Identification, isolation, and expression analysis of heat shock transcription factors in the diploid woodland strawberry Fragaria Vesca

Frontiers in Plant Science

Volumn 6, Issue September, 2015, Pages

  Hu, Yang ^a,b   Han, Yong Tao ^a   Wei, Wei ^a,b   Li, Ya Juan ^a   Zhang, Kai ^a,b   Gao, Yu Rong ^a   Zhao, Feng Li ^a   Feng, Jia Yue ^a,b  

^a NORTHWEST A F UNIVERSITY   (China)

^b AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

Author keywords

Abiotic stress; Expression analysis; Heat shock transcription factor; Heat stress; Phytohormones; Strawberry (Fragaria vesca); Subcellular localization

Indexed keywords

EID: 84942858700     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00736     Document Type: Article

References (60)

1. Almoguera, C., Prieto-Dapena, P., Diaz-Martin, J., Espinosa, J. M., Carranco, R., and Jordano, J. (2009). The HaDREB2 transcription factor enhances basal thermotolerance and longevity of seeds through functional interaction with HaHSFA9. BMC Plant Biol. 9:75. doi: 10.1186/1471-22 29-9-75
2. Begum, T., Reuter, R., and Schoffl, F. (2013). Overexpression of AtHsfB4 induces specific effects on root development of Arabidopsis. Mech. Dev. 130, 54-60. doi: 10.1016/j.mod.2012.05.008
3. Bharti, K., Von Koskull-Doring, P., Bharti, S., Kumar, P., Tintschl-Korbitzer, A., Treuter, E., et al. (2004). Tomato heat stress transcription factor HsfB1 represents a novel type of general transcription coactivator with a histone-like motif interacting with the plant CREB binding protein ortholog HAC1. Plant Cell 16, 1521-1535. doi: 10.1105/tpc.019927
4. Chan-Schaminet, K. Y., Baniwal, S. K., Bublak, D., Nover, L., and Scharf, K. D. (2009). Specific interaction between tomato HsfA1 and HsfA2 creates hetero-oligomeric superactivator complexes for synergistic activation of heat stress gene expression. J. Biol. Chem. 284, 20848-20857. doi: 10.1074/jbc.M109.007336
5. Chung, E., Kim, K. M., and Lee, J. H. (2013). Genome-wide analysis and molecular characterization of heat shock transcription factor family in Glycine max. J. Genet. Genomics 40, 127-135. doi: 10.1016/j.jgg.2012.12.002
6. Clarke, S. M., Cristescu, S. M., Miersch, O., Harren, F. J. M., Wasternack, C., and Mur, L. A. (2009). Jasmonates act with salicylic acid to confer basal thermotolerance in Arabidopsis thaliana. New Phytol. 182, 175-187. doi: 10.1111/j.1469-8137.2008.02735.x
7. Darwish, O., Shahan, R., Liu, Z. C., Slovin, J. P., and Alkharouf, N. W. (2015). Re-annotation of the woodland strawberry (Fragaria vesca) genome. BMC Genomics 16:29. doi: 10.1186/s12864-015-1221-1
8. Davletova, S., Rizhsky, L., Liang, H., Shengqiang, Z., Oliver, D. J., Coutu, J., et al. (2005). Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17, 268-281. doi: 10.1105/tpc.104.026971
9. de Souza, S. J., Long, M., Kleln, R. J., Roy, S., Lin, S., and Gilbert, W. (1998). Toward a resolution ofthe introns early/late debate: onlyphase zero introns are correlated with the structure ofancient proteins. Proc. Natl. Acad. Sci. U.S.A. 95, 5094-5099. doi: 10.1073/pnas.95.9.5094
10. Deng, Q. L., Ishii, S., and Sarai, A. (1996). Binding site analysis of c-Myb: Screening ofpotential binding sites by using the mutation matrixderived from systematic binding affinity measurements. Nucleic Acids Res. 24, 766-774. doi: 10.1093/nar/24.4.766
11. Doring, P., Treuter, E., Kistner, C., Lyck, R., Chen, A., and Nover, L. (2000). The role ofAHA motifs in the activator function oftomato heat stress transcription factors HsfA1 and HsfA2. Plant Cell 12,265-278. doi: 10.1105/tpc.12.2.265
