Open access peer-reviewed chapter
Abstract
Different organisms respond to the altered environmental conditions by different ways. Heat shock proteins’ (HSPs) production is one among the different defense mechanisms which defend the photosystem II and thylokoid membrane in plants. There are different types of HSPs based on their size, that is, high molecular weight (60–100 kDa) and low molecular weight heat shock proteins (15–30 kDa). Small HSPs are further classified based on their localization and role in different sub-cellular organelles. Cp-sHSPs are the chloroplast-specific small HSPs that protect the photosystem II and thylokoid membrane. A model to control the Cp-sHSPs in Chenopodium album has been put forward in this chapter. According to this model, Cp-sHSPs of Chenopodium album are created in cytoplasm and are moved toward chloroplast. The transit peptide is removed on reaching to the target sub-cellular organelle, that is, chloroplast and the premature Cp-sHSPs are converted into mature ones which have multiple roles under different abiotic stress conditions.
Keywords
- plants HSPs
- abiotic stresses
- HSPs model
- Chenopodium album
1. Introduction
Organisms respond to the changed growth conditions through heat shock proteins’ (HSPs) production [1] and that is the way of survival for the cell which responds differentially [2]. Different environmental conditions including abiotic and biotic stress conditions influence the plants’ development and production [3]. Different stress conditions like heat, salt, and low water conditions may majorly influence the plants’ physiology and production [4, 5, 6, 7, 8], but plants response to the changed environmental conditions may vary depending upon duration, intensity, and combination of different environmental growth conditions [9]. Different processes in the plants including biochemistry, development, and physiology may affected by stress conditions and so the expression of different genes may be turned off or on in response to the changed environmental conditions, which may lead to the creation of different proteins and metabolites that protect the cells against such conditions [10].
2. Stress types
Stresses due to living and non-living things can affect the plants’ development and production. Different organisms like viruses, bacteria, and fungi may cause stress conditions for the plants [8] which may activate different defense pathways of the plants [9]. There are reports that abiotic stress conditions are responsible to make mostly changes in plant biochemistry and physiology [10]. So plant growth may negatively be affected by abiotic stress conditions also known as non-living factors [6], and any kind of change in environmental conditions may lead the plants toward adaptation under altered growth conditions [11]. Below are the details of different abiotic stress conditions which may affect the plants.
2.1 Types of abiotic stresses and their effects on plants
2.1.1 High temperature or heat stress
Heat stress is the main factor among abiotic stress conditions that affects the plants yield [12] and so different factors in the plants like metabolite concentration, osmolytes, membrane fluidity, proteins structure, and nucleic acids are seriously changed by temperature [13]. Additionally, high-temperature stress affects the chloroplast photochemical activity [14]. Photosystem II is considered as the most sensitive part of thylokoid membrane [15] and heat stress conditions may influence the photosystem II (PS II) reaction center and the light harvesting complexes [16].
Plants adapt their system to the changed growth conditions through complex mechanisms [17]. Thus, different processes at cellular level are reprogrammed under high- and low-temperature growth conditions and many changes in transcription may happen in different parts of the plants, that is, seedlings, roots, pollens, and leaves [18, 19]. Effect on plants may vary with intensity and duration of temperature [20]. One of the plants responses is the reactive oxygen species (ROS) production which is increased by low- and high-temperature stress conditions, while oxidative damage and cell death have also been reported as a result of high-temperature stress conditions [21]. Photosynthesis inhibition has also been reported by researchers under high-temperature conditions [17], additional to the damage of the oxygen evolving complex (OEC) of photosystem II caused by heat stress [22].
Plants adapt to the high-temperature conditions through heat shock proteins (HSPs) production, which are found to be produced in all organisms from prokaryotes to eukaryotes and have role in cell protection under harsh conditions [2]. Establishment of defense mechanism under high-temperature growth conditions is necessary for cells survival which is not specifically occurred only under high temperature but it is also significant under different stress conditions [23].
2.1.2 Low temperature or cold stress
Low temperature represses the plants development without stopping the cell functions and may cause problems to different processes at cellular level [3]. Temperature is the main factor to control the growth changes from vegetative till reproductive level [24]. Low temperature may increase the ROS production additional to the reduction of cellular respiration [25] as well as damages the cell membrane [26].
Low-temperature stress conditions may reduce photosystem I and this effect has been reported to be increased under low light conditions [27]. The same effects have also been observed by different researchers in different plants like winter rye and barley [28, 29].
Expression of different genes and proteins has been reported to be up- or down-regulated by low-temperature stress conditions [30]. Researchers have reported the up-regulation of the defensive genes under cold stress [24]. For example, almost 300 genes have been reported to get up-regulated under cold stress conditions, while 88 genes (27%) were down-regulated in
2.1.3 Metal stress
Development of the plants is badly affected by heavy metals [32] and roots are usually damaged by heavy metals which lead to build up different defensive mechanisms for normal growth [33]. Membrane potential and permeability are changed by interactions of heavy metals with membrane components [32]. Plants take up the heavy metals as essential nutrients and are passed to the upper parts of the plants following the pathways of the essential elements transport [34].
