Prospects of engineering thermotolerance in crops through modulation of heat stress transcription factor and heat shock protein networks

Plant Cell and Environment

Volumn 38, Issue 9, 2015, Pages 1881-1895

  Fragkostefanakis, Sotirios ^a   Röth, Sascha ^a   Schleiff, Enrico ^a   Scharf, Klaus Dieter ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

Chaperone; Protein homeostasis; Stress response; Transcriptional regulation

Indexed keywords

DNA BINDING PROTEIN; HEAT SHOCK PROTEIN; HEAT STRESS TRANSCRIPTION FACTORS; PLANT PROTEIN; TRANSCRIPTION FACTOR;

CHEMISTRY; CROP; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC ENGINEERING; GENETICS; HEAT; HEAT SHOCK RESPONSE; METABOLISM; MULTIGENE FAMILY; PHYSIOLOGY; PROCEDURES;

CROPS, AGRICULTURAL; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; GENETIC ENGINEERING; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; HOT TEMPERATURE; MULTIGENE FAMILY; PLANT PROTEINS; TRANSCRIPTION FACTORS;

EID: 84938637176     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12396     Document Type: Review

References (166)

1. Agarwal M., Katiyar-Agarwal S., Sahi C., Gallie D.R. & Grover A. (2001) Arabidopsis thaliana Hsp100 proteins: kith and kin. Cell Stress and Chaperones 6, 219-224.
2. Ahuja I., de Vos R.C., Bones A.M. & Hall R.D. (2010) Plant molecular stress responses face climate change. Trends in Plant Science 15, 664-674.
3. Akerfelt M., Morimoto R.I. & Sistonen L. (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nature Reviews. Molecular Cell Biology 11, 545-555.
4. Almoguera C., Prieto-Dapena P., Díaz-Martín J., Espinosa J.M., Carranco R. & Jordano J. (2009) The HaDREB2 transcription factor enhances basal thermotolerance and longevity of seeds through functional interaction with HaHSFA9. BMC Plant Biology 9, 75.
5. Almoguera C., Prieto-Dapena P., Personat J.M., Tejedor-Cano J., Lindahl M., Diaz-Espejo A. & Jordano J. (2012) Protection of the photosynthetic apparatus from extreme dehydration and oxidative stress in seedlings of transgenic tobacco. PLoS One 7, e51443.
6. von Arnim A.G., Jia Q. & Vaughn J.N. (2014) Regulation of plant translation by upstream open reading frames. Plant Science: An International Journal of Experimental Plant Biology 214, 1-12.
7. Aviezer-Hagai K., Skovorodnikova J., Galigniana M., Farchi-Pisanty O., Maayan E., Bocovza S., ... Breiman A. (2007) Arabidopsis immunophilins ROF1 (AtFKBP62) and ROF2 (AtFKBP65) exhibit tissue specificity, are heat-stress induced, and bind HSP90. Plant Molecular Biology 63, 237-255.
8. Ballinger C.A., Connell P., Wu Y., Hu Z., Thompson L.J., Yin L.-Y. & Patterson C. (1999) Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Molecular and Cellular Biology 19, 4535-4545.
9. Baniwal S.K., Chan K.Y., Scharf K.-D. & Nover L. (2007) Role of heat stress transcription factor HsfA5 as specific repressor of HsfA4. The Journal of Biological Chemistry 282, 3605-3613.
10. Banti V., Mafessoni F., Loreti E., Alpi A. & Perata P. (2010) The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiology 152, 1471-1483.
11. Basha E., O'Neill H. & Vierling E. (2012) Small heat shock proteins and α-crystallins: dynamic proteins with flexible functions. Trends in Biochemical Sciences 37, 106-117.
12. Bechtold U., Albihlal W.S., Lawson T., Fryer M.J., Sparrow P.A., Richard F., ... Martin C. (2013) Arabidopsis HEAT SHOCK TRANSCRIPTION FACTOR A1b overexpression enhances water productivity, resistance to drought, and infection. Journal of Experimental Botany 64, 3467-3481.
13. Begum T., Reuter R. & Schöffl F. (2013) Overexpression of AtHsfB4 induces specific effects on root development of Arabidopsis. Mechanisms of Development 130, 54-60.
14. Bharti K., Schmidt E., Lyck R., Heerklotz D., Bublak D. & Scharf K.D. (2000) Isolation and characterization of HsfA3, a new heat stress transcription factor of Lycopersicon peruvianum. The Plant Journal: For Cell and Molecular Biology 22, 355-365.
15. Bharti K., von Koskull-Döring P., Bharti S., Kumar P., Tintschl-Körbitzer 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. The Plant Cell 16, 1521-1535.
