**Chapter 16** HSPs under Abiotic Stresses

*Noor ul Haq and Samina N. Shakeel*

## **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 subcellular 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 [4–8], 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 hightemperature 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 downregulated 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 *Arabidopsis thaliana* [31].

#### *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

**339**

*HSPs under Abiotic Stresses*

*2.1.4 Salt stress*

*2.1.5 Drought stress*

*DOI: http://dx.doi.org/10.5772/intechopen.93787*

changed photosynthetic metabolism [49].

decreased nutrient uptake and ion transport [55, 56].

**2.2 Effect of stress conditions on gene expression**

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

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].

Plants respond differentially to the heavy metal toxicity [35] and that is the reason

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

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

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].

the plants following the pathways of the essential elements transport [34].

#### *HSPs under Abiotic Stresses DOI: http://dx.doi.org/10.5772/intechopen.93787*

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*

*Abiotic Stress in Plants*

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

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 hightemperature 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].

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

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

Expression of different genes and proteins has been reported to be up- or downregulated 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 *Arabidopsis thaliana* [31].

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

cellular respiration [25] as well as damages the cell membrane [26].

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*

*2.1.2 Low temperature or cold stress*

**338**

barley [28, 29].

*2.1.3 Metal 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, 59–62].

## **3. Heat shock proteins (HSPs)**

Heat shock response has been characterized in salivary glands of *Drosophila* [63]. Heat shock proteins have been studied in the result of transcription and translation in chromosomal puffs with active sites [64]. HSPs are produced in all organisms, that is, from bacteria to humans under changed environmental conditions [2] and have chaperone activity that protects the proteins from damage [65].

#### **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

**341**

shock proteins [97].

*HSPs under Abiotic Stresses*

plants [80].

*3.2.1.2 HSP90*

*3.2.1.3 HSP70*

*3.2.1.4 HSP60*

*DOI: http://dx.doi.org/10.5772/intechopen.93787*

expressed under heat stress conditions [84].

*3.2.2 Small heat shock proteins (sHSPs)*

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], *Arabidopsis thaliana* [76], soybean [77] and maize [78]. Besides the above, HSP100 family members have also been reported with differential expression at different developmental stages [79] which may be the reason that HSP100 family members have been reported with high concentration in mature seeds of different

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 *Arabidopsis* and are classified based on sub-cellular localization, that is, three have been reported to be localized in endoplasmic reticulum, chloroplast, and mitochondria while the remaining four are localized in cytosole [83]. Three among the four cytosolic isoforms are expressed constitutively while fourth one is

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

HSP70 family proteins may be classified into four classes based on the subcellular localization and thus are localized in four different compartments (cytosol,

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].

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 subcellular 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,

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

class VI has been reported to be localized in endoplasmic reticulum [94].

among sub-cellular compartments and proteins folding [88].

mitochondria, plastids, and endoplasmic reticulum) of the cell [89].

#### *HSPs under Abiotic Stresses DOI: http://dx.doi.org/10.5772/intechopen.93787*

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], *Arabidopsis thaliana* [76], soybean [77] and maize [78]. Besides the above, HSP100 family members have also been reported with differential expression at different developmental stages [79] which may be the reason that HSP100 family members have been reported with high concentration in mature seeds of different plants [80].

#### *3.2.1.2 HSP90*

*Abiotic Stress in Plants*

oxidative stress conditions [43, 59–62].

**3. Heat shock proteins (HSPs)**

**3.1 Role of heat shock proteins**

**3.2 Types of HSPs**

is ranging from 15 to 30 kDa [69].

details of which are as below.

proteins family members [72].

*3.2.1.1 HSP100*

ent environmental conditions and survival [68].

*3.2.1 High molecular weight heat shock proteins*

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

Heat shock response has been characterized in salivary glands of *Drosophila* [63]. Heat shock proteins have been studied in the result of transcription and translation in chromosomal puffs with active sites [64]. HSPs are produced in all organisms, that is, from bacteria to humans under changed environmental conditions [2] and

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 differ-

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

High molecular weight heat shock proteins are further divided into different classes based on molecular weight, that is, HSP100, HSP90, HSP70, and HSP60, the

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

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

have chaperone activity that protects the proteins from damage [65].

**340**

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 *Arabidopsis* and are classified based on sub-cellular localization, that is, three have been reported to be localized in endoplasmic reticulum, chloroplast, and mitochondria while the remaining four are localized in cytosole [83]. Three among the four cytosolic isoforms are expressed constitutively while fourth one is expressed under heat stress conditions [84].

#### *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 subcellular 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 subcellular 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, *Chenopodium album* [43, 62], carrot [98], sugarcane [99], Agave [100], *Arabidopsis* [101], cotton [102], tomato [18], maize [103], tobacco [104], etc. The abovementioned studies of sHSPs in different plants show the importance of this class of HSPs in adaptation under different environmental conditions [92].

