Skip to content
naulon
Get started

No retraction, correction or concern found when last checked on Oct 22, 2026.

Multi-Level Interactions Between Heat Shock Factors, Heat Shock Proteins, and the Redox System Regulate Acclimation to Heat

Nicky Driedonks, Jiemeng Xu, Janny L. Peters and 2 more

Frontiers in Plant Science · 2015 · Review

doi:10.3389/fpls.2015.00999

Abstract

High temperature has become a global concern because it seriously affects the growth and reproduction of plants. Exposure of plant cells to high temperatures result in cellular damage and can even lead to cell death. Part of the damage can be ascribed to the action of reactive oxygen species (ROS), which accumulate during abiotic stresses such as heat stress. ROS are toxic and can modify other biomacromolecules including membrane lipids, DNA, and proteins. In order to protect the cells, ROS scavenging is essential. In contrast with their inherent harms, ROS also function as signaling molecules, inducing stress tolerance mechanisms. This review examines the evidence for crosstalk between the classical heat stress response, which consists of heat shock factors (HSFs) and heat shock proteins (HSPs), with the ROS network at multiple levels in the heat response process. Heat stimulates HSF activity directly, but also indirectly via ROS. HSFs in turn stimulate the expression of HSP chaperones and also affect ROS scavenger gene expression. In the short term, HSFs repress expression of superoxide dismutase scavenger genes via induction of miRNA398, while they also activate scavenger gene expression and stabilize scavenger protein activity via HSP induction. We propose that these contrasting effects allow for the boosting of the heat stress response at the very onset of the stress, while preventing subsequent oxidative damage. The described model on HSFs, HSPs, ROS, and ROS scavenger interactions seems applicable to responses to stresses other than heat and may explain the phenomenon of crossacclimation.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 22, 2026. Paragraph numbers are ours, so an answer can point at one.

The Heat Response

Plants are continuously exposed to biotic and abiotic stress factors, such as herbivory, pathogen attack, drought, salinity and extreme temperatures. These challenges pose a serious threat to their growth and reproduction and as such affect agricultural yields. With considerable advances in pest and disease management, abiotic factors are now thought to be the primary cause for crop losses worldwide. In case plants cannot prevent an abiotic stress factor from affecting organismal homeostasis (i.e., escape or avoid internal stress), they may adapt their metabolism to acquire a certain level of tolerance.

Heat stress can be defined as a rise in temperature beyond a threshold level for a period of time, sufficient to cause irreversible damage to plant growth and development. Sudden rises in temperature to high levels may lead to cell death within a few minutes as a consequence of extensive protein denaturation and aggregation and loss of membrane integrity. Furthermore, prolonged exposure to moderately high temperatures can lead to reduced cellular function and overall plant fitness. An important process in this respect is the accumulation of reactive oxygen species (ROS), formed as a by-product in various aerobic metabolic pathways in different cellular compartments such as chloroplasts, mitochondria and peroxisomes and probably also in the apoplast through the activation of NADPH oxidases. Under steady state conditions, ROS molecules are formed as quickly as they are scavenged by anti-oxidative defense mechanisms, but this equilibrium is perturbed by abiotic stress factors such as heat. There is ample evidence that, when plants are exposed to heat, ROS production rapidly becomes excessive. This causes cellular damage to membranes, proteins, lipids, organelles, and DNA. In order to prevent cell damage and regain redox homeostasis, one of the responses to heat is the hyper-activation of the ROS scavenging machinery. The expression and protein level of genes responsible for ROS scavenging are induced under heat stress in many different plant species and has been associated to basal heat tolerance. Furthermore, the induction of scavenging genes was significantly stronger in heat tolerant genotypes than that of sensitive ones, and improvement of plant heat stress tolerance has been achieved by increasing antioxidant enzymes activities. Taken together, this shows the importance of ROS scavenging in the heat-stress response.

In contrast to their harmful character, however, ROS are also considered as important signal molecules. Cells are capable of rapid and dynamic production and control of several forms of ROS, enabling a tight local control in the cell as well as more holistic control of the entire plant. Therefore, they are thought to be involved in the transduction of intracellular and intercellular signals controlling gene expression and activity of anti-stress systems. Indeed, NADPH oxidase activity is rapidly induced upon heat and the mutation of RBOHB makes Arabidopsis seedlings more sensitive to heat.

One of the best studied anti-stress mechanisms is the production of heat shock proteins (HSPs) upon exposure to high temperatures. By acting as molecular chaperones, HSPs prevent deleterious protein conformations and eliminate non-native aggregations, which are formed during stress. The expression of HSPs and other heat-responsive genes is regulated by heat shock factors (HSFs; ) through their association to a palindromic binding motif (5′-nAGAAnnTTCTn-3′) in the promoter region of the heat-responsive genes: the heat shock element (HSE;; ). Activation of HSFs upon stress occurs via a multistep process involving homotrimer formation and acquisition of transcriptional competence for target gene induction.

Clearly, both the activation and production of HSFs/HSPs and the increase in ROS/scavenging activity belong to the major responses of plants to heat stress and play important roles in acclimation. A number of recent genetic and biochemical studies, however, indicate that there are complex interactions between these responses. This review describes the evidence for crosstalk between HSFs, HSPs, ROS, and ROS scavenging enzymes at various points in the heat stress response pathway and presents a model with a timing component.

Activation of HSFs by ROS

In non-stressed situations, the HSFs are located in the cytoplasm for most eukaryotes, in an inactive monomeric form due to association with HSP70, HSP90, and potentially other proteins. According to the chaperone titration model, heat results in a higher load of denatured proteins, which pulls HSPs away from HSF complexes through competitions to act as molecular chaperones. This then leads to the release of HSFs, which form trimers and relocate to the nucleus to activate expression of HSP and other heat-responsive genes.

