LlHSFA1, a novel heat stress transcription factor in lily (Lilium longiflorum), can interact with LlHSFA2 and enhance the thermotolerance of transgenic Arabidopsis thaliana

Plant Cell Reports

Volumn 33, Issue 9, 2014, Pages 1519-1533

  Gong, Benhe ^a   Yi, Jin ^a,b   Wu, Jian ^a   Sui, Juanjuan ^a,c   Khan, Muhammad Ali ^a   Wu, Ze ^a   Zhong, Xionghui ^a   Seng, Shanshan ^a   He, Junna ^a   Yi, Mingfang ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b BEIJING NORMAL UNIVERSITY   (China)

^c FUYANG NORMAL UNIVERSITY   (China)

Author keywords

Ectopic overexpression; Gene expression; Heat stress transcription factor; Lilium longiflorum; Protein interaction; Thermotolerance

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; LILIUM; LILIUM LONGIFLORUM; NICOTIANA BENTHAMIANA;

COMPLEMENTARY DNA; DNA BINDING PROTEIN; HEAT SHOCK PROTEIN; HEAT STRESS TRANSCRIPTION FACTORS; HYBRID PROTEIN; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; HEAT; HEAT SHOCK RESPONSE; LILY; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; PLANT LEAF; PLANT ROOT; REPORTER GENE; SEQUENCE ALIGNMENT; TRANSCRIPTION INITIATION; TRANSGENIC PLANT; TWO HYBRID SYSTEM;

AMINO ACID SEQUENCE; ARABIDOPSIS; BASE SEQUENCE; DNA, COMPLEMENTARY; DNA-BINDING PROTEINS; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; HOT TEMPERATURE; LILIUM; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84906262600     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-014-1635-2     Document Type: Article

References (57)