#### *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, 60–62, 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 oxygenevolving 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 *Physcomitrella patens* [114]. Additional to the above, researchers have also reported the rice promoter (Oshsp16.9A) to induce the expression of sHSPs under high-temperature stress conditions [115]. Small heat shock proteins have also been reported to get expressed under different abiotic stress conditions additional to the sHSPs expression at different developmental stages [43, 61, 62, 110, 116].

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

**343**

**Figure 1.**

*Proposed model of expression and role of Cp-sHSPs [65].*

*HSPs under Abiotic Stresses*

**conditions**

*DOI: http://dx.doi.org/10.5772/intechopen.93787*

difference in the location and arrangements of its basic units (nGAAn), for example, AtHsp90–1 gene promoter has heat shock element 1 (HSE1) (tGAAgcTTCtg-GAAt), 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 *Arabidopsis*. But some TTC-rich regions are also present with no binding potential with HsfA1a, for example, TTC-rich 2 (nTTCn[5bp]nTTCn[4bp]nTTCn) and TTC-rich 4 (nTTCn[3bp]nTTCn) [119]. Besides the above, other cis-regulatory elements are also present in HSPs promoter to regulate their expression under different growth conditions, for example, stress response elements (STREs), metal response elements (MREs), and CAAT boxes C/EBP [123–125]. Metalothionein gene of animals and plants has also been reported to get activated by heavy metal stress conditions because of the presence of MRE in promoter region of this gene [126–128]. Similarly, another stress-related element, that is, STRE (AGGGG) is also

regulated by different abiotic stress conditions in yeast [129].

**5. Model to express the Cp-sHSPs under different environmental** 

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

*HSPs under Abiotic Stresses DOI: http://dx.doi.org/10.5772/intechopen.93787*

*Abiotic Stress in Plants*

Small HSPs expression has been reported in different plants, for example, *Chenopodium album* [43, 62], carrot [98], sugarcane [99], Agave [100], *Arabidopsis* [101], cotton [102], tomato [18], maize [103], tobacco [104], etc. The abovementioned studies of sHSPs in different plants show the importance of this class of HSPs

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

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

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 oxygenevolving 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

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 *Physcomitrella patens* [114]. Additional to the above, researchers have also reported the rice promoter (Oshsp16.9A) to induce the expression of sHSPs under high-temperature stress conditions [115]. Small heat shock proteins have also been reported to get expressed under different abiotic stress conditions additional to

the sHSPs expression at different developmental stages [43, 61, 62, 110, 116].

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

in adaptation under different environmental conditions [92].

the other sHSPs-specific regions [106].

*3.2.3 Chloroplast small heat shock proteins (Cp-sHSPs) and their role*

plants under environmental stress conditions [43, 60–62, 109, 110].

have no capability to repair inactivated PS II [107].

**4. HSP gene expression and promoters**

**342**

difference in the location and arrangements of its basic units (nGAAn), for example, AtHsp90–1 gene promoter has heat shock element 1 (HSE1) (tGAAgcTTCtg-GAAt), 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 *Arabidopsis*. But some TTC-rich regions are also present with no binding potential with HsfA1a, for example, TTC-rich 2 (nTTCn[5bp]nTTCn[4bp]nTTCn) and TTC-rich 4 (nTTCn[3bp]nTTCn) [119]. Besides the above, other cis-regulatory elements are also present in HSPs promoter to regulate their expression under different growth conditions, for example, stress response elements (STREs), metal response elements (MREs), and CAAT boxes C/EBP [123–125]. Metalothionein gene of animals and plants has also been reported to get activated by heavy metal stress conditions because of the presence of MRE in promoter region of this gene [126–128]. Similarly, another stress-related element, that is, STRE (AGGGG) is also regulated by different abiotic stress conditions in yeast [129].

#### **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

**Figure 1.** *Proposed model of expression and role of Cp-sHSPs [65].*

conditions, that is, salt, drought, cold, metal, and high-temperature stress conditions. Cp-sHSPs in *Chenopodium album* have been shown to protect thylakoid membranes and photosystem II under different abiotic stress conditions. Different abiotic stress conditions, that is, heat, cold, heavy metal, drought, and salt stress conditions may regulate the single Cp-sHSP transcript in *C. album* which produces the precursor proteins that have transit peptide which directs that toward chloroplast. The transit peptide is detached from the proteins while reaching toward chloroplast in the result of which these proteins are matured that have the function in chloroplast. As per this proposed model, differential regulation of the same Cp-sHSP family member in *C. album* makes it able to play multiple roles under different abiotic stress conditions, that is, salt, drought, heavy metal, cold, and heat stress conditions [62].