A number of studies, however, report that expression of heat-responsive genes is also increased upon application of the ROS H2O2. For example, AtHSP17.6 and AtHSP18.6 achieved similar expression levels through heat treatment as they do through H2O2 application at room temperature. Several hypotheses have been formulated that suggest that heat can indirectly activate HSFs via the action of ROS.

Firstly, damaging amounts of heat-induced ROS also induce protein denaturation. In this way ROS enhances dissociation of the HSP–HSF complex, as described by the titration model. Secondly, and similar to what was found for mammalian and Drosophila HSFs, it has been proposed that certain plant HSFs act as H2O2 sensors. Among all the ROS molecules, H2O2 plays a key role in signaling due to its moderate reactivity and thus relatively long lifetime. In addition, H2O2 can bypass membranes easily, making it a good candidate to function as a signaling molecule. suggested that H2O2 might directly modify HSFs and induce HSF trimerization. Indeed, both heat and oxidative stresses result in the formation of high molecular weight HSE-binding complexes and the formation of these complexes has been shown to be a signature of early HSFA1a/A1b-dependent gene expression in heat-stressed leaves of Arabidopsis. In vitro and in vivo studies confirmed activation of AtHSFA1a via trimerization in response to heat and H2O2 stress but also via pH alterations. HSFA1a, purified from E. coli, sensed the different stresses directly in a redox dependent fashion. In vitro stress treatments caused monomer-to-trimer transitions of HSFA1a, while the presence of the reducing agent dithiothreitol reversed this action. Although the study suggested a redox dependent fashion for HSF trimerization for all three stresses, the exact mechanism of action is still unclear. There is empirical evidence that the transcription factors may be sensitive to H2O2 via “single-Cys” or “two-Cys” redox sensory mechanisms. These cysteine residues are typically responsive to oxidative stress. HSFA1a contains one Cys residue located at the N-terminal portion of the trimerization domain. N-terminal deletions of HSFA1a negatively affected the sensing of H2O2 and pH changes, which suggests that trimerizations were induced by HSF conformational changes. In addition, recently showed that an HSFA8 Cys residue is responsible for translocation to the nucleus upon oxidative stress: H2O2 treated protoplasts showed cytosol-to-nucleus translocations of the wild-type HSFA8, but not of the HSFA8C24S mutant variant. Interestingly, however, the N-terminal deletion of HSFA1a did not inhibit heat sensing. This shows that activation of this particular transcription factor is stress-specifically regulated despite a common dependency on oxidative activity. Notably, all stress treatments induced of HSFA1a binding to the HSP18.2 and HSP70 promoter, as detected by both formaldehyde cross-linking and chromatin immunoprecipitation, which paralleled the mRNA expression of these HSFA1a target genes.

In addition to the above two processes, cellular communication between ROS and HSFs may involve mitogen-activated protein kinases (MAPK). HSF phosphorylation has been observed in yeasts and mammals and might thus occur in plants as well. Indeed, Arabidopsis HSFA2 was found to be phosphorylated by MPK6 on T249 after heat treatment, and this was associated with subsequent intracellular localization changes. Furthermore, MPK3- and MPK6-dependent phosphorylation of AtHSFA4A Ser309 and physical interaction between the proteins was reported recently. Activated HSFA4A in turn controlled the transcription of HSP17.6A. In tomato, heat-induced MAPKs were shown to transduce heat stress signals via HSFA3. In Arabidopsis, the same MAPKs that phosphorylate HSFs, namely MAPK3 and MAPK6, have been shown to be activated by H2O2. However, despite the presence of putative phosphorylation sites in tomato HSFA1, no heat-induced phosphorylation of this HSF was observed. Also, the phosphorylation site in AtHSFA4 was not conserved in HSFA4A proteins of citrus, grapevine and poplar. Taken together, this implies that both HSF oxidation and ROS-dependent phosphorylation can play a role in HSF activation, but that the latter is not a general signaling mechanism.

HSF–ROS Scavenging Gene Interactions

In addition to activation of HSFs by ROS signaling, evidence for interaction between HSFs and ROS scavenging genes has also been obtained. The expression of APX1 was found to be regulated by HSFA2: overexpression of HSFA2 resulted in increased expression of APX1, while AthsfA2 knock out mutants showed a reduced expression of APX1. In agreement with this, AtHSFA2 overexpression lines showed increased heat and oxidative stress tolerance. Expression of a dominant-negative construct for AtHSFA4a prevented the accumulation of APX1 transcripts. Interestingly, the AtHSFA4a dominant-negative construct also prevented accumulation of the H2O2-responsive zinc-finger protein ZAT12, which is required for APX1 expression during oxidative stress. The ZAT12 promoter contains HSE binding sites and therefore, HSFA4a might directly interact with the ZAT12 promoter. However, HSEs are also present in the promoter region of the APX1 gene itself, suggesting that direct activation via HSFs is also possible. Using Pennisetum glaucum APX1 and a PgHSFA, a specific binding interaction between the APX1 HSE and HSF was confirmed, via in vitro gel shift assays as well as their expression patterns over time.

Although APX1 has been shown to be a central component of the Arabidopsis ROS network, APX2, another isoform also localized in the cytosol, revealed a stronger induction by heat stress. AtHSFA2 has also been found to act as an APX2 activator. Transcription level comparison between wild-type and athsfa2 knock out plants revealed that transcripts of APX2 were absent in heat shock induced leaves of the knock out background, but present in the wild-type plants. Deletion analyses of the promoter region of APX2 functionally mapped the HSFA2 binding sites to HSEs near the transcription start site.

In addition, and found strongly enhanced expression of galactinol synthase (GolS1 and GolS2) ROS scavenging genes in an HSFA2 overexpressing line.