16. Bita C.E. & Gerats T. (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Frontiers in Plant Science 4, 273.
17. Bokszczanin K.L., Solanaceae Pollen Thermotolerance Initial Training Network C. & Fragkostefanakis S. (2013) Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. Frontiers in Plant Science 4, 315.
18. Cabello J.V., Lodeyro A.F. & Zurbriggen M.D. (2014) Novel perspectives for the engineering of abiotic stress tolerance in plants. Current Opinion in Biotechnology 26, 62-70.
19. Cazalé A.-C., Clément M., Chiarenza S., Roncato M.-A., Pochon N., Creff A., ... Noël L.D. (2009) Altered expression of cytosolic/nuclear HSC70-1 molecular chaperone affects development and abiotic stress tolerance in Arabidopsis thaliana. Journal of Experimental Botany 60, 2653-2664.
20. Chan-Schaminet K.Y., Baniwal S.K., 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. The Journal of Biological Chemistry 284, 20848-20857.
21. Chang C.C., Huang P.S., Lin H.R. & Lu C.H. (2007) Transactivation of protein expression by rice HSP101 in planta and using Hsp101 as a selection marker for transformation. Plant and Cell Physiology 48, 1098-1107.
22. Charng Y.Y., Liu H.C., Liu N.Y., Chi W.T., Wang C.N., Chang S.H. & Wang T.T. (2007) A heat-inducible transcription faktor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiology 143, 251-262.
23. Chaturvedi P., Ischebeck T., Egelhofer V., Lichtscheidl I. & Weckwerth W. (2013) Cell-specific analysis of the tomato pollen proteome from pollen mother cell to mature pollen provides evidence for developmental priming. Journal of Proteome Research 12, 4892-4903.
24. 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. Molecular Genetics and Genomics 286, 171-187.
25. Chauhan H., Khurana N., Agarwal P., Khurana J.P. & 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, e79577.
26. Chen H., Hwang J.E., Lim C.J., Kim D.Y., Lee S.Y. & Lim C.O. (2010) Arabidopsis DREB2C functions as a transcriptional activator of HsfA during the heat stress response. Biochemical and Biophysical Research Communications 401, 238-244.
27. Cho E.K. & Choi Y.J. (2009) A nuclear-localized HSP70 confers thermoprotective activity and drought-stress tolerance on plants. Biotechnology Letters 31, 597-606.
28. Czarnecka-Verner E., Pan S., Salem T. & Gurley W.B. (2004) Plant class B HSFs inhibit transcription and exhibit affinity for TFIIB and TBP. Plant Molecular Biology 56, 57-75.
29. Dafny-Yelin M., Tzfira T., Vainstein A. & Adam Z. (2008) Non-redundant functions of sHSP-CIs in acquired thermotolerance and their role in early seed development in Arabidopsis. Plant Molecular Biology 67, 363-373.
30. Davletova S., Rizhsky L., Liang H., Shengqiang Z., Oliver D.J., Coutu J., ... Mittler R. (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. The Plant Cell 17, 268-281.
31. 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. The Plant Cell 12, 265-278.
32. Eyles S.J. & Gierasch L.M. (2010) Nature's molecular sponges: small heat shock proteins grow into their chaperone roles. Proceedings of the National Academy of Sciences of the United States of America 107, 2727-2728.
33. Frank G., Pressman E., Ophir R., Althan L., Shaked R., Freedman M., ... Firon N. (2009) Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response. Journal of Experimental Botany 60, 3891-3908.
34. Fu S. & Scanlon M.J. (2004) Clonal mosaic analysis of EMPTY PERICARP2 reveals nonredundant functions of the duplicated HEAT SHOCK FACTOR BINDING PROTEINs during maize shoot development. Genetics 167, 1381-1394.
35. Fu S., Meeley R. & Scanlon M.J. (2002) Empty pericarp2 encodes a negative regulator of the heat shock response and is required for maize embryogenesis. The Plant Cell 14, 3119-3132.
36. Fu S., Rogowsky P., Nover L. & Scanlon M.J. (2006) The maize heat shock factor-binding protein paralogs EMP2 and HSBP2 interact non-redundantly with specific heat shock factors. Planta 224, 42-52.
37. Gao H., Brandizzi F., Benning C. & Larkin R.M. (2008) A membrane-tethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 105, 16398-16403.
38. Giorno F., Wolters-Arts M., Grillo S., Scharf K.-D., Vriezen W.H. & Mariani C. (2010) Developmental and heat stress-regulated expression of HsfA2 and small heat shock proteins in tomato anthers. Journal of Experimental Botany 61, 453-462.
