Multi-level interactions between heat shock factors, heat shock proteins, and the redox system regulate acclimation to heat

Frontiers in Plant Science

Volumn 6, Issue NOVEMBER, 2015, Pages

  Driedonks, Nicky ^a   Xu, Jiemeng ^a   Peters, Janny L ^a   Park, Sunghun ^b   Rieu, Ivo ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b KANSAS STATE UNIVERSITY   (United States)

Author keywords

Cross talk; Heat response; Heat shock factor; Heat shock protein; Interaction; Reactive oxygen species; ROS scavenging; Signaling

Indexed keywords

EID: 84947579084     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00999     Document Type: Review

References (131)

1. Ahn, S.-G., and Thiele, D. J. (2003). Redox regulation of mammalian heat shock factor 1 is essential for Hsp gene activation and protection from stress. Genes Dev. 17, 516-528. doi: 10.1101/gad.1044503
2. Almeselmani, M., Deshmukh, P., Sairam, R., Kushwaha, S., and Singh, T. (2006). Protective role of antioxidant enzymes under high temperature stress. Plant Sci. 171, 382-388. doi: 10.1016/j.plantsci.2006.04.009
3. Apel, K., and Hirt, H. (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373-399. doi: 10.1146/annurev.arplant.55.031903.141701
4. Badiani, M., Schenone, G., Paolacci, A. R., and Fumagalli, I. (1993). Daily fluctuations of antioxidants in bean (Phaseolus vulgaris L.) leaves as affected by the presence of ambient air pollutants. Plant Cell Physiol. 34, 271-279.
5. Baker, C. J., and Orlandi, E. W. (1995). Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 33, 299-321. doi: 10.1146/annurev.py.33.090195.001503
6. Banti, V., Loreti, E., Novi, G., Santaniello, A., Alpi, A., and Perata, P. (2008). Heat acclimation and cross-tolerance against anoxia in Arabidopsis. Plant Cell Environ. 31, 1029-1037. doi: 10.1111/j.1365-3040.2008.01816.x
7. Banti, V., Mafessoni, F., Loreti, E., Alpi, A., and Perata, P. (2010). The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiol.152, 1471-1483. doi: 10.1104/pp.109.149815
8. Bartoli, C. G., Casalongué, C. A., Simontacchi, M., Marquez-Garcia, B., and Foyer, C. H. (2013). Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environ. Exp. Bot. 94, 73-88. doi: 10.1016/j.envexpbot.2012.05.003
9. Bartoli, C. G., Pastori, G. M., and Foyer, C. H. (2000). Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV.Plant Physiol. 123, 335-344.
10. Bechtold, U., Albihlal, W. S., Lawson, T., Fryer, M. J., Sparrow, P. A., Richard, F., et al. (2013). Arabidopsis HEAT SHOCK TRANSCRIPTION FACTORA1b overexpression enhances water productivity, resistance to drought, and infection. J. Exp. Bot. 64, 3467-3481. doi: 10.1093/jxb/ert185
11. Bekh-Ochir, D., Shimada, S., Yamagami, A., Kanda, S., Ogawa, K., Nakazawa, M., et al. (2013). A novel mitochondrial DnaJ/Hsp40 family protein BIL2 promotes plant growth and resistance against environmental stress in brassinosteroid signaling.Planta 237, 1509-1525. doi: 10.1007/s00425-013-1859-3
12. Bhattacharjee, S. (2012). An inductive pulse of hydrogen peroxide pretreatment restores redox-homeostasis and oxidative membrane damage under extremes of temperature in two rice cultivars. Plant Growth Regul. 68, 395-410. doi: 10.1007/s10725-012-9728-9
13. Bhattacharjee, S. (2013). Heat and chilling induced disruption of redox homeostasis and its regulation by hydrogen peroxide in germinating rice seeds (Oryza sativa L., Cultivar Ratna). Physiol. Mol. Biol. Plants 19, 199-207. doi: 10.1007/s12298-012-0159-x
14. Bokszczanin, K. L., Solanaceae PollenThermotolerance Initial Training Network (SPOT-ITN) Consortium, and Fragkostefanakis, S. (2013). Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance.Front. Plant Sci. 4:315. doi: 10.3389/fpls.2013.00315
15. Boston, R. S., Viitanen, P. V., and Vierling, E. (1996). Molecular chaperones and protein folding in plants. Plant Mol. Biol. 32, 191-222.