Combining these results, HSFA2 seems to play a central role in ROS scavenger expression and thus constitute an important link between heat shock and oxidative stress responses.

HSP Chaperones Support ROS Scavenging Activity

Heat shock proteins function as molecular chaperones and play an important role in stress tolerance. In tomato, overexpression of the LeCDJ1 DnaJ protein coding gene (also known as J-protein or HSP40; ) resulted in improved thermotolerance, accompanied by increased APX and superoxide dismutase (SOD) activity after heat stress and reduced accumulation of O2– and H2O2. Despite the higher APX and SOD activity, transcription of the corresponding genes was not enhanced in the transgenic plants. Therefore, the influence of DnaJ proteins on APX and SOD activity was proposed to be post-transcriptional, due to their functionality as chaperones. Other studies have found similar effects of HSPs on ROS scavenging proteins upon heat stress. In Arabidopsis, overexpression of RcHSP17.8 enhanced SOD activity whereas overexpression of ZmHSP16.9 in tobacco enhanced POD, CAT, and SOD activity. Altogether, it may be hypothesized that the HSP proteins positively affect thermotolerance by protecting ROS scavenging protein conformation and activity, resulting in a lower ROS concentration.

An alternative link between DnaJ proteins and ROS scavenging was suggested by. They showed that Arabidopsis AtDjB1 knockout plants (atj1-1) were more sensitive to heat stress than wild-type plants. After heat shock, the knockout plants showed an increased concentration of H2O2 and other oxidative products as well as a decreased concentration of the antioxidant ascorbate (ASC;; ). The viability of atj1-1 knockout seedlings after heat stress was rescued by exogenous ASC application. This suggests that lower concentrations of the antioxidant in atj1-1 knockout plants resulted in increased H2O2 concentrations leading to a decreased thermotolerance. As the underlying cause, the authors hypothesize a link with the electron transport chain (ETC). AtDjB1 directly interacts with a mitochondrial HSP70 and stimulates ATPase activity, a mechanism which is conserved among several kingdoms. AtDjB1 knockout potentially leads to the accumulation of cellular ATP, which feedback inhibits ETC. Because the last step of ASC synthesis is linked to the ETC, decreased ETC results in decreased ASC concentration and, consequently, the accumulation of H2O2.

Although it is unclear whether there is a specific interaction between HSPs and the ROS scavenging machinery or that HSPs generally maintain protein functions, these results indicate that upon heat stress, accumulation of ROS is reduced via HSP supported ROS scavenger activity.

A Positive Feedback Loop Including HSFs, ROS Scavenging Genes, and miRNA398

In contrast to the positive effects of ROS reducing mechanisms on heat stress tolerance, an Arabidopsis study provided evidence linking enhanced ROS accumulation to higher stress tolerance. The research indicated the existence of a positive a feedback loop, whereby heat and ROS allow for further ROS accumulation, depending on the actions of microRNA398 (miRNA398). miRNA398 expression was found to be induced within 1 h and reach its peak 2 h after heat stress. The miRNA398 promoter region contains a putative HSE, and chromatin immune-precipitation assays revealed direct binding of HSFA1b and HSFA7b to the HSE promoter region under heat stress. Thus, association of these HSFs to the promoter region seems to be responsible for the induction of this miRNA upon heat stress. miRNA398 negatively regulates the expression of three target genes: CSD1, CSD2, and CCS. CSD1 and CSD2 genes are isoforms of copper/zinc-SOD scavenging genes which are located in the cytoplasm and chloroplasts, respectively and CCS is a copper chaperone encoding gene, which delivers copper to both CSD genes. Consequently, CSD1, CSD2, and CCS are down-regulated during heat stress, allowing further ROS accumulation. This pathway acts in an autocatalytic manner, as H2O2 in turn promotes expression of various HSFs, including HSFA7b. Accumulation of ROS seems to be an unfavorable response for the plant to survive heat stress. However, comparison of wild-type and csd1, csd2, and ccs mutants plants revealed higher heat tolerance in mutant plants while transgenic plants over-expressing miR398-resistant versions of CSD1, CSD2, or CCS were hypersensitive to heat stress.

These unexpected outcomes may be explained by the increases in oxidative power for helping activate the primary set of HSFs at the start of the heat response. In contrast to; found that lack of miRNA398 enhances tolerance to some other stress factors, high light and chemically induced ROS, via enhanced expression of CSD1 and CSD2. Therefore, it seems that the benefit of reduced SOD activity is heat-specific, potentially due to the importance of high HSF activity in the first hours of the response to this stress.

A Multi-Level Interaction Model

A number of recent studies have provided evidence for connections between HSFs, HSPs, ROS, and ROS scavengers upon heat stress. Here, we propose a comprehensive model on the relations between the various components to explain a large proportion of the observations (Figure 1). Through contrasting effects on ROS scavenging activity, heat shock induces a short-term positive (roughly, within the first few hours of heat stress) and a long-term negative feedback loop (after the first few hours of heat stress) on the HSF signaling pathway. The proposed complexity of the heat-stress response network is mirrored in some of the counter-intuitive observations, such as enhanced heat tolerance in certain scavenger mutants. However, analogous to the proposed miRNA398 mechanism, constitutively, slightly elevated ROS levels in such mutants may result in a primed state and, as a consequence, a stronger and/or faster response to a heat treatment. indeed showed that knockout mutations in CSD1 and CSD2 were accompanied by constitutively higher levels of HSF and HSP transcripts. In accordance, the importance of ROS at early heat response was shown by: a rapid oxidative burst of ROS during the first 15 min of the heat shock stimulates HSF DNA-binding and is essential for the induction of heat responsive gene expression, e.g., of HSPs and APX2. The typical “late” high mobility HSE-binding complexes, formed after 2 h, were shown to be ROS independent, which is in accordance with the production of anti-oxidants and ROS scavengers reducing the ROS overload after the early onset of the HSR. Nevertheless, if plants are continuously exposed to heat stress, the activity of some antioxidants and scavengers, e.g., APX and CAT, decreased after 3 days of heat stress in tomato, alfalfa and tobacco cell cultures. The changes of these components of the antioxidant system were ascribed to the impaired health and growth of plants under long term heat stress and are different from short term heat stress.