Plants respond differentially to the heavy metal toxicity [35] and that is the reason that some plants do not show any phytotoxicity symptoms on heavy metals accumulation [36]. But heavy metals restrict the plants growth and cause cell death due to interruption in different physiological and biochemical pathways [37]. Different essential ions are replaced by heavy metals, for example, Ni replaces Mg ion that results in the changed activity of ribulose-1,5-biphosphate carboxylated oxygenase [38]. Chlorophyll activity is altered [39], while heavy metals break the disulfide bridges of the proteins, which leads to the destabilization of proteins [37]. Besides the formerly mentioned adverse roles in plants, heavy metals interact with the hydroxyl and carboxyl groups of proteins and thus interrupt in the proteins functions [40].
Plants adopt different defense mechanisms while get exposure to heavy metals. These mechanisms include the synthesis of cystein-rich polypeptides phytochelatins and metallothioneins [32]. Researchers have also reported the up-regulation of HSP70 gene and chaperonin 60 family members under different heavy metals, that is, Cd and Ni [41, 42]. Additional to the former HSP families, chloroplast small heat shock proteins (Cp-sHSPs) are also reported to be up-regulated by heavy metals [43].
2.1.4 Salt stress
Based on the response to salt stress, plants may be two types either glycophytes or halophytes. The former kind of plants has no tolerance to the saline environment, while the latter group plants covering are natively grown in saline environment [44]. Halophytes cover almost 1% of the world flora [45]. Salt stress adversely affects the plants growth and productivity by different ways; for example, sodium chloride salt can cause the ionic toxicity and osmotic stress to the plants [46]. Researchers have also reported the adverse effect of salt on growth and photosynthesis of the plants [47] by lowering the intra-cellular CO2 availability [48] or by changed photosynthetic metabolism [49].
2.1.5 Drought stress
Crops yield and quality are adversely affected by drought conditions. Drought conditions may affect the macro- and micromolecules in a cell including minerals, lipids, proteins, hormones, carbohydrates, or even DNA or RNA [50]. The combination of drought with salt, high- or low-temperature stress conditions becomes more severe for the plants, which affects the plants’ growth, development, and signal transduction [51, 52]. Besides the abovementioned macro−/micromolecules, photosynthesis that needs water is adversely affected by environmental stress conditions [53, 54]. Additional to the above, drought conditions may affect the metabolism of the plants because catabolism is enhanced due to hydrolytic enzymatic activity while anabolism is decreased due to lowering synthase activity [52]. In short, drought stress conditions adversely affect the photosynthesis in the chloroplast by decreased nutrient uptake and ion transport [55, 56].
2.2 Effect of stress conditions on gene expression
Stress conditions may activate the defense mechanism of the plants and result the change in different gene expression. The expression of heat shock proteins has been reported to be changed due to heat stress [57]. Heat shock proteins function as chaperones and safeguard the heat sensitive organelles and intra-cellular processes [2]. Proteins other than HSPs have also been reported to get produced and their expression is regulated differentially under heat stress conditions [58]. Besides the HSPs expression under heat stress conditions, these proteins have also been up-regulated under different stress conditions including heavy metal, cold, salt, drought, and oxidative stress conditions [43, 59, 60, 61, 62].
3. Heat shock proteins (HSPs)
Heat shock response has been characterized in salivary glands of
3.1 Role of heat shock proteins
Genes encoding HSPs respond to abiotic stress factors like high temperature, drought, salt, and low-temperature stress conditions [66]. HSPs having low expression under normal environmental conditions may have different function like chaperone function, prevention of proteins aggregation and folding, as well as to target the miss-folded proteins toward the specific pathways or for degradation [67]. Additional to the HSPs expression under abiotic stress conditions, these proteins have differential expression in different tissues and organelles. Taking all together, HSPs production is to protect the metabolic apparatus for adaptation under different environmental conditions and survival [68].
3.2 Types of HSPs
HSPs are divided into two classes based on their molecular weight, that is, high molecular weight heat shock proteins (HSP100, HSP90, HSP70, HSP60, and HSP40) and low molecular weight heat shock proteins (sHSPs), the weight of which is ranging from 15 to 30 kDa [69].
3.2.1 High molecular weight heat shock proteins
High molecular weight heat shock proteins are further divided into different classes based on molecular weight, that is, HSP100, HSP90, HSP70, and HSP60, the details of which are as below.
3.2.1.1 HSP100
HSP100 (protein family), found in all organisms from prokaryotes to eukaryotes [70], possess two subunits and are reported primarily in prokaryotes, that is, bacteria: (1) large-subunit (ClpA) which is ATP-dependent unfoldase and (2) protease which is a small-subunit ClpP [71]. Nucleotide-binding domain 1 & 2 (NBD1 & NBD2), carboxyl domains, middle domain, and amino and are the five parts of HSP100 proteins family members [72].
HSP100 genes have been reported to be up-regulated under heat stress conditions while the same pattern of expression has not been observed [73] but earlier than these findings, researchers have reported the expression of a member of HSP100 family under abscisic acid (ABA), cold and salt stresses additional to the high-temperature stress conditions [74]. Differential expression of one gene or this family member has been suggested under different abiotic stress conditions [75]. HSP100 family members have been reported with up-regulation under heat stress conditions in different plants like wheat and tobacco [75], rice [74],
3.2.1.2 HSP90
All organisms from prokaryotes to eukaryotes have HSP90 [81] and are involved to activate the component proteins involved in proteins transportation, assembling, folding and signal transduction [82]. Seven different isoforms of HSP90 have been identified in
3.2.1.3 HSP70
HSP70 are expressed under normal conditions in plants so these are also named as heat shock cognates [85]. HSP70 are having important role under different environmental conditions including heat stress [86, 87]. This class of proteins may function to stabilize the unstable proteins [82] additional to the proteins transport among sub-cellular compartments and proteins folding [88].