## **Author details**

Noor ul Haq1 \* and Samina N. Shakeel2

1 Department of Computer Science and Bioinformatics, Khushal Khan Khattak University, Karak, Khyber-Pakhtunkhwa, Pakistan

2 Department of Biochemistry, Quaid-i-Azam University, Islamabad, Pakistan

\*Address all correspondence to: noorqu@gmail.com; noorulhaq@kkkuk.edu.pk

© 2020 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

**345**

*HSPs under Abiotic Stresses*

[1] Parsell DA, Lindquist S. The

[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.

[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

[8] Fahad S, Bano A. Effect of salicylic acid on physiological and biochemical characterization of maize grown in saline area. Pakistan Journal of Botany.

[9] Lefebvre V, Kiani SP, Durand-Tardif M. A focus on natural variation

2017;**24**:14551-14566

Science. 2017;**8**:1147

2012;**44**:1433-1438

Genetics. 1993;**27**:437-496

**References**

*DOI: http://dx.doi.org/10.5772/intechopen.93787*

function of heat-shock proteins in stress tolerance: Degradation and reactivation of damaged proteins. Annual Review of

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

[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.

[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

[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.

[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

Phytologist. 2008;**177**:49-59

2006;**25**:1263-1274

2007;**12**:444-451

Research. 2009;**681**:134-149

## **References**

*Abiotic Stress in Plants*

stress conditions [62].

**344**

**Author details**

\* and Samina N. Shakeel2

University, Karak, Khyber-Pakhtunkhwa, Pakistan

provided the original work is properly cited.

1 Department of Computer Science and Bioinformatics, Khushal Khan Khattak

conditions, that is, salt, drought, cold, metal, and high-temperature stress conditions. Cp-sHSPs in *Chenopodium album* have been shown to protect thylakoid membranes and photosystem II under different abiotic stress conditions. Different abiotic stress conditions, that is, heat, cold, heavy metal, drought, and salt stress conditions may regulate the single Cp-sHSP transcript in *C. album* which produces the precursor proteins that have transit peptide which directs that toward chloroplast. The transit peptide is detached from the proteins while reaching toward chloroplast in the result of which these proteins are matured that have the function in chloroplast. As per this proposed model, differential regulation of the same Cp-sHSP family member in *C. album* makes it able to play multiple roles under different abiotic stress conditions, that is, salt, drought, heavy metal, cold, and heat

2 Department of Biochemistry, Quaid-i-Azam University, Islamabad, Pakistan

\*Address all correspondence to: noorqu@gmail.com; noorulhaq@kkkuk.edu.pk

© 2020 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium,

Noor ul Haq1

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[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. Heatresponsive 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.

**347**

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2008;**35**:579-588

2008;**70**:223-230

2006;**172**:261-271

2009;**9**:2602-2621

Heavy-metal stress induced

[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.

[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.

[40] Ahsan N, Renaut J, Komatsu S. Recent developments in the application of proteomics to the analysis of plant responses to heavy metals. Proteomics.

[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

[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

accumulation of chitinase isoforms in plants. Molecular Biology Reports.

*DOI: http://dx.doi.org/10.5772/intechopen.93787*

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[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

Botany. 2005;**56**:3149-3158

Behavior. 2010;**5**:233-238

2006;**57**:1025-1043

2007;**30**:1284-1298

[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

[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 &

[50] Munns R, James RA, Lauchli A. Approaches to increasing the salt tolerance of wheat and other cereals. Journal of Experimental Botany.

[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.

*HSPs under Abiotic Stresses DOI: http://dx.doi.org/10.5772/intechopen.93787*

*Abiotic Stress in Plants*

1997;**94**:1579-1584

[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.

to cold: Transcriptome analysis of wheat. Plant Biotechnology Journal.

[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.

[29] Xing W, Rajashekar CB. Glycine betaine involvement in freezing

*thaliana*. Environmental and Experimental Botany. 2001;**46**:21-28

[31] Ivanov AG, Morgan RM,

Temperature/light dependent

Photoinhibition of photosystem I in field-grown barley (*Hordeum vulgare* L.): Induction, recovery and acclimation. Photosynthesis Research.

[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.

[35] Bekesiova B, Hraska S, Libantova J,

Moravcikova J, Matusikova I.

2002;**14**:1675-1690

Letters. 1998;**430**:288-292

Gray GR, Velitchkova MY, Huner NP.

development of selective resistance to photoinhibition of photosystem I. FEBS

[32] Teicher HB, Moller BL, Scheller HV.

tolerance and water stress in *Arabidopsis* 

[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.