Importantly, the model described here refers specifically to the complexity of events after a short term heat shock; its applicability to other types of heat stress, e.g., mild levels of heat stress, which only affect plant physiology in the long term, is not evident and more research will be necessary in order to clarify how the HSF/HSP and ROS systems behave under those circumstances. Also, it should be noted that the proposed model is not stand-alone and will interact with other factors, such as phytohormones. Abscisic acid (ABA), salicylic acid (SA) and ethylene have all been implicated in the heat response and can induce the production of ROS. While a number of phytohormone-related mutants show impaired tolerance to heat, application of these hormones may enhance thermotolerance via an effect of ROS. SA application, for example, enhanced SOD activity and HSP expression during heat stress. Dedicated analysis of the role of hormones during the first hours of heat treatment should clarify their putative positions in the response model.

The model may well have broader applicability then to the heat response only. Not only are ROS accumulation, signaling and scavenging thought to occur and play a role in myriad other stress responses, but so is HSP activity. HSPs are also induced upon water stress, salinity and osmotic stress, cold, anoxia, UV-B light, and oxidative stress. Furthermore, overexpression of various HSFs enhanced tolerance to abiotic stresses other than heat, including salt, drought, osmotic, and anoxic stress. Also, tomato plants overexpressing the DnaJ/HSP40 LeCDJ1 showed both higher heat and chilling tolerance and overexpression of BRZ-INSENSITIVE-LONG HYPOCOTYLS 2 (BIL2), a mitochondrial-localized DnaJ/HSP40 family member, enhanced resistance against salinity and high light stress. The role of both the oxidative stress and HSF/HSP systems in multiple stress responses might explain the phenomenon of cross-acclimation, where exposure to a certain stress factor improves tolerance to a subsequent different stress factor.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References 131

  1. 1.

    Ahn S.-G. 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.

    Not in our library10.1101/gad.1044503

  2. 2.

    Almeselmani M. Deshmukh P. Sairam R. Kushwaha S. Singh T. (2006 ). Protective role of antioxidant enzymes under high temperature stress. Plant Sci. 171, 382–388.

    Not in our library10.1016/j.plantsci.2006.04.009

  3. 3.

    Apel K. Hirt H. (2004 ). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373–399.

    Not in our library10.1146/annurev.arplant.55.031903.141701

  4. 4.

    Badiani M. Schenone G. Paolacci A. R. 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.

    Not in our library

  5. 5.

    Baker C. J. Orlandi E. W. (1995 ). Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 33, 299–321.

    Not in our library10.1146/annurev.py.33.090195.001503

  6. 6.

    Banti V. Loreti E. Novi G. Santaniello A. Alpi A. Perata P. (2008 ). Heat acclimation and cross-tolerance against anoxia in Arabidopsis. Plant Cell Environ. 31, 1029–1037.

    Not in our library10.1111/j.1365-3040.2008.01816.x

  7. 7.

    Banti V. Mafessoni F. Loreti E. Alpi A. Perata P. (2010 ). The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiol. 152, 1471–1483.

    Not in our library10.1104/pp.109.149815

  8. 8.

    Bartoli C. G. Casalongué C. A. Simontacchi M. Marquez-Garcia B. 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.

    Not in our library10.1016/j.envexpbot.2012.05.003

  9. 9.

    Bartoli C. G. Pastori G. M. 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.

    Not in our library10.1104/pp.123.1.335

  10. 10.

    Bechtold U. Albihlal W. S. Lawson T. Fryer M. J. Sparrow P. A. Richard F. (2013 ). Arabidopsis HEAT SHOCK TRANSCRIPTION FACTORA1b overexpression enhances water productivity, resistance to drought, and infection. J. Exp. Bot. 64, 3467–3481.

    Not in our library10.1093/jxb/ert185

  11. 11.

    Bekh-Ochir D. Shimada S. Yamagami A. Kanda S. Ogawa K. Nakazawa M. (2013 ). A novel mitochondrial DnaJ/Hsp40 family protein BIL2 promotes plant growth and resistance against environmental stress in brassinosteroid signaling. Planta 237, 1509–1525.

    Not in our library10.1007/s00425-013-1859-3

  12. 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.

    Not in our library10.1007/s10725-012-9728-9

  13. 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.

    Not in our library10.1007/s12298-012-0159-x

  14. 14.
    Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance · 2013
    No notice
  15. 15.

    Boston R. S. Viitanen P. V. Vierling E. (1996 ). Molecular chaperones and protein folding in plants. Plant Mol. Biol. 32, 191–222.

    Not in our library10.1007/bf00039383

  16. 16.

    Bowler C. Montagu M. V. Inze D. (1992 ). Superoxide dismutase and stress tolerance. Annu. Rev. Plant Biol. 43, 83–116.

    Not in our library10.1146/annurev.pp.43.060192.000503

  17. 17.

    Byth-Illing H.-A. Bornman L. (2013 ). Heat shock, with recovery, promotes protection of Nicotiana tabacum during subsequent exposure to Ralstonia solanacearum. Cell Stress Chaperones 19, 193–203.

    Not in our library10.1007/s12192-013-0445-8

  18. 18.

    Chaitanya K. Sundar D. Masilamani S. Reddy A. R. (2002 ). Variation in heat stress-induced antioxidant enzyme activities among three mulberry cultivars. Plant Growth Regul. 36, 175–180.