16. Bowler, C., Montagu, M. V., and Inze, D. (1992). Superoxide dismutase and stress tolerance. Annu. Rev. Plant Biol. 43, 83-116. doi: 10.1146/annurev.pp.43.060192.000503
17. Byth-Illing, H.-A., and Bornman, L. (2013). Heat shock, with recovery, promotes protection of Nicotiana tabacum during subsequent exposure to Ralstonia solanacearum. Cell Stress Chaperones 19, 193-203. doi: 10.1007/s12192-013-0445-8
18. Chaitanya, K., Sundar, D., Masilamani, S., and Reddy, A. R. (2002). Variation in heat stress-induced antioxidant enzyme activities among three mulberry cultivars. Plant Growth Regul. 36, 175-180. doi: 10.1023/A:1015092628374
19. Chao, Y.-Y., Hsu, Y., and Kao, C. (2009). Involvement of glutathione in heat shock- and hydrogen peroxide-induced cadmium tolerance of rice (Oryza sativa L.) seedlings.Plant Soil 318, 37-45. doi: 10.1007/s11104-008-9815-x
20. Chauhan, H., Khurana, N., Agarwal, P., Khurana, J., and 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. doi: 10.1371/journal.pone.0079577
21. Chen, S., Liu, A., Zhang, S., Li, C., Chang, R., Liu, D., et al. (2013). Overexpression of mitochondrial uncoupling protein conferred resistance to heat stress and Botrytis cinerea infection in tomato. Plant Physiol. Biochem. 73, 245-253. doi: 10.1016/j.plaphy.2013.10.002
22. Chou, T.-S., Chao, Y.-Y., and Kao, C. H. (2012). Involvement of hydrogen peroxide in heat shock-and cadmium-induced expression of ascorbate peroxidase and glutathione reductase in leaves of rice seedlings. J. Plant Physiol. 169, 478-486. doi: 10.1016/j.jplph.2011.11.012
23. Chu, B., Soncin, F., Price, B. D., Stevenson, M. A., and Calderwood, S. K. (1996). Sequential phosphorylation by mitogen-activated protein kinase and glycogen synthase kinase 3 represses transcriptional activation by heat shock factor-1. J. Biol. Chem. 271, 30847-30857. doi: 10.1074/jbc.271.48.30847
24. Clarke, S. M., Mur, L. A., Wood, J. E., and Scott, I. M. (2004). Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. Plant J. 38, 432-447. doi: 10.1111/j.1365-313X.2004.02054.x
25. Cohu, C. M., Abdel-Ghany, S. E., Reynolds, K. A. G., Onofrio, A. M., Bodecker, J. R., Kimbrel, J. A., et al. (2009). Copper delivery by the copper chaperone for chloroplast and cytosolic copper/zinc-superoxide dismutases: regulation and unexpected phenotypes in an Arabidopsis mutant. Mol. Plant 2, 1336-1350. doi: 10.1093/mp/ssp084
26. Das, K., and Roychoudhury, A. (2014). Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front. Environ. Sci. 2:53. doi: 10.3389/fenvs.2014.00053
27. Dat, J. F., Foyer, C. H., and Scott, I. M. (1998). Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. Plant Physiol. 118, 1455-1461. doi: 10.1104/pp.118.4.1455
28. 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
29. del Rio, L. A., Sandalio, L. M., Corpas, F. J., Palma, J. M., and Barroso, J. B. (2006). Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol. 141, 330-335. doi: 10.1104/pp.106.078204
30. de Pinto, M. C., Locato, V., Paradiso, A., and De Gara, L. (2015). Role of redox homeostasis in thermo-tolerance under a climate change scenario. Ann. Bot. 116, 487-496. doi: 10.1093/aob/mcv071
31. Desikan, R., Hancock, J., and Neill, S. (2004). "Oxidative stress signalling," in Plant Responses to Abiotic Stress, eds H. Hirt, and K. Shinozaki (Berlin: Springer), 121-149.