39. Grover A., Mittal D., Negi M. & Lavania D. (2013) Generating high temperature tolerant transgenic plants: achievements and challenges. Plant Science: An International Journal of Experimental Plant Biology 205, 38-47.
40. Guan Q., Yue X., Zeng H. & Zhu J. (2014) The protein phosphatase RCF2 and its interacting partner NAC019 are critical for heat stress-responsive gene regulation and thermotolerance in Arabidopsis. The Plant Cell 26, 438-453.
41. Guo L., Chen S., Liu K., Liu Y., Ni L., Zhang K. & Zhang L. (2008) Isolation of heat shock factor HsfA1a-binding sites in vivo revealed variations of heat shock elements in Arabidopsis thaliana. Plant and Cell Physiology 49, 1306-1315.
42. Gutsche I., Essen L.-O. & Baumeister W. (1999) Group II chaperonins: new TRiC(k)s and turns of a protein folding machine. Journal of Molecular Biology 293, 295-312.
43. Hahn A., Bublak D., Schleiff E. & Scharf K.-D. (2011) Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. The Plant Cell 23, 741-755.
44. Heerklotz D., Döring P., Bonzelius F., Winkelhaus S. & Nover L. (2001) The balance of nuclear import and export determines the intracellular distribution and function of tomato heat stress transcription factor HsfA2. Molecular and Cellular Biology 21, 1759-1768.
45. Hemmingsen S.M., Woolford C., van der Vies S.M., Tilly K., Dennis D.T., Georgopoulos C.P., ... Ellis R.J. (1988) Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature 333, 330-334.
46. Hong S.W. & Vierling E. (2000) Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proceedings of the National Academy of Sciences of the United States of America 97, 4392-4397.
47. Hong S.W. & Vierling E. (2001) Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress. The Plant Journal: For Cell and Molecular Biology 27, 25-35.
48. Howarth C.J. (2005) Genetic improvements of tolerance to high temperature. In Abiotic Stresses: Plant Resistance through Breeding and Molecular Approaches (eds M. Ashraf & P.J.C. Harris), pp. 277-300. Howarth Press Inc, New York.
49. Hsu S.F. & Jinn T.L. (2010) AtHSBP functions in seed development and the motif is required for subcellular localization and interaction with AtHSFs. Plant Signaling and Behavior 5, 1042-1044.
50. Hsu S.F., Lai H.C. & Jinn T.L. (2010) Cytosol-localized heat shock factor-binding protein, AtHSBP, functions as a negative regulator of heat shock response by translocation to the nucleus and is required for seed development in Arabidopsis. Plant Physiology 153, 773-784.
51. Hwang S.M., Kim D.W., Woo M.S., Jeong H.S., Son Y.S., Akhter S., ... Bahk J.D. (2013) Functional characterization of Arabidopsis HsfA6a as a heat-shock transcription factor under high salinity and dehydration conditions. Plant, Cell & Environment 37, 1202-1222.
52. Ikeda M. & Ohme-Takagi M. (2009) A novel group of transcriptional repressors in Arabidopsis. Plant and Cell Physiology 50, 970-975.
53. Ikeda M., Mitsuda N. & 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 Physiology 157, 1243-1254.
54. IPCC (2012) Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation (eds C.B. Field, V. Barros, T.F. Stocker, D. Qin, D.J. Dokken, K.L. Ebi, ... P.M. Midgley) A Special Report of Working Groups I and II of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge, UK.
55. Jiang C., Xu J., Zhang H., Zhang X., Shi J., Li M. & Ming F. (2009) A cytosolic class I small heat shock protein, RcHSP17.8, of Rosa chinensis confers resistance to a variety of stresses to Escherichia coli, yeast and Arabidopsis thaliana. Plant, Cell & Environment 32, 1046-1059.
56. Jung H.-S., Crisp P.A., Estavillo G.M., Cole B., Hong F., Mockler T.C., ... Chory J. (2013) Subset of heat-shock transcription factors required for the early response of Arabidopsis to excess light. Proceedings of the National Academy of Sciences of the United States of America 110, 14474-14479.
57. Katiyar-Agarwal S., Agarwal M. & Grover A. (2003) Heat-tolerant basmati rice engineered by over-expression of hsp101. Plant Molecular Biology 51, 677-686.
58. von Koskull-Döring P., Scharf K.D. & Nover L. (2007) The diversity of plant heat stress transcription factors. Trends in Plant Science 12, 452-457.
59. 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. The Plant Journal: For Cell and Molecular Biology 39, 98-112.
60. Kotak S., Larkindale J., Lee U., von Koskull-Doring P., Vierling E. & Scharf K.D. (2007a) Complexity of the heat stress response in plants. Current Opinion in Plant Biology 10, 310-316.