    Not in our library10.1023/a:1015092628374

  19. 19.

    Chao Y.-Y. Hsu Y. 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.

    Not in our library10.1007/s11104-008-9815-x

  20. 20.
    A seed preferential heat shock transcription factor from wheat provides abiotic stress tolerance and yield enhancement in transgenic Arabidopsis under heat stress environment. · 2013
    Not checked
  21. 21.

    Chen S. Liu A. Zhang S. Li C. Chang R. Liu D. (2013 ). Overexpression of mitochondrial uncoupling protein conferred resistance to heat stress and Botrytis cinerea infection in tomato. Plant Physiol. Biochem. 73, 245–253.

    Not in our library10.1016/j.plaphy.2013.10.002

  22. 22.

    Chou T.-S. Chao Y.-Y. 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.

    Not in our library10.1016/j.jplph.2011.11.012

  23. 23.

    Chu B. Soncin F. Price B. D. Stevenson M. A. 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.

    Not in our library10.1074/jbc.271.48.30847

  24. 24.

    Clarke S. M. Mur L. A. Wood J. E. 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.

    Not in our library10.1111/j.1365-313x.2004.02054.x

  25. 25.

    Cohu C. M. Abdel-Ghany S. E. Reynolds K. A. G. Onofrio A. M. Bodecker J. R. Kimbrel J. A. (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.

    Not in our library10.1093/mp/ssp084

  26. 26.

    Das K. Roychoudhury A. (2014 ). Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front. Environ. Sci. 2:53

    Not in our library10.3389/fenvs.2014.00053

  27. 27.

    Dat J. F. Foyer C. H. Scott I. M. (1998 ). Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. Plant Physiol. 118, 1455–1461.

    Not in our library10.1104/pp.118.4.1455

  28. 28.

    Davletova S. Rizhsky L. Liang H. Shengqiang Z. Oliver D. J. Coutu J. (2005 ). Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17, 268–281.

    Not in our library10.1105/tpc.104.026971

  29. 29.

    del Rio L. A. Sandalio L. M. Corpas F. J. Palma J. M. 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.

    Not in our library10.1104/pp.106.078204

  30. 30.

    de Pinto M. C. Locato V. Paradiso A. De Gara L. (2015 ). Role of redox homeostasis in thermo-tolerance under a climate change scenario. Ann. Bot. 116, 487–496.

    Not in our library10.1093/aob/mcv071

  31. 31.

    Desikan R. Hancock J. Neill S. (2004 ). “Oxidative stress signalling,” in Plant Responses to Abiotic Stress, eds Hirt H. Shinozaki K. (Berlin: Springer), 121–149.

    Not in our library

  32. 32.

    Desikan R. Soheila A.-H. Hancock J. T. Neill S. J. (2001 ). Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 127, 159–172.

    Not in our library10.1104/pp.127.1.159

  33. 33.

    Dong X. Yi H. Lee J. Nou I.-S. Han C.-T. 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.

    Not in our library10.1371/journal.pone.0130451

  34. 34.

    Evrard A. Kumar M. Lecourieux D. Lucks J. von Koskull-Döring P. Hirt H. (2013 ). Regulation of the heat stress response in Arabidopsis by MPK6-targeted phosphorylation of the heat stress factor HsfA2. PeerJ 1, e59.

    Not in our library10.7717/peerj.59

  35. 35.

    Foyer C. Noctor G. (2005 ). Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17, 1866–1875.

    Not in our library10.1105/tpc.105.033589

  36. 36.

    Foyer C. H. Noctor G. (2009 ). Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid. Redox Signal. 11, 861–905.

    Not in our library10.1089/ars.2008.2177

  37. 37.

    Frank G. Pressman E. Ophir R. Althan L. Shaked R. Freedman M. (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.

    Not in our library10.1093/jxb/erp234

  38. 38.

    Galvez-Valdivieso G. Mullineaux P. (2010 ). The role of reactive oxygen species in signalling from chloroplasts to the nucleus. Physiol. Plant. 138, 430–439.

    Not in our library10.1111/j.1399-3054.2009.01331.x

  39. 39.

    Gechev T. S. Hille J. (2005 ). Hydrogen peroxide as a signal controlling plant programmed cell death. J. Cell Biol. 168, 17–20.

    Not in our library10.1083/jcb.200409170

  40. 40.

    Giardi M. T. Masojidek J. Godde D. (1997 ). Effects of abiotic stresses on the turnover of the D1 reaction centre II protein. Physiol. Plant. 101, 635–642.

    Not in our library10.1111/j.1399-3054.1997.tb01048.x

  41. 41.

    Giesguth M. Sahm A. Simon S. 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.

    Not in our library10.1016/j.febslet.2015.01.039

  42. 42.

    Guan Q. Lu X. Zeng H. Zhang Y. Zhu J. (2013 ). Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. Plant J. 74, 840–851.

    Not in our library10.1111/tpj.12169

  43. 43.

    Gupta A. S. Webb R. P. Holaday A. S. 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.

    Not in our library10.1104/pp.103.4.1067

  44. 44.

    Hasanuzzaman M. Hossain M. A. da Silva J. A. T. 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 Venkateswarlu B. Shanker A. K. Shanker C. Maheswari M. (New York: Springer), 261–315.

    Not in our library

  45. 45.
    Physiological, Biochemical, and Molecular Mechanisms of Heat Stress Tolerance in Plants · 2013
    No notice
  46. 46.

    He Y. Liu Y. Cao W. Huai M. Xu B. Huang B. (2005 ). Effects of salicylic acid on heat tolerance associated with antioxidant metabolism in Kentucky bluegrass. Crop Sci. 45, 988–995.

    Not in our library10.2135/cropsci2003.0678

  47. 47.
    Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging · 2015
    No notice
  48. 48.