32. Desikan, R., Soheila, A.-H., Hancock, J. T., and Neill, S. J. (2001). Regulation of theArabidopsis transcriptome by oxidative stress. Plant Physiol. 127, 159-172. doi: 10.1104/pp.127.1.159
33. Dong, X., Yi, H., Lee, J., Nou, I.-S., Han, C.-T., and Hur, Y. (2015). Global gene-expression analysis to identify differentially expressed genes critical for the heat stress response in Brassica rapa. PLoS ONE 10:e0130451. doi: 10.1371/journal.pone.0130451
34. Evrard, A., Kumar, M., Lecourieux, D., Lucks, J., von Koskull-Döring, P., and Hirt, H. (2013). Regulation of the heat stress response in Arabidopsis by MPK6-targeted phosphorylation of the heat stress factor HsfA2. PeerJ 1, e59. doi: 10.7717/peerj.59
35. Foyer, C., and Noctor, G. (2005). Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell17, 1866-1875. doi: 10.1105/tpc.105.033589
36. Foyer, C. H., and Noctor, G. (2009). Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid. Redox Signal. 11, 861-905. doi: 10.1089/ars.2008.2177
37. Frank, G., Pressman, E., Ophir, R., Althan, L., Shaked, R., Freedman, M., et al. (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. J. Exp. Bot. 60, 3891-3908. doi: 10.1093/jxb/erp234
38. Galvez-Valdivieso, G., and Mullineaux, P. (2010). The role of reactive oxygen species in signalling from chloroplasts to the nucleus. Physiol. Plant. 138, 430-439. doi: 10.1111/j.1399-3054.2009.01331.x
39. Gechev, T. S., and Hille, J. (2005). Hydrogen peroxide as a signal controlling plant programmed cell death. J. Cell Biol. 168, 17-20. doi: 10.1083/jcb.200409170
40. Giardi, M. T., Masojidek, J., and Godde, D. (1997). Effects of abiotic stresses on the turnover of the D1 reaction centre II protein. Physiol. Plant. 101, 635-642. doi: 10.1111/j.1399-3054.1997.tb01048.x
41. 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
42. Guan, Q., Lu, X., Zeng, H., Zhang, Y., and Zhu, J. (2013). Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis.Plant J. 74, 840-851. doi: 10.1111/tpj.12169
43. Gupta, A. S., Webb, R. P., Holaday, A. S., and Allen, R. D. (1993). Overexpression of superoxide dismutase protects plants from oxidative stress (induction of ascorbate peroxidase in superoxide dismutase-overexpressing plants). Plant Physiol. 103, 1067-1073.
44. Hasanuzzaman, M., Hossain, M. A., da Silva, J. A. T., and Fujita, M. (2012). "Plant response and tolerance to abiotic oxidative stress: antioxidant defense is a key factor," in Crop Stress and its Management: Perspectives and Strategies, eds B. Venkateswarlu, A. K. Shanker, C. Shanker, and M. Maheswari (New York: Springer), 261-315.