12. Ghiurcuta, C. G., and Moret, B. M. E. (2014). Evaluating synteny for improved comparative studies. Bioinformatics 30, 9-18. doi: 10.1093/bioinformatics/btu259
13. Giesguth, M., Sahm, A., Simon, S., and Dietz, K. J. (2015). Redox-dependent translocation of the heat shock transcription factor AtHSFA8 from the cytosol to the nucleus in Arabidopsis thaliana. FEBS Lett. 589, 718-725. doi: 10.1016/j.febslet.2015.01.039
14. Giorno, F., Guerriero, G., Baric, S., and Mariani, C. (2012). Heat shock transcriptional factors in Malus domestica: identification, classification and expression analysis. BMC Genomics 13:639. doi: 10.1186/1471-216413-639
15. Guo, J. K., Wu, J., Ji, Q., Wang, C., Luo, L., Yuan, Y., et al. (2008). Genome-wide analysis ofheat shocktranscription factor families in rice and Arabidopsis. J. Genet. Genomics 35, 105-118. doi: 10.1016/S1673-8527(08)60016-8
16. Hahn, A., Bublak, D., Schleiff, E., and Scharf, K. D. (2011). Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. Plant Cell 23,741-755. doi: 10.1105/ttpc. 110.076018
17. Harrison, C. J., Bohm, A. A., and Nelson, H. C. M. (1994). Crystal-structure of the DNA-binding domain of the heat-shock transcription factor. Science 263, 224-227. doi: 10.1126/science.8284672
18. Hedhly, A., Hormaza, J. I., and Herrero, M. (2009). Global warming and sexual plant reproduction. Trends Plant Sci. 14, 30-36. doi: 10.1016/j.tplants.2008.11.001
19. Heerklotz, D., Doring, P., Bonzelius, F., Winkelhaus, S., and Nover, L. (2001). The balance of nuclear import and export determines the intracellular distribution and function of tomato heat stress transcription factor HsfA2. Mol. Cell. Biol. 21, 1759-1768. doi: 10.1128/MCB.21.5.1759-1768.2001
20. Hwang, S. M., Kim, D. W., Woo, M. S., Jeong, H. S., Son, Y. S., Akhter, S., et al. (2014). Functional characterization ofArabidopsis HsfA6a as a heat-shock transcription factor under high salinityand dehydration conditions. Plant Cell Environ. 37, 1202-1222. doi: 10.1111/pce.12228
21. Ikeda, M., Mitsuda, N., and Ohme-Takagi, M. (2011). Arabidopsis HsfB1 and HsfB2b act as repressors of the expression of heat-inducible Hsfs but positively regulate the acquired thermotolerance. Plant Physiol. 157, 1243-1254. doi: 10.1104/pp.111.179036
22. Jiang, C., Iu, B., and Singh, J. (1996). Requirement ofa CCGAC cis-acting element for cold induction of the BN115 gene from winter Brassica napus. Plant Mol. Biol. 30, 679-684. doi: 10.1007/BF00049344
23. Kotak, S., Port, M., Ganguli, A., Bicker, F., and Von Koskull-Doring, P. (2004). Characterization ofC-terminal domains ofArabidopsis heat stress transcription factors (Hsfs) and identification of a new signature combination of plant class A Hsfs with AHA and NES motifs essential for activator function and intracellular localization. Plant J. 39, 98-112. doi: 10.1111/j.1365-313X.2004.02111.x
24. Kotak, S., Vierling, E., Baumlein, H., and Von Koskull-Doring, P. (2007). A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. Plant Cell 19, 182-195. doi: 10.1105/tpc.106.048165
25. Kumar, M., Busch, W., Birke, H., Kemmerling, B., Nurnberger, T., and Schoffl, F. (2009). Heat shock factors HsfB1 and HsfB2b are involved in the regulation of Pdf1.2 expression and pathogen resistance in Arabidopsis. Mol. Plant 2, 152-165. doi: 10.1093/mp/ssn095
26. Lee, T. H., Tang, H. B., Wang, X. Y., and Paterson, A. H. (2013). PGDD: a database ofgene and genome duplication in plants. Nucleic Acids Res. 41, D1152-D1158. doi: 10.1093/nar/gks1104
27. Littlefield, O., and Nelson, H. C. M. (1999). A new use for the 'wing' of the 'winged' helix-turn-helix motif in the HSF-DNA cocrystal. Nat. Struct. Biol. 6, 464-470. doi: 10.1038/8269