HSP70 family proteins may be classified into four classes based on the sub-cellular localization and thus are localized in four different compartments (cytosol, mitochondria, plastids, and endoplasmic reticulum) of the cell [89].
3.2.1.4 HSP60
HSP60 family members encoded by nuclear DNA [90] are present in prokaryotes to eukaryotes and have function in cells under stress and normal conditions [91]. Bacterial HSP60 plays role in proteins assembling to form complexes (oligomeric) and movement through cell membrane [91] but the same family proteins are involved in organelle (chloroplast and mitochondria)-specific proteins folding [91].
3.2.2 Small heat shock proteins (sHSPs)
Plants’ small heat shock proteins having molecular weight from 15 to 30 kDa are encoded by nuclear DNA and are classified into further six classes based on sub-cellular localization [92]. Researchers have classified the abovementioned proteins as per the localization in different cellular organelles, that is, first two are localized in cytosol and the next three classes (III, IV, and V) are localized in endoplasmic reticulum, mitochondria, and plastids, respectively [93]. Additional to the above, class VI has been reported to be localized in endoplasmic reticulum [94].
C-terminal region, N-terminal region, and α-crystallin domain are the three main parts of small heat shock proteins. Small HSPs are characterized by 100 amino acids sequence having α-crystalline domain [95] as well as N-terminal region on one side and C-terminal region on the other side of the formerly mentioned domain [96]. The abovementioned three domains are the conserved regions of small heat shock proteins [97].
Small HSPs expression has been reported in different plants, for example,
3.2.3 Chloroplast small heat shock proteins (Cp-sHSPs) and their role
Cp-sHSPs are produced in cytoplasm followed by its import toward chloroplast [105]. As the name shows, these kinds of proteins are located in chloroplast and have consensus-III or methionine rich region at the N-terminal region additional to the other sHSPs-specific regions [106].
These proteins protect photosynthesis of the plants under heat and oxidative stress conditions [107]. There are different mechanisms to protect photosynthesis, for example, chloroplast membrane stabilization or avoiding everlasting proteins aggregation [108] but the role of Cp-sHSPs is very important in this case [109]. Different researchers have shown the relation of sHSPs with the adaptation of the plants under environmental stress conditions [43, 60, 61, 62, 109, 110].
It has been established in vitro by researchers that these chloroplast-specific proteins may protect photosynthetic electron transport under high-temperature stress conditions [59]. Cp-sHSPs associate with photosystem II (PS II) through oxygen-evolving complex (OEC) proteins under high-temperature conditions. It has been confirmed by researchers that these proteins protect PS II from inactivation under heat stress conditions by the protection of oxygen evolution and OEC proteins but have no capability to repair inactivated PS II [107].
4. HSP gene expression and promoters
Promoters regulate gene expression quantitatively and qualitatively [111]. There are three types of promoters that regulate the gene expression, that is, inducible, spatiotemporal, and constitutive promoters. Constitutive promoters promote the gene expression throughout the tissues irrespective to the environmental and developmental conditions, while spatiotemporal promoters direct the target gene expression in specific tissues, but inducible promoters are independent of the endogenous factors but dependent upon the external stimuli and environmental conditions [112]. Almost all kinds of promoters have the same core sequence with TATA-box, initiator, and the TF binding-specific cis-acting motifs specific to the target genes [113].
There are very less reports about the regulation of organelle-localized sHSPs under specific stress conditions or even under combination of stresses though it has been known that these genes are mainly regulated at transcriptional level. Researchers have reported the use of soybean promoter (GmHSP17.3B) to induce the sHSPs expression in
Heat shock transcription factors (HSFs) and heat shock elements (HSEs) may control the HSPs expression in the result of complex network of interaction [117]. HSFs (more than 20 in number) [118] may control the heat shock response both in vitro and in vivo [119]. Thermotolerance is increased in the result of higher expression of HSPs that is resulted by binding the HSFs to HSEs [120, 121]. Differential expression of HSPs is resulted by the variations in HSEs of HSPs. These HSEs have difference in the location and arrangements of its basic units (nGAAn), for example, AtHsp90–1 gene promoter has heat shock element 1 (HSE1) (tGAAgcTTCtgGAAt), heat shock element 2 (HSE2) (agTCtcGAAacGAAaaGAActTTCtgGAAt), and heat shock element 3 (HSE3) (gGAAgaaTCcaGAAt) [122]. Additional to the above elements, other motifs to regulate HSPs (gap-type 1, gap-type 2, and gap-type 3 with the sequences nTTCnnGAAn[5bp]nGAAn, nTTCn[1bp]nGAAn[5bp]nGAAn and nTTCn[2bp]nGAAn[5bp]nGAAn respectively) have also been reported. Researchers have also reported TTC-rich type regulatory elements with 2–4 units of nTTCn with 0–8 bp gap {e.g., TTC-rich 1 (nTTCn[1bp]nTTCn[6bp]nTTCn) and 3 (nTTCnnTTCn[8bp]nTTCn[1bp]nTTCn)} that have binding capability with HsfA1a of
5. Model to express the Cp-sHSPs under different environmental conditions
There is no model put forward by researchers to control the expression of chloroplast-specific small heat shock proteins (Cp-sHSPs), but a model (Figure 1) to control the formerly mentioned genes has been proposed by Haq et al. [62]. According to this model, the presence of different cis-regulatory elements in Cp-sHSPs promoter shows the role of Cp-sHSPs under different abiotic stress conditions, that is, salt, drought, cold, metal, and high-temperature stress conditions. Cp-sHSPs in
Figure 1.