45. Hasanuzzaman, M., Nahar, K., Alam, M. M., Roychowdhury, R., and Fujita, M. (2013). Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int. J. Mol. Sci. 14, 9643-9684. doi: 10.3390/ijms14059643
46. He, Y., Liu, Y., Cao, W., Huai, M., Xu, B., and Huang, B. (2005). Effects of salicylic acid on heat tolerance associated with antioxidant metabolism in Kentucky bluegrass.Crop Sci. 45, 988-995. doi: 10.2135/cropsci2003.0678
47. Hossain, M. A., Bhattacharjee, S., Armin, S., Qian, P., Xin, W., Li, H., et al. (2015). Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front. Plant Sci. 6:420. doi: 10.3389/fpls.2015.00420
48. Hossain, M. A., Mostofa, M. G., and Fujita, M. (2013). Cross protection by cold-shock to salinity and drought stress-induced oxidative stress in mustard (Brassica campestris L.) seedlings. Mol. Plant Breed. 4, 50-70. doi: 10.5376/mpb.2013.04.0007
49. Hübel, A., and Schöffl, F. (1994). Arabidopsis heat shock factor: isolation and characterization of the gene and the recombinant protein. Plant Mol. Biol. 26, 353-362. doi: 10.1007/BF00039545
50. Jammes, F., Song, C., Shin, D., Munemasa, S., Takeda, K., Gu, D., et al. (2009). MAP kinases MPK9 and MPK12 are preferentially expressed in guard cells and positively regulate ROS-mediated ABA signaling. Proc. Natl. Acad. Sci. U.S.A. 106, 20520-20525. doi: 10.1073/pnas.0907205106
51. Jiang, C., Xu, J., Zhang, H., Zhang, X., Shi, J., Li, M., et al. (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 Environ. 32, 1046-1059. doi: 10.1111/j.1365-3040.2009.01987.x
52. Jiang, M., and Zhang, J. (2002). Involvement of plasma-membrane NADPH oxidase in abscisic acid-and water stress-induced antioxidant defense in leaves of maize seedlings. Planta 215, 1022-1030. doi: 10.1007/s00425-002-0829-y
53. 2 pre-applied leaves of cucumber and tomato seedlings. J. Jpn. Soc. Hort. Sci. 78, 320-329. doi: 10.2503/jjshs1.78.320
54. Kim, D., Kim, S., and Li, G. (1999). Proteasome inhibitors MG132 and lactacystin hyperphosphorylate HSF1 and induce hsp70 and hsp27 expression. Biochem. Biophys. Res. Commun. 254, 264-268. doi: 10.1006/bbrc.1998.9840
55. Kliebenstein, D. J., Monde, R.-A., and Last, R. L. (1998). Superoxide dismutase inArabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol. 118, 637-650. doi: 10.1104/pp.118.2.637
56. Knauf, U., Newton, E. M., Kyriakis, J., and Kingston, R. E. (1996). Repression of human heat shock factor 1 activity at control temperature by phosphorylation. Genes Dev. 10, 2782-2793. doi: 10.1101/gad.10.21.2782
57. Kong, F., Deng, Y., Wang, G., Wang, J., Liang, X., and Meng, Q. (2014a). LeCDJ1, a chloroplast DnaJ protein, facilitates heat tolerance in transgenic tomatoes. J. Integr. Plant Biol. 56, 63-74. doi: 10.1111/jipb.12119
58. Kong, F., Deng, Y., Zhou, B., Wang, G., Wang, Y., and Meng, Q. (2014b). A chloroplast-targeted DnaJ protein contributes to maintenance of photosystem II under chilling stress. J. Exp. Bot. 65, 143-158. doi: 10.1093/jxb/ert357
59. Kotak, S., Larkindale, J., Lee, U., von Koskull-Döring, P., Vierling, E., and Scharf, K.-D. (2007). Complexity of the heat stress response in plants. Curr. Opin. Plant Biol. 10, 310-316. doi: 10.1016/j.pbi.2007.04.011
60. Kovtun, Y., Chiu, W.-L., Tena, G., and Sheen, J. (2000). Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl. Acad. Sci. U.S.A. 97, 2940-2945. doi: 10.1073/pnas.97.6.2940
61. Krasensky, J., and Jonak, C. (2012). Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J. Exp. Bot. 63, 1593-1608. doi: 10.1093/jxb/err460
62. Kreslavski, V. D., Los, D. A., Allakhverdiev, S. I., and Vl, V. K. (2012). Signaling role of reactive oxygen species in plants under stress. Russ. J. Plant Physiol. 59, 163-178. doi: 10.1134/S1021443712020057
63. Kwak, J. M., Nguyen, V., and Schroeder, J. I. (2006). The role of reactive oxygen species in hormonal responses. Plant Physiol. 141, 323-329. doi: 10.1104/pp.106.079004
64. Larkindale, J., Hall, J. D., Knight, M. R., and Vierling, E. (2005). Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol. 138, 882-897. doi: 10.1104/pp.105.062257
65. Larkindale, J., and Knight, M. R. (2002). Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol. 128, 682-695. doi: 10.1104/pp.010320
66. Li, C., Chen, Q., Gao, X., Qi, B., Chen, N., Xu, S., et al. (2005). AtHsfA2 modulates expression of stress responsive genes and enhances tolerance to heat and oxidative stress in Arabidopsis. Sci. China C Life Sci. 48, 540-550.