28. Li, Z., Zhang, L., Wang, A., Xu, X., and Li, J. (2013). Ectopic overexpression of SlHsfA3, a heat stress transcription factor from tomato, confers increased thermotolerance and salt hypersensitivity in germination in transgenic Arabidopsis. PLoS ONE 8:e54880. doi: 10.1371/journal.pone.0054880
29. Liu, H., Xie, W. F., Zhang, L., Valpuesta, V., Ye, Z. W., Gao, Q. H., et al. (2014). Auxin biosynthesis by the YUCCA6 flavin monooxygenase gene in woodland strawberry. J. Integr. Plant Biol. 56, 350-363. doi: 10.1111/jipb.12150
30. Lyck, R., Harmening, U., Hohfeld, I., Treuter, E., Scharf, K. D., and Nover, L. (1997). Intracellular distribution and identification of the nuclear localization signals of two plant heat-stress transcription factors. Planta 202, 117-125. doi: 10.1007/s004250050110
31. Maughan, T. L., Black, B. L., and Drost, D. (2015). Critical temperature for sub-lethal cold injury of strawberry leaves. Sci. Hortic. 183, 8-12. doi: 10.1016/j.scienta.2014.12.001
32. Mayer, K. F. X., Rogers, J., Dolezel, J., Pozniak, C., Eversole, K., Feuillet, C., et al. (2014). A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345, 286. doi: 10.1126/science.1251788
33. Mittal, D., Chakrabarti, S., Sarkar, A., Singh, A., and Grover, A. (2009). Heat shock factor gene family in rice: genomic organization and transcript expression profiling in response to high temperature, low temperature and oxidative stresses. Plant Physiol. Biochem. 47, 785-795. doi: 10.1016/j.plaphy.2009.05.003
34. Mittler, R., Finka, A., and Goloubinoff, P. (2012). How do plants feel the heat? Trends Biochem. Sci. 37, 118-125. doi: 10.1016/j.tibs.2011.11.007
35. Never, L., Scharf, K. D., Gagliardi, D., Vergne, P., Czarneckaverner, E., and Gurley, W. B. (1996). The Hsf world: classification and properties of plant heat stress transcription factors. Cell Stress Chaperones 1, 215-223.
36. Nezhadahmadi, A., Faruq, G., and Rashid, K. (2015). The impact of drought stress on morphological and physiological parameters ofthree strawberryvarieties in different growing conditions. Pak. J. Agric. Sci. 52, 79-92.
37. Nishizawa-Yokoi, A., Yoshida, E., Yabuta, Y., and Shigeoka, S. (2009). Analysis of the regulation of target genes by an Arabidopsis heat shock transcription factor, HsfA2. Biosci. Biotechnol. Biochem. 73, 890-895. doi: 10.1271/bbb. 80809
38. Pick, T., Jaskiewicz, M., Peterhansel, C., and Conrath, U. (2012). Heat shock factor HsfB1 primes gene transcription and systemic acquired resistance in Arabidopsis. Plant Physiol. 159, 52-55. doi: 10.1104/pp.111.191841
39. Prieto-Dapena, P., Castano, R., Almoguera, C., and Jordano, J. (2008). The ectopic overexpression of a seed-specific transcription factor, HaHSFA9, confers tolerance to severe dehydration in vegetative organs. Plant J. 54, 1004-1014. doi: 10.1111/j.1365-313X.2008.03465.x
40. Raab, T., Lopez-Raez, J. A., Klein, D., Caballero, J. L., Moyano, E., Schwab, W., et al. (2006). FaQR, required for the biosynthesis of the strawberry flavor compound 4-hydroxy-2,5-dimethyl-3(2H)-furanone, encodes an enone oxidoreductase. Plant Cell 18, 1023-1037. doi: 10.1105/tpc.105.039784
41. Ren, J., Wen, L. P., Gao, X. J., Jin, C. J., Xue, Y., and Yao, X. B. (2009). DOG 1.0: illustrator of protein domain structures. Cell Res. 19, 271-273. doi: 10.1038/cr.2009.6
42. Rombauts, S., Dehais, P., Van Montagu, M., and Rouze, P. (1999). PlantCARE, a plant cis-acting regulatory element database. Nucleic Acids Res. 27, 295-296. doi: 10.1093/nar/27.1.295
43. Scharf, K. D., Berberich, T., Ebersberger, I., and Nover, L. (2012). The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim. Biophys. Acta 1819, 104-119. doi: 10.1016/j.bbagrm.2011.10.002