Proposed model of expression and role of Cp-sHSPs [
References
- 1.
Parsell DA, Lindquist S. The function of heat-shock proteins in stress tolerance: Degradation and reactivation of damaged proteins. Annual Review of Genetics. 1993; 27 :437-496 - 2.
Lindquist S. The heat-shock response. Annual Review of Biochemistry. 1986; 55 :1151-1191 - 3.
Balestrasse KB, Tomaro ML, Batlle A, Noriega GO. The role of 5-aminolevulinic acid in the response to cold stress in soybean plants. Phytochemistry. 2010; 71 :2038-2045 - 4.
Zhang H, Mao X, Wang C, Jing R. Overexpression of a common wheat gene TaSnRK2.8 enhances tolerance to drought, salt and low temperature in Arabidopsis . PLoS One. 2010;5 :e16041 - 5.
Zhang M, Li G, Huang W, Bi T, Chen G, Tang Z, et al. Proteomic study of Carissa spinarum in response to combined heat and drought stress. Proteomics. 2010;10 :3117-3129 - 6.
Khan A, Tan DKY, Afridi MZ, Luo H, Tung SA, Ajab M, et al. Nitrogen fertility and abiotic stresses management in cotton crop: A review. Environmental Science and Pollution Research International. 2017; 24 :14551-14566 - 7.
Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, et al. Crop production under drought and heat stress: Plant responses and management options. Frontiers in Plant Science. 2017; 8 :1147 - 8.
Fahad S, Bano A. Effect of salicylic acid on physiological and biochemical characterization of maize grown in saline area. Pakistan Journal of Botany. 2012; 44 :1433-1438 - 9.
Lefebvre V, Kiani SP, Durand-Tardif M. A focus on natural variation for abiotic constraints response in the model species Arabidopsis thaliana . International Journal of Molecular Sciences. 2009;10 :3547-3582 - 10.
Tuteja N, Ahmad P, Panda BB, Tuteja R. Genotoxic stress in plants: Shedding light on DNA damage, repair and DNA repair helicases. Mutation Research. 2009; 681 :134-149 - 11.
Dangl JL, Jones JD. Plant pathogens and integrated defence responses to infection. Nature. 2001; 411 :826-833 - 12.
Collinge M, Boller T. Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding. Plant Molecular Biology. 2001;46 :521-529 - 13.
Agarwal PK, Agarwal P, Reddy MK, Sopory SK. Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Reports. 2006; 25 :1263-1274 - 14.
Kvaalen H, Johnsen O. Timing of bud set in Picea abies is regulated by a memory of temperature during zygotic and somatic embryogenesis. The New Phytologist. 2008;177 :49-59 - 15.
Boyer JS. Plant productivity and environment. Science. 1982; 218 :443-448 - 16.
Chinnusamy V, Zhu J, Zhu JK. Cold stress regulation of gene expression in plants. Trends in Plant Science. 2007; 12 :444-451 - 17.
Ilik P, Kouril R, Kruk J, Mysliwa-Kurdziel B, Popelkova H, Strzalka K, et al. Origin of chlorophyll fluorescence in plants at 55-75°C. Photochemistry and Photobiology. 2003; 77 :68-76 - 18.
Lichtenthaler HK. The stress concept in plants: An introduction. Annals of the New York Academy of Sciences. 1998; 851 :187-198 - 19.
Keren N, Berg A, van Kan PJ, Levanon H, Ohad I. Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: The role of back electron flow. Proceedings of the National Academy of Sciences of the United States of America. 1997; 94 :1579-1584 - 20.
Zinn KE, Tunc-Ozdemir M, Harper JF. Temperature stress and plant sexual reproduction: Uncovering the weakest links. Journal of Experimental Botany. 2010; 61 :1959-1968 - 21.
Frank G, Pressman E, Ophir R, Althan L, Shaked R, Freedman M, et al. 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. 2009;60 :3891-3908 - 22.
Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF. Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiology. 2002;130 :2129-2141 - 23.
Thakur P, Kumar S, Malik JA, Berger JD, Nayyar H. Cold stress effects on reproductive development in grain crops: An overview. Environmental and Experimental Botany. 2010; 67 :429-443 - 24.
Apel K, Hirt H. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology. 2004; 55 :373-399 - 25.
Strasser BJ. Donor side capacity of photosystem II probed by chlorophyll a fluorescence transients. Photosynthesis Research. 1997; 52 :147-155 - 26.
Walther W, Stein U. Heat-responsive gene expression for gene therapy. Advanced Drug Delivery Reviews. 2009; 61 :641-649 - 27.
Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ. Plant responses to cold: Transcriptome analysis of wheat. Plant Biotechnology Journal. 2010; 8 :749-771 - 28.
Lee TM, Lur HS. Role of abscisic acid in cold tolerance of rice ( Oryza sativa L.) seedlings. II. Modulation of free polyamine levels. Plant Science. 1997;126 :1-10 - 29.