    Hossain M. A. Mostofa M. G. 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.

    Not in our library10.5376/mpb.2013.04.0007

  49. 49.

    Hübel A. Schöffl F. (1994 ). Arabidopsis heat shock factor: isolation and characterization of the gene and the recombinant protein. Plant Mol. Biol. 26, 353–362.

    Not in our library10.1007/bf00039545

  50. 50.

    Jammes F. Song C. Shin D. Munemasa S. Takeda K. Gu D. (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.

    Not in our library10.1073/pnas.0907205106

  51. 51.

    Jiang C. Xu J. Zhang H. Zhang X. Shi J. Li M. (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.

    Not in our library10.1111/j.1365-3040.2009.01987.x

  52. 52.

    Jiang M. 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.

    Not in our library10.1007/s00425-002-0829-y

  53. 53.

    Kang N. J. Kang Y. I. Kang K. H. Jeong B. R. (2009 ). Induction of thermotolerance and activation of antioxidant enzymes in H2O2 pre-applied leaves of cucumber and tomato seedlings. J. Jpn. Soc. Hort. Sci. 78, 320–329.

    Not in our library10.2503/jjshs1.78.320

  54. 54.

    Kim D. Kim S. Li G. (1999 ). Proteasome inhibitors MG132 and lactacystin hyperphosphorylate HSF1 and induce hsp70 and hsp27 expression. Biochem. Biophys. Res. Commun. 254, 264–268.

    Not in our library10.1006/bbrc.1998.9840

  55. 55.

    Kliebenstein D. J. Monde R.-A. Last R. L. (1998 ). Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol. 118, 637–650.

    Not in our library10.1104/pp.118.2.637

  56. 56.

    Knauf U. Newton E. M. Kyriakis J. Kingston R. E. (1996 ). Repression of human heat shock factor 1 activity at control temperature by phosphorylation. Genes Dev. 10, 2782–2793.

    Not in our library10.1101/gad.10.21.2782

  57. 57.

    Kong F. Deng Y. Wang G. Wang J. Liang X. Meng Q. (2014a ). LeCDJ1, a chloroplast DnaJ protein, facilitates heat tolerance in transgenic tomatoes. J. Integr. Plant Biol. 56, 63–74.

    Not in our library10.1111/jipb.12119

  58. 58.
    A chloroplast-targeted DnaJ protein contributes to maintenance of photosystem II under chilling stress · 2013
    No notice
  59. 59.

    Kotak S. Larkindale J. Lee U. von Koskull-Döring P. Vierling E. Scharf K.-D. (2007 ). Complexity of the heat stress response in plants. Curr. Opin. Plant Biol. 10, 310–316.

    Not in our library10.1016/j.pbi.2007.04.011

  60. 60.
    Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants · 2000
    Not checked
  61. 61.

    Krasensky J. Jonak C. (2012 ). Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J. Exp. Bot. 63, 1593–1608.

    Not in our library10.1093/jxb/err460

  62. 62.

    Kreslavski V. D. Los D. A. Allakhverdiev S. I. Vl V. K. (2012 ). Signaling role of reactive oxygen species in plants under stress. Russ. J. Plant Physiol. 59, 163–178.

    Not in our library10.1134/s1021443712020057

  63. 63.

    Kwak J. M. Nguyen V. Schroeder J. I. (2006 ). The role of reactive oxygen species in hormonal responses. Plant Physiol. 141, 323–329.

    Not in our library10.1104/pp.106.079004

  64. 64.

    Larkindale J. Hall J. D. Knight M. R. Vierling E. (2005 ). Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol. 138, 882–897.

    Not in our library10.1104/pp.105.062257

  65. 65.

    Larkindale J. 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.

    Not in our library10.1104/pp.010320

  66. 66.

    Li C. Chen Q. Gao X. Qi B. Chen N. Xu S. (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.

    Not in our library10.1360/062005-119

  67. 67.

    Li W. Wei Z. Qiao Z. Wu Z. Cheng L. Wang Y. (2013 ). Proteomics analysis of alfalfa response to heat stress. PLoS ONE 8:e82725.

    Not in our library10.1371/journal.pone.0082725

  68. 68.

    Link V. Sinha A. Vashista P. Hofmann M. Proels R. Ehness R. (2002 ). A heat-activated MAP kinase in tomato: a possible regulator of the heat stress response. FEBS Lett. 531, 179–183.

    Not in our library10.1016/s0014-5793(02)03498-1

  69. 69.

    Liu Y. Zhang C. Chen J. Guo L. Li X. Li W. (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.

    Not in our library10.1016/j.plaphy.2012.12.013

  70. 70.

    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. Mol. Genet. Genomics 271, 11–21.

    Not in our library10.1007/s00438-003-0954-8

  71. 71.

    Loreti E. Poggi A. Novi G. Alpi A. 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.

    Not in our library10.1104/pp.104.057299

  72. 72.

    Miller G. Mittler R. (2006 ). Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann. Bot. 98, 279–288.

    Not in our library10.1093/aob/mcl107

  73. 73.

    Miller G. Schlauch K. Tam R. Cortes D. Torres M. A. Shulaev V. (2009 ). The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2, ra45.

    Not in our library10.1126/scisignal.2000448

  74. 74.
    Genome-wide transcriptional profiles during temperature and oxidative stress reveal coordinated expression patterns and overlapping regulons in rice. · 2012
    Not checked
  75. 75.

    Mittler R. (2002 ). Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405–410.

    Not in our library10.1016/s1360-1385(02)02312-9

  76. 76.

    Mittler R. Vanderauwera S. Gollery M. Van Breusegem F. (2004 ). Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490–498.

    Not in our library10.1016/j.tplants.2004.08.009

  77. 77.