1. Baniwal SK, Bharti K, Chan KY, Fauth M, Ganguli A, Kotak S, Mishra SK, Nover L, Port M, Scharf KD, Tripp J, Weber C, Zielinski D, von Koskull-Doring P (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J Biosci 29(4): 471-487. doi: 10. 1007/bf02712120.
2. Batoko H, Zheng H-Q, Hawes C, Moore I (2000) A Rab1 GTPase is required for transport between the endoplasmic reticulum and Golgi apparatus and for normal Golgi movement in plants. Plant Cell 12: 2201-2217.
3. Bharti K, von Koskull-Doring P, Bharti S, Kumar P, Tintschl-Korbitzer A, Treuter E, Nover L (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(6): 1521-1535. doi: 10. 1105/tpc. 019927.
4. Busch W, Wunderlich M, Schoffl F (2005) Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J 41(1): 1-14. doi: 10. 1111/j. 1365-313X. 2004. 02272. x.
5. 2+ and CaM3 in regulation of thermotolerance in lily (Lilium longiflorum). Plant Mol Biol Rep 31(6): 1293-1304. doi: 10. 1007/s11105-013-0587-y.
6. Chan-Schaminet KY, Baniwal SK, Bublak D, Nover L, 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(31): 20848-20857. doi: 10. 1074/jbc. M109. 007336.
7. Charng YY, Liu HC, Liu NY, Chi WT, Wang CN, Chang SH, Wang TT (2007) A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol 143(1): 251-262. doi: 10. 1104/pp. 106. 091322.
8. Chauhan H, Khurana N, Agarwal P, Khurana P (2011) Heat shock factors in rice (Oryza sativa L.): genome-wide expression analysis during reproductive development and abiotic stress. Mol Genet Genomics 286(2): 171-187. doi: 10. 1007/s00438-011-0638-8.
9. Chauhan H, Khurana N, Agarwal P, Khurana JP, Khurana P (2013) A seed preferential heat shock transcription factor from wheat provides abiotic stress tolerance and yield enhancement in transgenic Arabidopsis under heat stress environment. PLoS One 8(11): e79577. doi: 10. 1371/journal. pone. 0079577.
10. Chen W, Yin X, Wang L, Tian J, Yang R, Liu D, Yu Z, Ma N, Gao J (2013) Involvement of rose aquaporin RhPIP1;1 in ethylene-regulated petal expansion through interaction with RhPIP2;1. Plant Mol Biol 83(3): 219-233. doi: 10. 1007/s11103-013-0084-6.
11. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6): 735-743.
12. Czarnecka-verner E, Pan S, Salem T, Gurley WB (2004) Plant class B HSFs inhibit transcription and exhibit affinity for TFIIB and TBP. Plant Mol Biol 56(1): 57-75. doi: 10. 1007/s11103-004-2307-3.
13. Döring P, Treuter E, Kistner C, Lyck R, Chen A, Nover L (2000) The role of AHA motifs in the activator function of tomato heat stress transcription factors HsfA1 and HsfA2. Plant Cell 12(2): 265-278.
14. Hahn A, Bublak D, Schleiff E, Scharf KD (2011) Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. Plant Cell 23(2): 741-755. doi: 10. 1105/tpc. 110. 076018.
15. Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol from nascent chain to folded protein. Science 295: 1852-1858.
16. Kotak S, Port M, Ganguli A, Bicker F, von Koskull-Döring P (2004) Characterization of C-terminal domains of Arabidopsis 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(1): 98-112. doi: 10. 1111/j. 1365-313X. 2004. 02111. x.
17. Larkindale J, Vierling E (2008) Core genome responses involved in acclimation to high temperature. Plant Physiol 146(2): 748-761. doi: 10. 1104/pp. 107. 112060.
18. Lee J-H, Yun HS, Kwon C (2012) Molecular communications between plant heat shock responses and disease resistance. Mol Cells 34(2): 109-116. doi: 10. 1007/s10059-012-0121-3.
19. Li Z, Zhang L, Wang A, Xu X, 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(1): e54880. doi: 10. 1371/journal. pone. 0054880. g001.
20. Liu HC, Charng YY (2012) Acquired thermotolerance independent of heat shock factor A1 (HsfA1), the master regulator of the heat stress response. Plant Signal Behav 7(5): 547-550. doi: 10. 4161/psb. 19803.
21. Liu HC, Charng YY (2013) Common and distinct functions of Arabidopsis class A1 and A2 heat shock factors in diverse abiotic stress responses and development. Plant Physiol 163(1): 276-290. doi: 10. 1104/pp. 113. 221168.
22. Liu HC, Liao HT, Charng YY (2011) The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. Plant Cell Environ 34(5): 738-751. doi: 10. 1111/j. 1365-3040. 2011. 02278. x.
23. Liu Y, Zhang C, Chen J, Guo L, Li X, Li W, Yu Z, Deng J, Zhang P, Zhang K, Zhang L (2013) Arabidopsis heat shock factor HsfA1a directly senses heat stress, pH changes, and hydrogen peroxide via the engagement of redox state. Plant Physiol Biochem 64: 92-98. doi: 10. 1016/j. plaphy. 2012. 12. 013.
24. Lyck R, Harmening U, Hohfeld I, Treuter E, Scharf KD, Nover L (1997) Intracellular distribution and identification of the nuclear localization signals of two plant heat-stress transcription factors. Planta 202(1): 117-125.
25. Mishra SK, Tripp J, Winkelhaus S, Tschiersch B, Theres K, Nover L, Scharf KD (2002) In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev 16(12): 1555-1567. doi: 10. 1101/gad. 228802.
26. Morimoto RI (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12(24): 3788-3796. doi: 10. 1101/gad. 12. 24. 3788.
27. Nishizawa-Yokoi A, Nosaka R, Hayashi H, Tainaka H, Maruta T, Tamoi M, Ikeda M, Ohme-Takagi M, Yoshimura K, Yabuta Y, Shigeoka S (2011) HsfA1d and HsfA1e involved in the transcriptional regulation of HsfA2 function as key regulators for the Hsf signaling network in response to environmental stress. Plant Cell Physiol 52(5): 933-945. doi: 10. 1093/pcp/pcr045.
28. Nover L, Scharf KD, Gagliardi D, Vergne P, CzarneckaVerner E, Gurley WB (1996) The Hsf world: classification and properties of plant heat stress transcription factors. Cell Stress Chaperones 1(4): 215-223.
29. Nover L, Bharti K, Döring P, Mishra SK, Ganguli A, Scharf KD (2001) Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones 6(3): 177-189. doi: 10. 1379/1466-1268(2001). 006<0177: aathst>2. 0. co;2.