61. Kotak S., Vierling E., Bäumlein H. & von Koskull-Döring P. (2007b) A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. The Plant Cell 19, 182-195.
62. Krishna P. & Gloor G. (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress and Chaperones 6, 238-246.
63. Kumar M., Busch W., Birke H., Kemmerling B., Nürnberger T. & Schöffl F. (2009) Heat shock factors HsfB1 and HsfB2b are involved in the regulation of Pdf1.2 expression and pathogen resistance in Arabidopsis. Molecular Plant 2, 152-165.
64. Larkindale J. & Vierling E. (2008) Core genome responses involved in acclimation to high temperature. Plant Physiology 146, 748-761.
65. Lee U., Rioflorido I., Hong S.W., Larkindale J., Waters E.R. & Vierling E. (2007) The Arabidopsis ClpB/Hsp100 family of proteins: chaperones for stress and chloroplast development. The Plant Journal: For Cell and Molecular Biology 49, 115-127.
66. Lee U., Wie C., Fernandez B.O., Feelisch M. & Vierling E. (2008) Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis. The Plant Cell 20, 786-802.
67. Li S., Zhou X., Chen L., Huang W. & Yu D. (2010) Functional characterization of Arabidopsis thaliana WRKY39 in heat stress. Molecules and Cells 29, 475-483.
68. Li S., Liu J., Liu Z., Li X., Wu F. & He Y. (2014) HEAT-INDUCED TAS1 TARGET1 mediates thermotolerance via HEAT STRESS TRANSCRIPTION FACTOR A1a-directed pathways in Arabidopsis. The Plant Cell 26, 1764-1780.
69. 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, e54880.
70. Lin M.Y., Chai K.H., Ko S.S., Kuang L.Y., Lur H.S. & Charng Y.Y. (2014) A positive feedback loop between HEAT SHOCK PROTEIN101 and HEAT STRESS-ASSOCIATED 32-KD PROTEIN modulates long-term acquired thermotolerance illustrating diverse heat stress responses in rice varieties. Plant Physiology 164, 2045-2053.
71. Liu H. & Charng Y. (2012) Acquired thermotolerance independent of heat shock factor A1 (HsfA1), the master regulator of the heat stress response. Plant Signaling and Behavior 7, 547-550.
72. Liu H.C. & Charng Y.Y. (2013) Common and distinct functions of Arabidopsis class A1 and A2 heat shock factors in diverse abiotic stress responses and development. Plant Physiology 163, 276-290.
73. Liu H.C., Liao H.T. & Charng Y.Y. (2011) The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. Plant, Cell & Environment 34, 738-751.
74. Liu H.T., Li B., Shang Z.L., Li X.Z., Mu R.L., Sun D.Y. & Zhou R.G. (2003) Calmodulin is involved in heat shock signal transduction in wheat. Plant Physiology 132, 1186-1195.
75. Liu H.T., Gao F., Li G.L., Han J.L., Liu D.L., Sun D.Y. & Zhou R.G. (2008) The calmodulin-binding protein kinase 3 is part of heat-shock signal transduction in Arabidopsis thaliana. The Plant Journal: For Cell and Molecular Biology 55, 760-773.
76. Liu J., Sun N., Liu M., Liu J., Du B., Wang X. & Qi X. (2013) An autoregulatory loop controlling Arabidopsis HsfA2 expression: role of heat shock-induced alternative splicing. Plant Physiology 162, 512-521.
77. Liu J.G., Qin Q.L., Zhang Z., Peng R.H., Xiong A.S., Chen J.M. & Yao Q.H. (2009) OsHSF7 gene in rice, Oryza sativa L., encodes a transcription factor that functions as a high temperature receptive and responsive factor. BMB reports 42, 16-21.
78. Liu J.X., Srivastava R., Che P. & Howell S.H. (2007) An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. The Plant Cell 19, 4111-4119.
79. Liu Z.B., Wang J.M., Yang F.X., Yang L., Yue Y.F., Xiang J.B., ... Wu X.J. (2014) A novel membrane-bound E3 ubiquitin ligase enhances the thermal resistance in plants. Plant Biotechnology Journal 12, 93-104.
80. Lohmann C., Eggers-Schumacher G., Wunderlich M. & Schöffl F. (2004) Two different heat shock transcription factors regulate immediate early expression of stress genes in Arabidopsis. Molecular Genetics and Genomics: MGG 271, 11-21.
81. Lyck R., Harmening U., Höhfeld I., Treuter E., Scharf K.D. & Nover L. (1997) Intracellular distribution and identification of the nuclear localization signals of two plant heat-stress transcription factors. Planta 202, 117-125.