    Mittler R. Vanderauwera S. Suzuki N. Miller G. Tognetti V. B. Vandepoele K. (2011 ). ROS signaling: the new wave? Trends Plant Sci. 16, 300–309.

    Not in our library10.1016/j.tplants.2011.03.007

  78. 78.

    Moon H. Lee B. Choi G. Shin D. Prasad D. T. Lee O. (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.

    Not in our library10.1073/pnas.252641899

  79. 79.

    Morgan R. W. Christman M. F. Jacobson F. S. Storz G. 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.

    Not in our library10.1073/pnas.83.21.8059

  80. 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.

    Not in our library10.1101/gad.12.24.3788

  81. 81.

    Mostofa M. G. Yoshida N. Fujita M. (2014 ). Spermidine pretreatment enhances heat tolerance in rice seedlings through modulating antioxidative and glyoxalase systems. Plant Growth Regul. 73, 31–44.

    Not in our library10.1007/s10725-013-9865-9

  82. 82.

    Munns R. Tester M. (2008 ). Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651–681.

    Not in our library10.1146/annurev.arplant.59.032607.092911

  83. 83.

    Navrot N. Rouhier N. Gelhaye E. Jacquot J. (2007 ). Reactive oxygen species generation and antioxidant systems in plant mitochondria. Physiol. Plant. 129, 185–195.

    Not in our library10.1111/j.1399-3054.2006.00777.x

  84. 84.

    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. Plant J. 48, 535–547.

    Not in our library10.1111/j.1365-313x.2006.02889.x

  85. 85.

    Nishizawa A. Yabuta Y. Shigeoka S. (2008 ). Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 147, 1251–1263.

    Not in our library10.1104/pp.108.122465

  86. 86.

    O’Kane D. Gill V. Boyd P. Burdon R. (1996 ). Chilling, oxidative stress and antioxidant responses in Arabidopsis thaliana callus. Planta 198, 371–377.

    Not in our library10.1007/bf00620053

  87. 87.

    Panchuk I. I. Volkov R. A. Schöffl F. (2002 ). Heat stress-and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol. 129, 838–853.

    Not in our library10.1104/pp.001362

  88. 88.

    Pastori G. 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.

    Not in our library10.1104/pp.011021

  89. 89.

    Pelham H. R. (1982 ). A regulatory upstream promoter element in the Drosophila hsp 70 heat-shock gene. Cell 30, 517–528.

    Not in our library10.1016/0092-8674(82)90249-5

  90. 90.

    Pérez-Salamó I. Papdi C. Gábor R. Zsigmond L. Vilela B. Lumbreras V. (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.

    Not in our library10.1104/pp.114.237891

  91. 91.

    Petrov V. D. Van Breusegem F. (2012 ). Hydrogen peroxide—a central hub for information flow in plant cells. AoB Plants 2012, pls014.

    Not in our library10.1093/aobpla/pls014

  92. 92.

    Pnueli L. Liang H. Rozenberg M. 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.

    Not in our library10.1046/j.1365-313x.2003.01715.x

  93. 93.

    Pucciariello C. Banti V. Perata P. (2012 ). ROS signaling as common element in low oxygen and heat stresses. Plant Physiol. Biochem. 59, 3–10.

    Not in our library10.1016/j.plaphy.2012.02.016

  94. 94.

    Qiu X.-B. Shao Y.-M. Miao S. Wang L. (2006 ). The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cell. Mol. Life Sci. 63, 2560–2570.

    Not in our library10.1007/s00018-006-6192-6

  95. 95.

    Rainwater D. Gossett D. Millhollon E. Hanna H. Banks S. Lucas M. (1996 ). The relationship between yield and the antioxidant defense system in tomatoes grown under heat stress. Free Radic. Res. 25, 421–435.

    Not in our library10.3109/10715769609149065

  96. 96.

    Reddy R. Kumar B. Reddy P. Mishra R. Mahanty S. Kaul T. (2009 ). Molecular cloning and characterization of genes encoding Pennisetum glaucum ascorbate peroxidase and heat-shock factor: interlinking oxidative and heat-stress responses. J. Plant Physiol. 166, 1646–1659.

    Not in our library10.1016/j.jplph.2009.04.007

  97. 97.

    Rentel M. C. Lecourieux D. Ouaked F. Usher S. L. Petersen L. Okamoto H. (2004 ). OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427, 858–861.

    Not in our library10.1038/nature02353

  98. 98.

    Rizhsky L. Davletova S. Liang H. 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.

    Not in our library10.1074/jbc.m313350200

  99. 99.

    Rizhsky L. Hallak-Herr E. Van Breusegem F. Rachmilevitch S. Barr J. E. Rodermel S. (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.

    Not in our library10.1046/j.1365-313x.2002.01427.x

  100. 100.

    Rui R. Nie Y. 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.

    Not in our library

  101. 101.

    Sairam R. Srivastava G. Saxena D. (2000 ). Increased antioxidant activity under elevated temperatures: a mechanism of heat stress tolerance in wheat genotypes. Biol. Plant. 43, 245–251.

    Not in our library10.1023/a:1002756311146

  102. 102.

    Scharf K.-D. Berberich T. Ebersberger I. Nover L. (2012 ). The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim. Biophys. Acta 1819, 104–119.

    Not in our library10.1016/j.bbagrm.2011.10.002

  103. 103.

    Schöffl F. Prändl R. Reindl A. (1998 ). Regulation of the heat-shock response. Plant Physiol. 117, 1135–1141.

    Not in our library10.1104/pp.117.4.1135

  104. 104.

    Schöffl F. Prändl R. Reindl A. (1999 ). “Molecular responses to heat stress,” in Molecular Responses to Cold, Drought, Heat and Salt Stress in Higher Plants, Yamaguchi-Shinozai K. Shinozaki K. (Austin, TX: Landes Co.), 81–98.