Xing W, Rajashekar CB. Glycine betaine involvement in freezing tolerance and water stress in Arabidopsis thaliana . Environmental and Experimental Botany. 2001;46 :21-28 - 30.
Li XG, Duan W, Meng QW, Zou Q , Zhao SJ. The function of chloroplastic NAD(P)H dehydrogenase in tobacco during chilling stress under low irradiance. Plant & Cell Physiology. 2004; 45 :103-108 - 31.
Ivanov AG, Morgan RM, Gray GR, Velitchkova MY, Huner NP. Temperature/light dependent development of selective resistance to photoinhibition of photosystem I. FEBS Letters. 1998; 430 :288-292 - 32.
Teicher HB, Moller BL, Scheller HV. Photoinhibition of photosystem I in field-grown barley ( Hordeum vulgare L.): Induction, recovery and acclimation. Photosynthesis Research. 2000;64 :53-61 - 33.
Thomashow MF. Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology. 1999; 50 :571-599 - 34.
Fowler S, Thomashow MF. Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. The Plant Cell. 2002;14 :1675-1690 - 35.
Bekesiova B, Hraska S, Libantova J, Moravcikova J, Matusikova I. Heavy-metal stress induced accumulation of chitinase isoforms in plants. Molecular Biology Reports. 2008; 35 :579-588 - 36.
Pavlikova D, Pavlik M, Staszkova L, Motyka V, Szakova J, Tlustos P, et al. Glutamate kinase as a potential biomarker of heavy metal stress in plants. Ecotoxicology and Environmental Safety. 2008; 70 :223-230 - 37.
Ma JF, Yamaji N, Mitani N, Xu XY, Su YH, McGrath SP, et al. Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proceedings of the National Academy of Sciences of the United States of America. 2008; 105 :9931-9935 - 38.
Metwally A, Safronova VI, Belimov AA, Dietz KJ. Genotypic variation of the response to cadmium toxicity in Pisum sativum L. Journal of Experimental Botany. 2005;56 :167-178 - 39.
Hart JJ, Welch RM, Norvell WA, Kochian LV. Characterization of cadmium uptake, translocation and storage in near-isogenic lines of durum wheat that differ in grain cadmium concentration. The New Phytologist. 2006; 172 :261-271 - 40.
Ahsan N, Renaut J, Komatsu S. Recent developments in the application of proteomics to the analysis of plant responses to heavy metals. Proteomics. 2009; 9 :2602-2621 - 41.
Van Assche F, Clijsters H. Inhibition of photosynthesis in Phaseolus valgaris by treatment with toxic concentration of zinc: Effects on electron transport and photophosphorylation. Physiologia Plantarum. 1986;66 :717-721 - 42.
Kupper H, Kupper F, Spiller M. Environmental relevance of heavy metal substituted chlorophylls using the example of water plants. Journal of Experimental Botany. 1996; 47 :259-266 - 43.
Sahr T, Voigt G, Paretzke HG, Schramel P, Ernst D. Caesium-affected gene expression in Arabidopsis thaliana . The New Phytologist. 2005;165 :747-754 - 44.
Ingle RA, Smith JA, Sweetlove LJ. Responses to nickel in the proteome of the hyperaccumulator plant Alyssum lesbiacum . Biometals. 2005;18 :627-641 - 45.
Kieffer P, Dommes J, Hoffmann L, Hausman JF, Renaut J. Quantitative changes in protein expression of cadmium-exposed poplar plants. Proteomics. 2008; 8 :2514-2530 - 46.
Haq NU, Raza S, Luthe DS, Heckathorn SA, Shakeel SN. A dual role for the chloroplast small heat shock protein of Chenopodium album including protection from both heat and metal stress. Plant Molecular Biology Reporter. 2013;31 :398-408 - 47.
Kader MA, Lindberg S. Uptake of sodium in protoplasts of salt-sensitive and salt-tolerant cultivars of rice, Oryza sativa L. determined by the fluorescent dye SBFI. Journal of Experimental Botany. 2005;56 :3149-3158 - 48.
Flowers TJ, Colmer TD. Salinity tolerance in halophytes. The New Phytologist. 2008; 179 :945-963 - 49.
Kader MA, Lindberg S. Cytosolic calcium and pH signaling in plants under salinity stress. Plant Signaling & Behavior. 2010; 5 :233-238 - 50.
Munns R, James RA, Lauchli A. Approaches to increasing the salt tolerance of wheat and other cereals. Journal of Experimental Botany. 2006; 57 :1025-1043 - 51.
Flexas J, Diaz-Espejo A, Galmes J, Kaldenhoff R, Medrano H, Ribas-Carbo M. Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant, Cell & Environment. 2007; 30 :1284-1298 - 52.
Lawlor DW, Cornic G. Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant, Cell & Environment. 2002; 25 :275-294 - 53.
Chae L, Sudat S, Dudoit S, Zhu T, Luan S. Diverse transcriptional programs associated with environmental stress and hormones in the Arabidopsis receptor-like kinase gene family. Molecular Plant. 2009;2 :84-107 - 54.
Halliwell B. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiology. 2006; 141 :312-322 - 55.
Ni FT, Chu LY, Shao HB, Liu ZH. Gene expression and regulation of higher plants under soil water stress. Current Genomics. 2009; 10 :269-280 - 56.