82. Mayer M.P. (2010) Gymnastics of molecular chaperones. Molecular Cell 39, 321-331.
83. Meiri D. & Breiman A. (2009) Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting the accumulation of HsfA2-regulated sHSPs. The Plant Journal: For Cell and Molecular Biology 59, 387-399.
84. Meiri D., Tazat K., Cohen-Peer R., Farchi-Pisanty O., Aviezer-Hagai K., Avni A. & Breiman A. (2010) Involvement of Arabidopsis ROF2 (FKBP65) in thermotolerance. Plant Molecular Biology 72, 191-203.
85. Milioni D. & Hatzopoulos P. (1997) Genomic organization of hsp90 gene family in Arabidopsis. Plant Molecular Biology 35, 955-961.
86. Mishra S.K., Tripp J., Winkelhaus S., Tschiersch B., Theres K., Nover L. & Scharf K.D. (2002) In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes and Development 16, 1555-1567.
87. Mittler R. & Blumwald E. (2010) Genetic engineering for modern agriculture: challenges and perspectives. Annual Review of Plant Biology 61, 443-462.
88. Mittler R., Finka A. & Goloubinoff P. (2012) How do plants feel the heat? Trends in Biochemical Sciences 37, 118-125.
89. Mogk A., Schlieker C., Friedrich K.L., Schönfeld H.-J., Vierling E. & Bukau B. (2003a) Refolding of substrates bound to small Hsps relies on a disaggregation reaction mediated most efficiently by ClpB/DnaK. The Journal of Biological Chemistry 278, 31033-31042.
90. Mogk A., Deuerling E., Vorderwülbecke S., Vierling E. & Bukau B. (2003b) Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Molecular Microbiology 50, 585-595.
91. Montero-Barrientos M., Hermosa R., Cardoza R.E., Gutiérrez S., Nicolás C. & Monte E. (2010) Transgenic expression of the Trichoderma harzianum hsp70 gene increases Arabidopsis resistance to heat and other abiotic stresses. Journal of Plant Physiology 167, 659-665.
92. Nakamoto H. & Vigh L. (2007) The small heat shock proteins and their clients. Cellular and Molecular Life Sciences 64, 294-306.
93. Neta-Sharir I., Isaacson T., Lurie S. & Weiss D. (2005) Dual role for tomato heat shock protein 21: protecting photosystem II from oxidative stress and promoting color changes during fruit maturation. The Plant Cell 17, 1829-1838.
94. Nieto-Sotelo J., Martínez L.M., Ponce G., Cassab G.I., Alagón A., Meeley R.B., ... Yang R. (2002) Maize HSP101 plays important roles in both induced and basal thermotolerance and primary root growth. The Plant Cell 14, 1621-1633.
95. Nishizawa A., Yabuta Y., Yoshida E., Maruta T., Yoshimura K. & Shigeoka S. (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. The Plant Journal: For Cell and Molecular Biology 48, 535-547.
96. Nishizawa-Yokoi A., Yoshida E., Yabuta Y. & Shigeoka S. (2009) Analysis of the regulation of target genes by an Arabidopsis heat shock transcription factor, HsfA2. Bioscience, Biotechnology, and Biochemistry 73, 890-895.
97. Nishizawa-Yokoi A., Nosaka R., Hayashi H., Tainaka H., Maruta T., Tamoi M., ... Yabuta Y. (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 and Cell Physiology 52, 933-945.
98. Nover L., Scharf K. & Neumann D. (1983) Formation of cytoplasmic heat shock granules in tomato cell cultures and leaves. Molecular and Cellular Biology 3, 1648-1655.
99. Nover L., Scharf K.D., Gagliardi D., Vergne P., Czarnecka-Verner E. & Gurley W.B. (1996) The Hsf world: classification and properties of plant heat stress transcription factors. Cell Stress and Chaperones 1, 215-223.
100. Nover L., Bharti K., Döring P., Mishra S.K., Ganguli A. & Scharf K.D. (2001) Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress and Chaperones 6, 177-189.
101. Ogawa D., Yamaguchi K. & Nishiuchi T. (2007) High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased themotolerance but also salt/osmotic stress tolerance and enhanced callus growth. Journal of Experimental Botany 58, 3373-3383.
102. Ono K., Hibino T., Kohinata T., Suzuki S., Tanaka Y., Nakamura T., ... Takabe T. (2001) Overexpression of DnaK from a halotolerant cyanobacterium Aphanothece halophytica enhances the high-temperature tolerance of tobacco during germination and early growth. Plant Science: An International Journal of Experimental Plant Biology 160, 455-461.
103. van Oosten-Hawle P., Porter R.S. & Morimoto R.I. (2013) Regulation of organismal proteostasis by transcellular chaperone signaling. Cell 153, 1366-1378.