30. Panchuk II, Volkov RA, Schoffl F (2002) Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol 129(2): 838-853. doi: 10. 1104/pp. 001362.
31. Panikulangara TJ, Eggers-Schumacher G, Wunderlich M, Stransky H, Schoffl F (2004) Galactinol synthase1. A novel heat shock factor target gene responsible for heat-induced synthesis of raffinose family oligosaccharides in Arabidopsis. Plant Physiol 136(2): 3148-3158. doi: 10. 1104/pp. 104. 042606.
32. Port M, Tripp J, Zielinski D, Weber C, Heerklotz D, Winkelhaus S, Bublak D, Scharf KD (2004) Role of Hsp17. 4-CII as coregulator and cytoplasmic retention factor of tomato heat stress transcription factor HsfA2. Plant Physiol 135(3): 1457-1470. doi: 10. 1104/pp. 104. 042820.
33. Qin F, Kakimoto M, Sakuma Y, Maruyama K, Osakabe Y, Tran LS, Shinozaki K, Yamaguchi-Shinozaki K (2007) Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant J 50(1): 54-69. doi: 10. 1111/j. 1365-313X. 2007. 03034. x.
34. Sato T, Miyoshi K (2006) Thermosensitivity of the restoration of male fertility and genotypic differences in the formation of aberrant filaments and pistils among three male-sterile cultivars of Asiatic hybrid lily. In: Schiva T (ed) Proceedings of the 22nd international eucarpia symposium section ornamentals: breeding for beauty. Acta Hortic 714: 67-74.
35. Scharf KD, Rose S, Zott W, Schoff F, Nover L (1990) 3 Tomato genes code for heat-stress transcription factors with a region of remarkable homology to the DNA-binding domain of the yeast Hsf. EMBO J 9(13): 4495-4501.
36. Scharf KD, Heider H, Hohfeld I, Lyck R, Schmidt E, 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(4): 2240-2251.
37. Scharf KD, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim Biophys Acta 1819(2): 104-119. doi: 10. 1016/j. bbagrm. 2011. 10. 002.
38. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3(6): 1101-1108. doi: 10. 1038/nprot. 2008. 73.
39. Schramm F, Ganguli A, Kiehlmann E, Englich G, Walch D, von Koskull-Döring 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(5): 759-772. doi: 10. 1007/s11103-005-5750-x.
40. Schramm F, Larkindale J, Kiehlmann E, Ganguli A, Englich G, Vierling E, Von Koskull-Döring P (2008) A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis. Plant J 53(2): 264-274. doi: 10. 1111/j. 1365-313X. 2007. 03334. x.
41. Suk-Whan H, Elizabeth V (2000) Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc Natl Acad Sci USA 97(8): 4392-4397.
42. Suter B, Kittanakom S, Stagljar I (2008) Two-hybrid technologies in proteomics research. Curr Opin Biotechnol 19(4): 316-323. doi: 10. 1016/j. copbio. 2008. 06. 005.
43. Suzuki N, Rizhsky L, Liang H, Shuman J, Shulaev V, Mittler R (2005) Enhanced tolerance to environmental stress in transgenic plants expressing the transcriptional coactivator multiprotein bridging factor 1c. Plant Physiol 139(3): 1313-1322. doi: 10. 1104/pp. 105. 070110.
44. Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37(6): 914-939. doi: 10. 1111/j. 1365-313X. 2004. 02016. x.
45. Treuter E, Nover L, Ohme K, Scharf KD (1993) Promoter specificity and deletion analysis of 3 heat-stress transcription factors of tomato. Mol Gen Genet 240(1): 113-125.
46. von Koskull-Döring P, Scharf KD, Nover L (2007) The diversity of plant heat stress transcription factors. Trends Plant Sci 12(10): 452-457. doi: 10. 1016/j. tplants. 2007. 08. 014.
47. Walter M, Chaban C, Schutze K, Batistic O, Weckermann K, Nake C, Blazevic D, Grefen C, Schumacher K, Oecking C, Harter K, Kudla J (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40(3): 428-438. doi: 10. 1111/j. 1365-313X. 2004. 02219. x.
48. Wang C, Zhang Q, Shou HX (2009) Identification and expression analysis of OsHsfs in rice. J Zhejiang Univ Sci B 10(4): 291-300. doi: 10. 1631/jzus. B0820190.
49. Weining S, Catherine B, van de Cotte B, Marc VM, Nathalie V (2001) AtHSP17. 6A, encoding a small heat shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J 27(5): 407-415.
50. Wise AA, Liu Z, Binns AN (2006) Three methods for the Introduction of Foreign DNA into Agrobacterium. Methods Mol Biol 343: 43-53.
51. Wu C (1995) Heat shock transcription factors structure and regulation. Annu Rev Cell Dev Biol 11: 441-469.
52. Xin H, Zhang H, Chen L, Li X, Lian Q, Yuan X, Hu X, Cao L, He X, Yi M (2010) Cloning and characterization of HsfA2 from Lily (Lilium longiflorum). Plant Cell Rep 29(8): 875-885. doi: 10. 1007/s00299-010-0873-1.
53. Yin H, Chen Q, Yi M (2008) Effects of short-term heat stress on oxidative damage and responses of antioxidant system in Lilium longiflorum. Plant Growth Regul 54(1): 45-54. doi: 10. 1007/s10725-007-9227-6.
54. Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H, Iwabuchi M, Oda K (2008) Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis. Planta 227(5): 957-967. doi: 10. 1007/s00425-007-0670-4.
55. Yoshida T, Ohama N, Nakajima J, Kidokoro S, Mizoi J, Nakashima K, Maruyama K, Kim JM, Seki M, Todaka D, Osakabe Y, Sakuma Y, Schoffl F, Shinozaki K, Yamaguchi-Shinozaki K (2011) Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression. Mol Genet Genomics 286(5-6): 321-332. doi: 10. 1007/s00438-011-0647-7.
56. Zhu B, Ye C, Lu H, Chen X, Chai G, Chen J, Wang C (2006) Identification and characterization of a novel heat shock transcription factor gene, GmHsfA1, in soybeans (Glycine max). J Plant Res 119(3): 247-256. doi: 10. 1007/s10265-006-0267-1.
57. Zhu Y, Wang Z, Jing Y, Wang L, Liu X, Liu Y, Deng X (2009) Ectopic over-expression of BhHsf1, a heat shock factor from the resurrection plant Boea hygrometrica, leads to increased thermotolerance and retarded growth in transgenic Arabidopsis and tobacco. Plant Mol Biol 71(4-5): 451-467. doi: 10. 1007/s11103-009-9538-2.