    Not in our library

  105. 105.

    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, 759–772.

    Not in our library10.1007/s11103-005-5750-x

  106. 106.

    Sgobba A. Paradiso A. Dipierro S. De Gara L. 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.

    Not in our library10.1111/ppl.12220

  107. 107.

    Shen Z. Ding M. Sun J. Deng S. Zhao R. Wang M. (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.

    Not in our library10.1007/s11240-013-0362-7

  108. 108.

    Storozhenko S. De Pauw P. Van Montagu M. Inzé D. Kushnir S. (1998 ). The heat-shock element is a functional component of the Arabidopsis APX1 gene promoter. Plant Physiol. 118, 1005–1014.

    Not in our library10.1104/pp.118.3.1005

  109. 109.

    Sun L. Liu Y. Kong X. Zhang D. Pan J. Zhou Y. (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.

    Not in our library10.1007/s00299-012-1262-8

  110. 110.

    Sunkar R. Kapoor A. 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.

    Not in our library10.1105/tpc.106.041673

  111. 111.

    Suzuki N. Miller G. Sejima H. Harper J. 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.

    Not in our library10.1093/jxb/ers335

  112. 112.

    Suzuki N. Rivero R. M. Shulaev V. Blumwald E. Mittler R. (2014 ). Abiotic and biotic stress combinations. New Phytol. 203, 32–43.

    Not in our library10.1111/nph.12797

  113. 113.
    Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways · 2007
    No notice
  114. 114.

    Torres M. A. Dangl J. L. (2005 ). Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr. Opin. Plant Biol. 8, 397–403.

    Not in our library10.1016/j.pbi.2005.05.014

  115. 115.

    Uchida A. Jagendorf A. T. Hibino T. Takabe T. Takabe T. (2002 ). Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci. 163, 515–523.

    Not in our library10.1016/s0168-9452(02)00159-0

  116. 116.

    Vacca R. de Pinto M. Valenti D. Passarella S. Marra E. 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.

    Not in our library10.1104/pp.103.035956

  117. 117.

    Valliyodan B. Nguyen H. T. (2006 ). Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr. Opin. Plant Biol. 9, 189–195.

    Not in our library10.1016/j.pbi.2006.01.019

  118. 118.

    Vanderauwera S. Suzuki N. Miller G. van de Cotte B. Morsa S. Ravanat J.-L. (2011 ). Extranuclear protection of chromosomal DNA from oxidative stress. Proc. Natl. Acad. Sci. U.S.A. 108, 1711–1716.

    Not in our library10.1073/pnas.1018359108

  119. 119.

    Vierling E. (1991 ). The roles of heat shock proteins in plants. Annu. Rev. Plant Biol. 42, 579–620.

    Not in our library10.1146/annurev.pp.42.060191.003051

  120. 120.

    Volkov R. A. Panchuk I. I. Mullineaux P. M. Schöffl F. (2006 ). Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol. Biol. 61, 733–746.

    Not in our library10.1007/s11103-006-0045-4

  121. 121.

    Vranová E. Inzé D. Van Breusegem F. (2002 ). Signal transduction during oxidative stress. J. Exp. Bot. 53, 1227–1236.

    Not in our library10.1093/jexbot/53.372.1227

  122. 122.

    Wahid A. Gelani S. Ashraf M. Foolad M. (2007 ). Heat tolerance in plants: an overview. Environ. Exp. Bot. 61, 199–223.

    Not in our library10.1016/j.envexpbot.2007.05.011

  123. 123.

    Wang L. Guo Y. Jia L. Chu H. Zhou S. Chen K. (2014a ). Hydrogen peroxide acts upstream of nitric oxide in the heat shock pathway in Arabidopsis seedlings. Plant Physiol. 164, 2184–2196.

    Not in our library10.1104/pp.113.229369

  124. 124.

    Wang X. Jia N. Zhao C. Fang Y. Lv T. Zhou W. (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.

    Not in our library10.1111/ppl.12169

  125. 125.

    Wang Y. Zhang J. Li J.-L. 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.

    Not in our library10.1007/s11738-014-1661-2

  126. 126.

    Wang W. Vinocur B. Altman A. (2003 ). Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218, 1–14.

    Not in our library10.1007/s00425-003-1105-5

  127. 127.

    Wang W. Vinocur B. Shoseyov O. Altman A. (2004 ). Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 9, 244–252.

    Not in our library10.1016/j.tplants.2004.03.006

  128. 128.

    Waters E. R. Lee G. J. Vierling E. (1996 ). Evolution, structure and function of the small heat shock proteins in plants. J. Exp. Bot. 47, 325–338.

    Not in our library10.1093/jxb/47.3.325

  129. 129.

    Wu Q. Lin J. Liu J.-Z. Wang X. Lim W. Oh M. (2012 ). Ectopic expression of Arabidopsis glutaredoxin AtGRXS17 enhances thermotolerance in tomato. Plant Biotechnol. J. 10, 945–955.

    Not in our library10.1111/j.1467-7652.2012.00723.x

  130. 130.

    Zhou W. Zhou T. Li M.-X. Zhao C.-L. Jia N. Wang X.-X. (2012 ). The Arabidopsis J-protein AtDjB1 facilitates thermotolerance by protecting cells against heat-induced oxidative damage. New Phytol. 194, 364–378.

    Not in our library10.1111/j.1469-8137.2012.04070.x

  131. 131.

    Zou J. Guo Y. Guettouche T. Smith D. F. 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.

    Not in our library10.1016/s0092-8674(00)81588-3

Cited by papers we hold 6

Reads

Read by people on this page

None yet.

Checked or read by AI through naulon

None yet.

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.

Are you an author?

Is this your paper?

Claim it to add your note and be paid when agents cite it. Free.