104. Pajerowska-Mukhtar K.M., Wang W., Tada Y., Oka N., Tucker C.L., Fonseca J.P. & Dong X. (2012) The HSF-like transcription factor TBF1 is a major molecular switch for plant growth-to-defense transition. Current Biology 22, 103-112.
105. Pelham H.R. (1982) A regulatory upstream promoter element in the Drosophila hsp 70 heat-shock gene. Cell 30, 517-528.
106. Pick T., Jaskiewicz M., Peterhänsel C. & Conrath U. (2012) Heat shock factor HsfB1 primes gene transcription and systemic acquired resistance in Arabidopsis. Plant Physiology 159, 52-55.
107. Port M., Tripp J., Zielinski D., Weber C., Heerklotz D., Winkelhaus S., ... Scharf K.D. (2004) Role of Hsp17.4-CII as coregulator and cytoplasmic retention factor of tomato heat stress transcription factor HsfA2. Plant Physiology 135, 1457-1470.
108. Prieto-Dapena P., Castaño R., Almoguera C. & Jordano J. (2008) The ectopic overexpression of a seed-specific transcription factor, HaHSFA9, confers tolerance to severe dehydration in vegetative organs. The Plant Journal: For Cell and Molecular Biology 54, 1004-1014.
109. Qi Y., Wang H., Zou Y., Liu C., Liu Y., Wang Y. & Zhang W. (2011) Over-expression of mitochondrial heat shock protein 70 suppresses programmed cell death in rice. FEBS Letters 585, 231-239.
110. Qin F., Kakimoto M., Sakuma Y., Maruyama K., Osakabe Y., Tran L.S.P., ... Yamaguchi-Shinozaki K. (2007) Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. The Plant Journal: For Cell and Molecular Biology 50, 54-69.
111. Qu A.L., Ding Y.F., Jiang Q. & Zhu C. (2013) Molecular mechanisms of the plant heat stress response. Biochemical and Biophysical Research Communications 432, 203-207.
112. Queitsch C., Hong S.W., Vierling E. & Lindquist S. (2000) Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. The Plant Cell 12, 479-492.
113. Rana R.M., Dong S., Tang H., Ahmad F. & Zhang H. (2012) Functional analysis of OsHSBP1 and OsHSBP2 revealed their involvement in the heat shock response in rice (Oryza sativa L.). Journal of Experimental Botany 63, 6003-6016.
114. dos Reis S.P., Lima A.M. & de Souza C.R.B. (2012) Recent molecular advances on downstream plant responses to abiotic stress. International Journal of Molecular Sciences 13, 8628-8647.
115. Rhoads D.M., White S.J., Zhou Y., Muralidharan M. & Elthon T.E. (2005) Altered gene expression in plants with constitutive expression of a mitochondrial small heat shock protein suggests the involvement of retrograde regulation in the heat stress response. Physiologia Plantarum 123, 435-444.
116. Ruelland E. & Zachowski A. (2010) How plants sense temperature. Environmental and Experimental Botany 69, 225-232.
117. Sagor G., Berberich T., Takahashi Y., Niitsu M. & Kusano T. (2013) The polyamine spermine protects Arabidopsis from heat stress-induced damage by increasing expression of heat shock-related genes. Transgenic Research 22, 595-605.
118. Sakuma Y., Maruyama K., Osakabe Y., Qin F., Seki M., Shinozaki K. & Yamaguchi-Shinozaki K. (2006a) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. The Plant Cell 18, 1292-1309.
119. Sakuma Y., Maruyama K., Qin F., Osakabe Y., Shinozaki K. & Yamaguchi-Shinozaki K. (2006b) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proceedings of the National Academy of Sciences of the United States of America 103, 18822-18827.
120. Satyal S.H., Chen D., Fox S.G., Kramer J.M. & Morimoto R.I. (1998) Negative regulation of the heat shock transcriptional response by HSBP1. Genes and Development 12, 1962-1974.
121. Scharf K.D., Heider H., Höhfeld 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. Molecular and Cellular Biology 18, 2240-2251.
122. Scharf K.D., Berberich T., Ebersberger I. & Nover L. (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochimica et Biophysica Acta 1819, 104-119.
123. Scheufler C., Brinker A., Bourenkov G., Pegoraro S., Moroder L., Bartunik H., ... Moarefi I. (2000) Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101, 199-210.
124. Schleiff E. & Becker T. (2011) Common ground for protein translocation: access control for mitochondria and chloroplasts. Nature Reviews. Molecular Cell Biology 12, 48-59.
125. Schmidt R., Schippers J.H., Welker A., Mieulet D., Guiderdoni E. & Mueller-Roeber B. (2012) Transcription factor OsHsfC1b regulates salt tolerance and development in Oryza sativa ssp. japonica. AoB Plants 2012, pls011; doi:10.1093/aobpla/pls01.