Bray EA. Genes commonly regulated by water-deficit stress in Arabidopsis thaliana . Journal of Experimental Botany. 2004;55 :2331-2341 - 57.
Andjelkovic V, Thompson R. Changes in gene expression in maize kernel in response to water and salt stress. Plant Cell Reports. 2006; 25 :71-79 - 58.
Boudsocq M, Lauriere C. Osmotic signaling in plants: Multiple pathways mediated by emerging kinase families. Plant Physiology. 2005; 138 :1185-1194 - 59.
Brooker RW. Plant-plant interactions and environmental change. The New Phytologist. 2006; 171 :271-284 - 60.
Feder ME, Hofmann GE. Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology. Annual Review of Physiology. 1999; 61 :243-282 - 61.
Wahid A, Gelani S, Ashraf M, Foolad MR. Heat tolerance in plants: An overview. Environmental and Experimental Botany. 2007; 61 :199-223 - 62.
Heckathorn SA, Downs CA, Sharkey TD, Coleman JS. The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiology. 1998; 116 :439-444 - 63.
Heckathorn SA, Ryan SL, Baylis JA, Wang D, Hamilton IEW, Cundiff L, et al. In vivo evidence from an Agrostis stolonifera selection genotype that chloroplast small heat-shock proteins can protect photosystem II during heat stress. Functional Plant Biology. 2002;29 :933-944 - 64.
Shakeel S, Haq NU, Heckathorn SA, Hamilton EW, Luthe DS. Ecotypic variation in chloroplast small heat-shock proteins and related thermotolerance in Chenopodium album . Plant Physiology and Biochemistry. 2011;49 :898-908 - 65.
Haq NU, Ammar M, Bano A, Luthe DS, Heckathorn SA, Shakeel SN. Molecular characterization of Chenopodium album chloroplast small heat shock protein and its expression in response to different abiotic stresses. Plant Molecular Biology Reporter. 2013;31 :1230-1241 - 66.
Ritossa FM. A new puffing pattern induced by a temperature shock and DNP in Drosophila . Experientia. 1962;18 :571-573 - 67.
Ashburner M, Bonner JJ. The induction of gene activity in Drosophila by heat shock. Cell. 1979;17 :241-254 - 68.
Taylor RP, Benjamin IJ. Small heat shock proteins: A new classification scheme in mammals. Journal of Molecular and Cellular Cardiology. 2005; 38 :433-444 - 69.
Cho EK, Hong CB. Molecular cloning and expression pattern analyses of heat shock protein 70 genes from Nicotiana tabacum . Journal of Plant Biology. 2004;47 :149-159 - 70.
Kalmar B, Greensmith L. Induction of heat shock proteins for protection against oxidative stress. Advanced Drug Delivery Reviews. 2009; 61 :310-318 - 71.
Huang B, Xu C. Identification and characterization of proteins associated with plant tolerance to heat stress. Journal of Integrative Plant Biology. 2008; 50 :1230-1237 - 72.
Tower J. Hsps and aging. Trends in Endocrinology and Metabolism. 2009; 20 :216-222 - 73.
Agarwal M, Katiyar-Agarwal S, Sahi C, Gallie DR, Grover A. Arabidopsis thaliana Hsp100 proteins: Kith and kin. Cell Stress & Chaperones. 2001;6 :219-224 - 74.
Gottesman S, Squires C, Pichersky E, Carrington M, Hobbs M, Mattick JS, et al. Conservation of the regulatory subunit for the Clp ATP-dependent protease in prokaryotes and eukaryotes. Proceedings of the National Academy of Sciences of the United States of America. 1990; 87 :3513-3517 - 75.
Batra G, Chauhan VS, Singh A, Sarkar NK, Grover A. Complexity of rice Hsp100 gene family: Lessons from rice genome sequence data. Journal of Biosciences. 2007; 32 :611-619 - 76.
Agarwal M, Katiyar-Agarwal S, Grover A. Plant Hsp100 proteins: Structure, function and regulation. Plant Science. 2002; 163 :397-405 - 77.
Pareek A, Singla SL, Grover A. Immunological evidence for accumulation of two high-molecular-weight (104 and 90 kDa) HSPs in response to different stresses in rice and in response to high temperature stress in diverse plant genera. Plant Molecular Biology. 1995; 29 :293-301 - 78.
Campbell JL, Klueva NY, Zheng HG, Nieto-Sotelo J, Ho TD, Nguyen HT. Cloning of new members of heat shock protein HSP101 gene family in wheat ( Triticum aestivum (L.) Moench) inducible by heat, dehydration, and ABA(1). Biochimica et Biophysica Acta. 2001;1517 :270-277 - 79.
Schirmer EC, Lindquist S, Vierling E. An Arabidopsis heat shock protein complements a thermotolerance defect in yeast. The Plant Cell. 1994;6 :1899-1909 - 80.
Lee YR, Nagao RT, Key JL. A soybean 101-kD heat shock protein complements a yeast HSP104 deletion mutant in acquiring thermotolerance. The Plant Cell. 1994; 6 :1889-1897 - 81.
Nieto-Sotelo J, Kannan KB, Martinez LM, Segal C. Characterization of a maize heat-shock protein 101 gene, HSP101, encoding a ClpB/Hsp100 protein homologue. Gene. 1999; 230 :187-195 - 82.
Queitsch C, Hong SW, Vierling E, Lindquist S. Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis . The Plant Cell. 2000;12 :479-492 - 83.