67. Li, W., Wei, Z., Qiao, Z., Wu, Z., Cheng, L., and Wang, Y. (2013). Proteomics analysis of alfalfa response to heat stress. PLoS ONE 8:e82725. doi: 10.1371/journal.pone.0082725
68. Link, V., Sinha, A., Vashista, P., Hofmann, M., Proels, R., Ehness, R., et al. (2002). A heat-activated MAP kinase in tomato: a possible regulator of the heat stress response.FEBS Lett. 531, 179-183. doi: 10.1016/S0014-5793(02)03498-1
69. Liu, Y., Zhang, C., Chen, J., Guo, L., Li, X., Li, W., et al. (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
70. Lohmann, C., Eggers-Schumacher, G., Wunderlich, M., and Schöffl, F. (2004). Two different heat shock transcription factors regulate immediate early expression of stress genes in Arabidopsis. Mol. Genet. Genomics 271, 11-21. doi: 10.1007/s00438-003-0954-8
71. Loreti, E., Poggi, A., Novi, G., Alpi, A., and Perata, P. (2005). A genome-wide analysis of the effects of sucrose on gene expression in Arabidopsis seedlings under anoxia.Plant Physiol. 137, 1130-1138. doi: 10.1104/pp.104.057299
72. Miller, G., and Mittler, R. (2006). Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann. Bot. 98, 279-288. doi: 10.1093/aob/mcl107
73. Miller, G., Schlauch, K., Tam, R., Cortes, D., Torres, M. A., Shulaev, V., et al. (2009). The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2, ra45. doi: 10.1126/scisignal.2000448
74. Mittal, D., Madhyastha, D., and Grover, A. (2012). Genome-wide transcriptional profiles during temperature and oxidative stress reveal coordinated expression patterns and overlapping regulons in rice. PLoS ONE 7:e40899. doi: 10.1371/journal.pone.0040899
75. Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405-410. doi: 10.1016/S1360-1385(02)02312-9
76. Mittler, R., Vanderauwera, S., Gollery, M., and Van Breusegem, F. (2004). Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490-498. doi: 10.1016/j.tplants.2004.08.009
77. Mittler, R., Vanderauwera, S., Suzuki, N., Miller, G., Tognetti, V. B., Vandepoele, K., et al. (2011). ROS signaling: the new wave? Trends Plant Sci. 16, 300-309. doi: 10.1016/j.tplants.2011.03.007
78. Moon, H., Lee, B., Choi, G., Shin, D., Prasad, D. T., Lee, O., et al. (2003). NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proc. Natl. Acad. Sci. U.S.A. 100, 358-363. doi: 10.1073/pnas.252641899
79. Morgan, R. W., Christman, M. F., Jacobson, F. S., Storz, G., and Ames, B. N. (1986). Hydrogen peroxide-inducible proteins in Salmonella typhimurium overlap with heat shock and other stress proteins. Proc. Natl. Acad. Sci. U.S.A. 83, 8059-8063. doi: 10.1073/pnas.83.21.8059
80. Morimoto, R. (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, 3788-3796. doi: 10.1101/gad.12.24.3788
81. Mostofa, M. G., Yoshida, N., and Fujita, M. (2014). Spermidine pretreatment enhances heat tolerance in rice seedlings through modulating antioxidative and glyoxalase systems. Plant Growth Regul. 73, 31-44. doi: 10.1007/s10725-013-9865-9
82. Munns, R., and Tester, M. (2008). Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651-681. doi: 10.1146/annurev.arplant.59.032607.092911
83. Navrot, N., Rouhier, N., Gelhaye, E., and Jacquot, J. (2007). Reactive oxygen species generation and antioxidant systems in plant mitochondria. Physiol. Plant. 129, 185-195. doi: 10.1111/j.1399-3054.2006.00777.x
84. Nishizawa, A., Yabuta, Y., Yoshida, E., Maruta, T., Yoshimura, K., and Shigeoka, S. (2006). Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J. 48, 535-547.
