YG, Rhee SY, Stockinger EJ, Thomashow MF (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: 905-919.