Singla SL, Pareek A, Grover A. Plant Hsp 100 family with special reference to rice. Journal of Biosciences. 1998; 23 :337-345 - 84.
Wegele H, Muller L, Buchner J. Hsp70 and Hsp90--a relay team for protein folding. Reviews of Physiology, Biochemistry and Pharmacology. 2004; 151 :1-44 - 85.
Garavaglia BS, Garafalo CG, Orellano EG, Ottado J. Hsp70 and Hsp90 expression in citrus and pepper plants in response to Xanthomonas axonopodis pv.citri. European Journal of Plant Pathology. 2009;123 :91-97 - 86.
Krishna P, Gloor G. The Hsp90 family of proteins in Arabidopsis thaliana . Cell Stress & Chaperones. 2001;6 :238-246 - 87.
Yabe N, Takahashi T, Komeda Y. Analysis of tissue-specific expression of Arabidopsis thaliana HSP90-family gene HSP81. Plant & Cell Physiology. 1994;35 :1207-1219 - 88.
Sung DY, Kaplan F, Guy CL. Plant Hsp70 molecular chaperones: Protein structure, gene family, expression and function. Physiologia Plantarum. 2001; 113 :443-451 - 89.
Wu CH, Caspar T, Browse J, Lindquist S, Somerville C. Characterization of an HSP70 cognate gene family in Arabidopsis . Plant Physiology. 1988;88 :731-740 - 90.
Miersch J, Grancharov K. Cadmium and heat response of the fungus Heliscus lugdunensis isolated from highly polluted and unpolluted areas. Amino Acids. 2008;34 :271-277 - 91.
Fink AL. Chaperone-mediated protein folding. Physiological Reviews. 1999; 79 :425-449 - 92.
Nikolaidis N, Nei M. Concerted and nonconcerted evolution of the Hsp70 gene superfamily in two sibling species of nematodes. Molecular Biology and Evolution. 2004; 21 :498-505 - 93.
Reading DS, Hallberg RL, Myers AM. Characterization of the yeast HSP60 gene coding for a mitochondrial assembly factor. Nature. 1989; 337 :655-659 - 94.
Craig EA, Gambill BD, Nelson RJ. Heat shock proteins: Molecular chaperones of protein biogenesis. Microbiological Reviews. 1993; 57 :402-414 - 95.
Gao C, Jiang B, Wang Y, Liu G, Yang C. Overexpression of a heat shock protein (ThHSP18.3) from Tamarix hispida confers stress tolerance to yeast. Molecular Biology Reports. 2011;39 :4889-4897 - 96.
Heckathorn SA, Downs CA, Coleman JS. Small heat shock proteins protect electron transport in chloroplasts and mitochondria during stress. American Zoologist. 1999; 39 :865-876 - 97.
LaFayette PR, Nagao RT, O’Grady K, Vierling E, Key JL. Molecular characterization of cDNAs encoding low-molecular-weight heat shock proteins of soybean. Plant Molecular Biology. 1996; 30 :159-169 - 98.
Kappe G, Leunissen JA, de Jong WW. Evolution and diversity of prokaryotic small heat shock proteins. Progress in Molecular and Subcellular Biology. 2002; 28 :1-17 - 99.
Nakamoto H, Vigh L. The small heat shock proteins and their clients. Cellular and Molecular Life Sciences. 2007; 64 :294-306 - 100.
Laksanalamai P, Robb FT. Small heat shock proteins from extremophiles: A review. Extremophiles. 2004; 8 :1-11 - 101.
Malik MK, Slovin JP, Hwang CH, Zimmerman JL. Modified expression of a carrot small heat shock protein gene, hsp17. 7, results in increased or decreased thermotolerance double dagger. The Plant Journal. 1999; 20 :89-99 - 102.
Tiroli AO, Ramos CH. Biochemical and biophysical characterization of small heat shock proteins from sugarcane. Involvement of a specific region located at the N-terminus with substrate specificity. The International Journal of Biochemistry & Cell Biology. 2007; 39 :818-831 - 103.
Lujan R, Lledias F, Martinez LM, Barreto R, Cassab GI, Nieto-Sotelo J. Small heat-shock proteins and leaf cooling capacity account for the unusual heat tolerance of the central spike leaves in Agave tequilana var.weber. Plant, Cell & Environment. 2009;32 :1791-1803 - 104.
Dafny-Yelin M, Tzfira T, Vainstein A, Adam Z. Nonredundant functions of sHSP-CIs in acquired thermotolerance and their role in early seed development in Arabidopsis . Plant Molecular Biology. 2008;67 :363-373 - 105.
Maqbool A, Abbas W, Rao AQ , Irfan M, Zahur M, Bakhsh A, et al. Gossypium arboreum GHSP26 enhances drought tolerance inGossypium hirsutum . Biotechnology Progress. 2010;26 :21-25 - 106.
Cao Z, Jia Z, Liu Y, Wang M, Zhao J, Zheng J, et al. Constitutive expression of ZmsHSP in Arabidopsis enhances their cytokinin sensitivity. Molecular Biology Reports. 2010;37 :1089-1097 - 107.
Hamilton Iii EW, Coleman JS. Heat-shock proteins are induced in unstressed leaves of Nicotiana attenuata (Solanaceae) when distant leaves are stressed. American Journal of Botany. 2001;88 :950-955 - 108.