85. Nishizawa, A., Yabuta, Y., and Shigeoka, S. (2008). Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 147, 1251-1263. doi: 10.1104/pp.108.122465
86. O'Kane, D., Gill, V., Boyd, P., and Burdon, R. (1996). Chilling, oxidative stress and antioxidant responses in Arabidopsis thaliana callus. Planta 198, 371-377. doi: 10.1007/BF00620053
87. Panchuk, I. I., Volkov, R. A., and Schöffl, F. (2002). Heat stress-and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase inArabidopsis. Plant Physiol. 129, 838-853. doi: 10.1104/pp.001362
88. Pastori, G., and Foyer, C. (2002). Common components, networks, and pathways of cross-tolerance to stress. The central role of "redox" and abscisic acid-mediated controls. Plant Physiol. 129, 460-468. doi: 10.1104/pp.011021
89. Pelham, H. R. (1982). A regulatory upstream promoter element in the Drosophila hsp 70 heat-shock gene. Cell 30, 517-528. doi: 10.1016/0092-8674(82)90249-5
90. Pérez-Salamó, I., Papdi, C., Gábor, R., Zsigmond, L., Vilela, B., Lumbreras, V., et al. (2014). The Heat Shock Factor HSFA4A confers salt tolerance and is regulated by oxidative stress and the MAP kinases, MPK3 and MPK6. Plant Physiol. 165, 319-334. doi: 10.1104/pp.114.237891
91. Petrov, V. D., and Van Breusegem, F. (2012). Hydrogen peroxide-a central hub for information flow in plant cells. AoB Plants 2012, pls014. doi: 10.1093/aobpla/pls014
92. Pnueli, L., Liang, H., Rozenberg, M., and Mittler, R. (2003). Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants. Plant J. 34, 187-203. doi: 10.1046/j.1365-313X.2003.01715.x
93. Pucciariello, C., Banti, V., and Perata, P. (2012). ROS signaling as common element in low oxygen and heat stresses. Plant Physiol. Biochem. 59, 3-10. doi: 10.1016/j.plaphy.2012.02.016
94. Qiu, X.-B., Shao, Y.-M., Miao, S., and Wang, L. (2006). The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cell. Mol. Life Sci.63, 2560-2570. doi: 10.1007/s00018-006-6192-6
95. Rainwater, D., Gossett, D., Millhollon, E., Hanna, H., Banks, S., and Lucas, M. (1996). The relationship between yield and the antioxidant defense system in tomatoes grown under heat stress. Free Radic. Res. 25, 421-435. doi: 10.3109/10715769609149065
96. Reddy, R., Kumar, B., Reddy, P., Mishra, R., Mahanty, S., Kaul, T., et al. (2009). Molecular cloning and characterization of genes encoding Pennisetum glaucumascorbate peroxidase and heat-shock factor: interlinking oxidative and heat-stress responses. J. Plant Physiol. 166, 1646-1659. doi: 10.1016/j.jplph.2009.04.007
97. Rentel, M. C., Lecourieux, D., Ouaked, F., Usher, S. L., Petersen, L., Okamoto, H., et al. (2004). OXI1 kinase is necessary for oxidative burst-mediated signalling inArabidopsis. Nature 427, 858-861. doi: 10.1038/nature02353
98. Rizhsky, L., Davletova, S., Liang, H., and Mittler, R. (2004). The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J. Biol. Chem. 279, 11736-11743. doi: 10.1074/jbc.M313350200
99. Rizhsky, L., Hallak-Herr, E., Van Breusegem, F., Rachmilevitch, S., Barr, J. E., Rodermel, S., et al. (2002). Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J. 32, 329-342. doi: 10.1046/j.1365-313X.2002.01427.x
100. Rui, R., Nie, Y., and Tong, H. (1990). SOD activity as a parameter for screening stress-tolerant germplasm resources in sweet potato (Ipomoea batatas L.). Jiangsu J. Agric. Sci. 6, 52-56.