126. 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 Molecular Biology 60, 759-772.
127. 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. The Plant Journal: For Cell and Molecular Biology 53, 264-274.
128. Schultheiss J., Kunert O., Gase U., Scharf K.D., Nover L. & Rüterjans H. (1996) Solution structure of the DNA-binding domain of the tomato heat-stress transcription factor HSF24. European Journal of Biochemistry 236, 911-921.
129. Sekhar K., Priyanka B., Reddy V.D. & Rao K.V. (2010) Isolation and characterization of a pigeonpea cyclophilin (CcCYP) gene, and its over-expression in Arabidopsis confers multiple abiotic stress tolerance. Plant, Cell & Environment 33, 1324-1338.
130. Seyffer F., Kummer E., Oguchi Y., Winkler J., Kumar M., Zahn R., ... Mogk A. (2012) Hsp70 proteins bind Hsp100 regulatory M domains to activate AAA+ disaggregase at aggregate surfaces. Nature Structural and Molecular Biology 19, 1347-1355.
131. Shahnejat-Bushehri S., Mueller-Roeber B. & Balazadeh S. (2012) Arabidopsis NAC transcription factor JUNGBRUNNEN1 affects thermomemory-associated genes and enhances heat stress tolerance in primed and unprimed conditions. Plant Signaling and Behavior 7, 1518-1521.
132. Shen Z., Ding M., Sun J., Deng S., Zhao R., Wang M., ... Qian Z. (2013) Overexpression of PeHSF mediates leaf ROS homeostasis in transgenic tobacco lines grown under salt stress conditions. Plant Cell, Tissue and Organ Culture (PCTOC) 115, 299-308.
133. Shim D., Hwang J.U., Lee J., Lee S., Choi Y., An G., ... Lee Y. (2009) Orthologs of the class A4 heat shock transcription factor HsfA4a confer cadmium tolerance in wheat and rice. The Plant Cell 21, 4031-4043.
134. Stankiewicz M., Nikolay R., Rybin V. & Mayer M.P. (2010) CHIP participates in protein triage decisions by preferentially ubiquitinating Hsp70-bound substrates. The FEBS Journal 277, 3353-3367.
135. Su P.H. & Li H.M. (2010) Stromal Hsp70 is important for protein translocation into pea and Arabidopsis chloroplasts. The Plant Cell 22, 1516-1531.
136. Sugio A., Dreos R., Aparicio F. & Maule A.J. (2009) The cytosolic protein response as a subcomponent of the wider heat shock response in Arabidopsis. The Plant Cell 21, 642-654.
137. Sung D.Y. & Guy C.L. (2003) Physiological and molecular assessment of altered expression of Hsc70-1 in Arabidopsis. Evidence for pleiotropic consequences. Plant Physiology 132, 979-987.
138. 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 Physiology 139, 1313-1322.
139. Suzuki N., Bajad S., Shuman J., Shulaev V. & Mittler R. (2008) The transcriptional co-activator MBF1c is a key regulator of thermotolerance in Arabidopsis thaliana. The Journal of Biological Chemistry 283, 9269-9275.
140. Suzuki N., Sejima H., Tam R., Schlauch K. & Mittler R. (2011) Identification of the MBF1 heat-response regulon of Arabidopsis thaliana. The Plant Journal: For Cell and Molecular Biology 66, 844-851.
141. Taipale M., Jarosz D.F. & Lindquist S. (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nature Reviews. Molecular Cell Biology 11, 515-528.
142. Tejedor-Cano J., Prieto-Dapena P., Almoguera C., Carranco R., Hiratsu K., Ohme-Takagi M. & Jordano J. (2010) Loss of function of the HSFA9 seed longevity program. Plant, Cell & Environment 33, 1408-1417.
143. Tejedor-Cano J., Carranco R., Personat J.-M., Prieto-Dapena P., Almoguera C., Espinosa J.M. & Jordano J. (2014) A passive repression mechanism that hinders synergic transcriptional activation by heat shock factors involved in sunflower seed longevity. Molecular Plant 7, 256-259.
144. Tripp J., Mishra S.K. & Scharf K.D. (2009) Functional dissection of the cytosolic chaperone network in tomato mesophyll protoplasts. Plant, Cell & Environment 32, 123-133.
145. Uchida A., Hibino T., Shimada T., Saigusa M., Takabe T., Araki E., ... Takabe T. (2008) Overexpression of DnaK chaperone from a halotolerant cyanobacterium Aphanothece halophytica increases seed yield in rice and tobacco. Plant Biotechnology 25, 141-150.