Vierling E. The roles of heat shock proteins in plants. Annual Review of Plant Physiology and Plant Molecular Biology. 1991; 42 :579-620 - 109.
Chen Q , Vierling E. Analysis of conserved domains identifies a unique structural feature of a chloroplast heat shock protein. Molecular & General Genetics. 1991; 226 :425-431 - 110.
Nakamoto H, Suzuki N, Roy SK. Constitutive expression of a small heat-shock protein confers cellular thermotolerance and thermal protection to the photosynthetic apparatus in cyanobacteria. FEBS Letters. 2000; 483 :169-174 - 111.
Torok Z, Goloubinoff P, Horvath I, Tsvetkova NM, Glatz A, Balogh G, et al. Synechocystis HSP17 is an amphitropic protein that stabilizes heat-stressed membranes and binds denatured proteins for subsequent chaperone-mediated refolding. Proceedings of the National Academy of Sciences of the United States of America. 2001; 98 :3098-3103 - 112.
Hamilton EW, Heckathorn SA. Mitochondrial adaptations to NaCl. Complex I is protected by anti-oxidants and small heat shock proteins, whereas complex II is protected by proline and betaine. Plant Physiology. 2001; 126 :1266-1274 - 113.
Shakeel SN, Haq NU, Heckathorn S, Luthe DS. Analysis of gene sequences indicates that quantity not quality of chloroplast small HSPs improves thermotolerance in C4 and CAM plants. Plant Cell Reports. 2012; 31 :1943-1957 - 114.
Kang TJ, Kwon TH, Kim TG, Loc NH, Yang MS. Comparing constitutive promoters using CAT activity in transgenic tobacco plants. Molecules and Cells. 2003; 16 :117-122 - 115.
Potenza C, Aleman L, Sengupta-Gopalan C. Targeting transgene expression in research, agricultural, and environmental applications: Promoters used in plant transformation. In Vitro Cellular & Developmental Biology. Plant. 2004; 40 :1-22 - 116.
Peremarti A, Twyman RM, Gomez-Galera S, Naqvi S, Farre G, Sabalza M, et al. Promoter diversity in multigene transformation. Plant Molecular Biology. 2010; 73 :363-378 - 117.
Saidi Y, Domini M, Choy F, Zryd JP, Schwitzguebel JP, Goloubinoff P. Activation of the heat shock response in plants by chlorophenols: Transgenic Physcomitrella patens as a sensitive biosensor for organic pollutants. Plant, Cell & Environment. 2007;30 :753-763 - 118.
Guan JC, Jinn TL, Yeh CH, Feng SP, Chen YM, Lin CY. Characterization of the genomic structures and selective expression profiles of nine class I small heat shock protein genes clustered on two chromosomes in rice ( Oryza sativa L.). Plant Molecular Biology. 2004;56 :795-809 - 119.
Sun W, Van Montagu M, Verbruggen N. Small heat shock proteins and stress tolerance in plants. Biochimica et Biophysica Acta. 2002; 1577 :1-9 - 120.
Guan JC, Yeh CH, Lin YP, Ke YT, Chen MT, You JW, et al. A 9 bp cis-element in the promoters of class I small heat shock protein genes on chromosome 3 in rice mediates L-azetidine-2-carboxylic acid and heat shock responses. Journal of Experimental Botany. 2010; 61 :4249-4261 - 121.
Nover L, Bharti K, Doring P, Mishra SK, Ganguli A, Scharf KD. Arabidopsis and the heat stress transcription factor world: How many heat stress transcription factors do we need? Cell Stress and Chaperones. 2001;6 :177-189 - 122.
Guo L, Chen S, Liu K, Liu Y, Ni L, Zhang K, et al. Isolation of heat shock factor HsfA1a-binding sites in vivo revealed variations of heat shock elements in Arabidopsis thaliana . Plant and Cell Physiology. 2008;49 :1306-1315 - 123.
Lee JH, Hubel A, Schoffl F. Derepression of the activity of genetically engineered heat shock factor causes constitutive synthesis of heat shock proteins and increased thermotolerance in transgenic Arabidopsis . The Plant Journal. 1995;8 :603-612 - 124.
Wunderlich M, Werr W, Schoffl F. Generation of dominant-negative effects on the heat shock response in Arabidopsis thaliana by transgenic expression of a chimaeric HSF1 protein fusion construct. The Plant Journal. 2003;35 :442-451 - 125.
Haralampidis K, Milioni D, Rigas S, Hatzopoulos P. Combinatorial interaction of cis elements specifies the expression of the Arabidopsis AtHsp90-1 gene. Plant Physiology. 2002;129 :1138-1149 - 126.
Amin J, Ananthan J, Voellmy R. Key features of heat shock regulatory elements. Molecular and Cellular Biology. 1988; 8 :3761-37619 - 127.
Xiao H, Lis JT. Germline transformation used to define key features of heat-shock response elements. Science. 1988; 239 :1139-1142 - 128.
Schoffl F, Prandl R, Reindl A. Regulation of the heat-shock response. Plant Physiology. 1998; 117 :1135-1141 - 129.
Karin M, Haslinger A, Heguy A, Dietlin T, Cooke T. Metal-responsive elements act as positive modulators of human metallothionein-IIA enhancer activity. Molecular and Cellular Biology. 1987; 7 :606-613