101. Sairam, R., Srivastava, G., and Saxena, D. (2000). Increased antioxidant activity under elevated temperatures: a mechanism of heat stress tolerance in wheat genotypes. Biol. Plant. 43, 245-251. doi: 10.1023/A:1002756311146
102. 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
103. Schöffl, F., Prändl, R., and Reindl, A. (1998). Regulation of the heat-shock response.Plant Physiol. 117, 1135-1141. doi: 10.1104/pp.117.4.1135
104. Schöffl, F., Prändl, R., and Reindl, A. (1999). "Molecular responses to heat stress," inMolecular Responses to Cold, Drought, Heat and Salt Stress in Higher Plants, K. Yamaguchi-Shinozai and K. Shinozaki (Austin, TX: Landes Co.), 81-98.
105. Schramm, F., Ganguli, A., Kiehlmann, E., Englich, G., Walch, D., and 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, 759-772. doi: 10.1007/s11103-005-5750-x
106. Sgobba, A., Paradiso, A., Dipierro, S., De Gara, L., and de Pinto, M. C. (2015). Changes in antioxidants are critical in determining cell responses to short- and long-term heat stress. Physiol. Plant. 153, 68-78. doi: 10.1111/ppl.12220
107. Shen, Z., Ding, M., Sun, J., Deng, S., Zhao, R., Wang, M., et al. (2013). Overexpression of PeHSF mediates leaf ROS homeostasis in transgenic tobacco lines grown under salt stress conditions. Plant Cell Tissue Organ Cult. 115, 299-308. doi: 10.1007/s11240-013-0362-7
108. Storozhenko, S., De Pauw, P., Van Montagu, M., Inzé, D., and Kushnir, S. (1998). The heat-shock element is a functional component of the Arabidopsis APX1 gene promoter. Plant Physiol. 118, 1005-1014. doi: 10.1104/pp.118.3.1005
109. Sun, L., Liu, Y., Kong, X., Zhang, D., Pan, J., Zhou, Y., et al. (2012). ZmHSP16.9, a cytosolic class I small heat shock protein in maize (Zea mays), confers heat tolerance in transgenic tobacco. Plant Cell Rep. 31, 1473-1484. doi: 10.1007/s00299-012-1262-8
110. Sunkar, R., Kapoor, A., and Zhu, J.-K. (2006). Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18, 2051-2065. doi: 10.1105/tpc.106.041673
111. Suzuki, N., Miller, G., Sejima, H., Harper, J., and Mittler, R. (2013). Enhanced seed production under prolonged heat stress conditions in Arabidopsis thaliana plants deficient in cytosolic ascorbate peroxidase 2. J. Exp. Bot. 64, 253-263. doi: 10.1093/jxb/ers335
112. Suzuki, N., Rivero, R. M., Shulaev, V., Blumwald, E., and Mittler, R. (2014). Abiotic and biotic stress combinations. New Phytol. 203, 32-43. doi: 10.1111/nph.12797
113. Swindell, W., Huebner, M., and Weber, A. (2007). Transcriptional profiling ofArabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 8:125. doi: 10.1186/1471-2164-8-125
114. Torres, M. A., and Dangl, J. L. (2005). Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr. Opin. Plant Biol. 8, 397-403. doi: 10.1016/j.pbi.2005.05.014
115. Uchida, A., Jagendorf, A. T., Hibino, T., Takabe, T., and Takabe, T. (2002). Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci. 163, 515-523. doi: 10.1016/S0168-9452(02)00159-0
116. Vacca, R., de Pinto, M., Valenti, D., Passarella, S., Marra, E., and De Gara, L. (2004). Production of reactive oxygen species, alteration of cytosolic ascorbate peroxidase, and impairment of mitochondrial metabolism are early events in heat shock-induced programmed cell death in tobacco Bright-Yellow 2 cells. Plant Physiol. 134, 1100-1112. doi: 10.1104/pp.103.035956