44. Scharf, K. D., Heider, H., Hohfeld, I., Lyck, R., Schmidt, E., and Nover, L. (1998). The tomato Hsf system: HsfA2 needs interaction with HsfA1 for efficient nuclear import and may be localized in cytoplasmic heat stress granules. Mol. Cell. Biol. 18,2240-2251.
45. Schmutz, J., Cannon, S. B., Schlueter, J., Ma, J. X., Mitros, T., Nelson, W., et al. (2010). Genome sequence of the palaeopolyploid soybean. Nature 463, 178-183. doi: 10.1038/nature08670
46. Schramm, F., Ganguli, A., Kiehlmann, E., Englich, G., Walch, D., and Von Koskull-Doring, P. (2006). The heat stress transcription factor HsfA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. Plant Mol. Biol. 60, 759-772. doi: 10.1007/s11103-005-5750-x
47. Schramm, F., Larkindale, J., Kiehlmann, E., Ganguli, A., Englich, G., Vierling, E., et al. (2008). A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis. Plant J. 53, 264-274. doi: 10.1111/j.1365-313X.2007. 03334.x
48. Schwartz, S., Meshorer, E., and Ast, G. (2009). Chromatin organization marks exon-intron structure. Nat. Struct. Mol. Biol. 16, 990-995. doi: 10.1038/nsmb.1659
49. Schwechheimer, C., and Bevan, M. (1998). The regulation of transcription factor activity in plants. Trends Plant Sci. 3, 378-383. doi: 10.1016/S1360-1385(98)01302-8
50. Shen, Z., Yao, J., Sun, J., Chang, L., Wang, S., Ding, M., et al. (2015). Populus euphratica HSF binds the promoter ofWRKY1 to enhance salt tolerance. Plant Sci. 235,89-100. doi: 10.1016/j.plantsci.2015.03.006
51. Shim, D., Hwang, J. U., Lee, J., Lee, S., Choi, Y., An, G., et al. (2009). Orthologs of the Class A4 heat shock transcription factor HsfA4a confer cadmium tolerance in wheat and rice. Plant Cell 21, 4031-4043. doi: 10.1105/tpc.109.066902
52. Shulaev, V., Sargent, D. J., Crowhurst, R. N., Mockler, T. C., Folkerts, O., Delcher, A. L., et al. (2011). The genome of woodland strawberry (Fragaria vesca). Nat. Genet. 43, 109-116. doi: 10.1038/ng.740
53. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739. doi: 10.1093/molbev/msr121
54. Velasco, R., Zharkikh, A., Affourtit, J., Dhingra, A., Cestaro, A., Kalyanaraman, A., et al. (2010). The genome ofthe domesticated apple (Malus xdomestica Borkh.). Nat. Genet. 42, 833-839. doi: 10.1038/ng.654
55. Von Koskull-Doring, P., Scharf, K. D., and Nover, L. (2007). The diversity of plant heat stress transcription factors. Trends Plant Sci. 12, 452-457. doi: 10.1016/j.tplants.2007.08.014
56. Xue, G. P., Drenth, J., and Mcintyre, C. L. (2015). TaHsfA6f is a transcriptional activator that regulates a suite ofheat stress protection genes in wheat (Triticum aestivum L.) including previously unknown Hsf targets. J. Exp. Bot. 66, 1025-1039. doi: 10.1093/jxb/eru462
57. Xue, G. P., Sadat, S., Drenth, J., and McIntyre, C. L. (2014). The heat shock factor family from Triticum aestivum in response to heat and other major abiotic stresses and their role in regulation of heat shock protein genes. J. Exp. Bot. 65, 539-557. doi: 10.1093/jxb/ert399
58. Yoo, S. D., Cho, Y. H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572. doi: 10.1038/nprot.2007.199
59. Yoshida, T., Fujita, Y., Sayama, H., Kidokoro, S., Maruyama, K., Mizoi, J., et al. (2010). AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J. 61, 672-685. doi: 10.1111/j.1365-313X.2009.04092.x
60. Zhang, K., Han, Y. T., Zhao, F. L., Hu, Y., Gao, Y. R., Ma, Y. F., et al. (2015). Genome-wide identification and expression analysis of the CDPK gene family in grape, Vitis spp. BMC Plant Biol. 15:164. doi: 10.1186/s12870-015-0552-z