146. Vierling E. (1991) The roles of heat shock proteins in plants. Annual Review of Plant Biology 42, 579-620.
147. Wahid A., Gelani S., Ashraf M. & Foolad M. (2007) Heat tolerance in plants: an overview. Environmental and Experimental Botany 61, 199-223.
148. Wang H., Bian M., Yang Z., Lin C. & Shi W. (2013) Preliminary functional analysis of the isoforms of OsHsfA2a (Oryza sativa L.) generated by alternative splicing. Plant Molecular Biology Reporter 31, 38-46.
149. Wang W., Vinocur B., Shoseyov O. & Altman A. (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends in Plant Science 9, 244-252.
150. Wu A., Allu A.D., Garapati P., Siddiqui H., Dortay H., Zanor M.-I., ... Tohge T. (2012a) JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. The Plant Cell 24, 482-506.
151. Wu Q., Lin J., Liu J.Z., Wang X., Lim W., Oh M., ... Cheng N.H. (2012b) Ectopic expression of Arabidopsis glutaredoxin AtGRXS17 enhances thermotolerance in tomato. Plant Biotechnology Journal 10, 945-955.
152. Wu T.Y., Juan Y.T., Hsu Y.H., Wu S.H., Liao H.T., Fung R.W. & Charng Y.Y. (2013) Interplay between heat shock proteins HSP101 and HSA32 prolongs heat acclimation memory posttranscriptionally in Arabidopsis. Plant Physiology 161, 2075-2084.
153. Wu X., Shiroto Y., Kishitani S., Ito Y. & Toriyama K. (2009) Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Reports 28, 21-30.
154. Xiang J., Ran J., Zou J., Zhou X., Liu A., Zhang X., ... Chen X. (2013) Heat shock factor OsHsfB2b negatively regulates drought and salt tolerance in rice. Plant Cell Reports 32, 1795-1806.
155. Yamanouchi U., Yano M., Lin H., Ashikari M. & Yamada K. (2002) A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. Proceedings of the National Academy of Sciences of the United States of America 99, 7530-7535.
156. Yan J., Wang J., Li Q., Hwang J.R., Patterson C. & Zhang H. (2003) AtCHIP, a U-box-containing E3 ubiquitin ligase, plays a critical role in temperature stress tolerance in Arabidopsis. Plant Physiology 132, 861-869.
157. 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, 957-967.
158. Yoshida T., Sakuma Y., Todaka D., Maruyama K., Qin F., Mizoi J., ... Yamaguchi-Shinozaki K. (2008) Functional analysis of an Arabidopsis heat-shock transcription factor HsfA3 in the transcriptional cascade downstream of the DREB2A stress-regulatory system. Biochemical and Biophysical Research Communications 368, 515-521.
159. Yoshida T., Ohama N., Nakajima J., Kidokoro S., Mizoi J., Nakashima K., ... Todaka D. (2011) Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression. Molecular Genetics and Genomics 286, 321-332.
160. Zhang L., Li Y., Xing D. & Gao C. (2009a) Characterization of mitochondrial dynamics and subcellular localization of ROS reveal that HsfA2 alleviates oxidative damage caused by heat stress in Arabidopsis. Journal of Experimental Botany 60, 2073-2091.
161. Zhang W., Zhou R.-G., Gao Y.-J., Zheng S.-Z., Xu P., Zhang S.-Q. & Sun D.-Y. (2009b) Molecular and genetic evidence for the key role of AtCaM3 in heat-shock signal transduction in Arabidopsis. Plant Physiology 149, 1773-1784.
162. Zhou J., Zhang Y., Qi J., Chi Y., Fan B., Yu J.Q. & Chen Z. (2014) E3 ubiquitin ligase CHIP and NBR1-mediated selective autophagy protect additively against proteotoxicity in plant stress responses. PLoS Genetics 10, e1004116.
163. Zhou Y., Chen H., Chu P., Li Y., Tan B., Ding Y., ... Huang S. (2012) NnHSP17.5, a cytosolic class II small heat shock protein gene from Nelumbo nucifera, contributes to seed germination vigor and seedling thermotolerance in transgenic Arabidopsis. Plant Cell Reports 31, 379-389.
164. Zhu B., Ye C., Lü 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). Journal of Plant Research 119, 247-256.
165. Zhu X., Thalor S.K., Takahashi Y., Berberich T. & Kusano T. (2012) An inhibitory effect of the sequence-conserved upstream open-reading frame on the translation of the main open-reading frame of HsfB1 transcripts in Arabidopsis. Plant, Cell & Environment 35, 2014-2030.
166. Zinn K.E., Tunc-Ozdemir M. & Harper J.F. (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. Journal of Experimental Botany 61, 1959-1968.