117. Valliyodan, B., and Nguyen, H. T. (2006). Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr. Opin. Plant Biol. 9, 189-195. doi: 10.1016/j.pbi.2006.01.019
118. Vanderauwera, S., Suzuki, N., Miller, G., van de Cotte, B., Morsa, S., Ravanat, J.-L., et al. (2011). Extranuclear protection of chromosomal DNA from oxidative stress. Proc. Natl. Acad. Sci. U.S.A. 108, 1711-1716. doi: 10.1073/pnas.1018359108
119. Vierling, E. (1991). The roles of heat shock proteins in plants. Annu. Rev. Plant Biol.42, 579-620. doi: 10.1146/annurev.pp.42.060191.003051
120. 2 is required for effective expression of heat shock genes in Arabidopsis.Plant Mol. Biol. 61, 733-746. doi: 10.1007/s11103-006-0045-4
121. Vranová, E., Inzé, D., and Van Breusegem, F. (2002). Signal transduction during oxidative stress. J. Exp. Bot. 53, 1227-1236. doi: 10.1093/jexbot/53.372.1227
122. Wahid, A., Gelani, S., Ashraf, M., and Foolad, M. (2007). Heat tolerance in plants: an overview. Environ. Exp. Bot. 61, 199-223. doi: 10.1016/j.envexpbot.2007.05.011
123. Wang, L., Guo, Y., Jia, L., Chu, H., Zhou, S., Chen, K., et al. (2014a). Hydrogen peroxide acts upstream of nitric oxide in the heat shock pathway in Arabidopsisseedlings. Plant Physiol. 164, 2184-2196. doi: 10.1104/pp.113.229369
124. Wang, X., Jia, N., Zhao, C., Fang, Y., Lv, T., Zhou, W., et al. (2014b). Knockout of AtDjB1, a J-domain protein from Arabidopsis thaliana, alters plant responses to osmotic stress and abscisic acid. Physiol. Plant. 152, 286-300. doi: 10.1111/ppl.12169
125. Wang, Y., Zhang, J., Li, J.-L., and Ma, X.-R. (2014c). Exogenous hydrogen peroxide enhanced the thermotolerance of Festuca arundinacea and Lolium perenne by increasing the antioxidative capacity. Acta Physiol. Plant. 36, 2915-2924. doi: 10.1007/s11738-014-1661-2
126. Wang, W., Vinocur, B., and Altman, A. (2003). Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta218, 1-14. doi: 10.1007/s00425-003-1105-5
127. Wang, W., Vinocur, B., Shoseyov, O., and Altman, A. (2004). Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 9, 244-252. doi: 10.1016/j.tplants.2004.03.006
128. Waters, E. R., Lee, G. J., and Vierling, E. (1996). Evolution, structure and function of the small heat shock proteins in plants. J. Exp. Bot. 47, 325-338. doi: 10.1093/jxb/47.3.325
129. Wu, Q., Lin, J., Liu, J.-Z., Wang, X., Lim, W., Oh, M., et al. (2012). Ectopic expression of Arabidopsis glutaredoxin AtGRXS17 enhances thermotolerance in tomato. Plant Biotechnol. J. 10, 945-955. doi: 10.1111/j.1467-7652.2012.00723.x
130. Zhou, W., Zhou, T., Li, M.-X., Zhao, C.-L., Jia, N., Wang, X.-X., et al. (2012). TheArabidopsis J-protein AtDjB1 facilitates thermotolerance by protecting cells against heat-induced oxidative damage. New Phytol. 194, 364-378. doi: 10.1111/j.1469-8137.2012.04070.x
131. Zou, J., Guo, Y., Guettouche, T., Smith, D. F., and Voellmy, R. (1998). Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 94, 471-480. doi: 10.1016/S0092-8674(00)81588-3