2010;**8**:749-771

1997;**126**:1-10

2004;**45**:103-108

2000;**64**:53-61

[20] Zinn KE, Tunc-Ozdemir M,

[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

Reviews. 2009;**61**:641-649

[26] Walther W, Stein U. Heatresponsive gene expression for gene therapy. Advanced Drug Delivery

[27] Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ. Plant responses

Botany. 2010;**61**:1959-1968

Harper JF. Temperature stress and plant sexual reproduction: Uncovering the weakest links. Journal of Experimental

**346**

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

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[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. Heatshock 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

**349**

*HSPs under Abiotic Stresses*

2008;**50**:1230-1237

2009;**20**:216-222

2001;**6**:219-224

*DOI: http://dx.doi.org/10.5772/intechopen.93787*

[70] Kalmar B, Greensmith L. Induction of heat shock proteins for protection against oxidative stress. Advanced Drug Delivery Reviews. 2009;**61**:310-318

of heat shock protein HSP101 gene family in wheat (*Triticum aestivum* (L.) Moench) inducible by heat,

[79] Schirmer EC, Lindquist S, Vierling E. An *Arabidopsis* heat shock protein complements a thermotolerance

defect in yeast. The Plant Cell.

[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.

[82] Queitsch C, Hong SW, Vierling E, Lindquist S. Heat shock protein 101 plays a crucial role in thermotolerance

in *Arabidopsis*. The Plant Cell.

[83] Singla SL, Pareek A, Grover A. Plant Hsp 100 family with special reference to rice. Journal of Biosciences.

[84] Wegele H, Muller L, Buchner J. Hsp70 and Hsp90--a relay team for protein folding. Reviews of Physiology, Biochemistry and Pharmacology.

[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.

1994;**6**:1899-1909

1999;**230**:187-195

2000;**12**:479-492

1998;**23**:337-345

2004;**151**:1-44

2001;**6**:238-246

dehydration, and ABA(1). Biochimica et Biophysica Acta. 2001;**1517**:270-277

[71] Huang B, Xu C. Identification and characterization of proteins associated with plant tolerance to heat stress. Journal of Integrative Plant Biology.

[72] Tower J. Hsps and aging. Trends in Endocrinology and Metabolism.

[73] Agarwal M, Katiyar-Agarwal S, Sahi C, Gallie DR, Grover A. *Arabidopsis* 

Pichersky E, Carrington M, Hobbs M, Mattick JS, et al. Conservation of the regulatory subunit for the Clp ATPdependent 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

[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-molecularweight (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

Biosciences. 2007;**32**:611-619

*thaliana* Hsp100 proteins: Kith and kin. Cell Stress & Chaperones.

[74] Gottesman S, Squires C,

*HSPs under Abiotic Stresses DOI: http://dx.doi.org/10.5772/intechopen.93787*

*Abiotic Stress in Plants*

[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

[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.

[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.

[65] Haq NU, Ammar M, Bano A, Luthe DS, Heckathorn SA, Shakeel SN.

*Chenopodium album* chloroplast small heat shock protein and its expression in response to different abiotic stresses. Plant Molecular Biology Reporter.

[66] Ritossa FM. A new puffing pattern induced by a temperature shock and DNP in *Drosophila*. Experientia.

[67] Ashburner M, Bonner JJ. The induction of gene activity in *Drosophila* by heat shock. Cell. 1979;**17**:241-254

[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

[68] Taylor RP, Benjamin IJ. Small heat shock proteins: A new classification scheme in mammals. Journal of Molecular and Cellular Cardiology.

Molecular characterization of

2002;**29**:933-944

2011;**49**:898-908

2013;**31**:1230-1241

1962;**18**:571-573

2005;**38**:433-444

[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

[56] Bray EA. Genes commonly regulated by water-deficit stress in *Arabidopsis thaliana*. Journal of Experimental Botany.

[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

interactions and environmental change. The New Phytologist. 2006;**171**:271-284

[60] Feder ME, Hofmann GE. Heatshock 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

[59] Brooker RW. Plant-plant

2004;**55**:2331-2341

[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

**348**

[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 ATPdependent 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-molecularweight (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

**351**

*HSPs under Abiotic Stresses*

*DOI: http://dx.doi.org/10.5772/intechopen.93787*

[112] Hamilton EW, Heckathorn SA. Mitochondrial adaptations to NaCl. Complex I is protected by anti-oxidants

[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**:

[115] Potenza C, Aleman L, Sengupta-Gopalan C. Targeting transgene

[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

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.

expression in research, agricultural, and environmental applications: Promoters used in plant transformation. In Vitro Cellular & Developmental Biology.

[117] Saidi Y, Domini M, Choy F, Zryd JP,

[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.

and small heat shock proteins, whereas complex II is protected by proline and betaine. Plant Physiology.

2001;**126**:1266-1274

117-122

Plant. 2004;**40**:1-22

2007;**30**:753-763

2004;**56**:795-809

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

[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

drought tolerance in *Gossypium hirsutum*. Biotechnology Progress.

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.

[108] Vierling E. The roles of heat shock proteins in plants. Annual Review of Plant Physiology and Plant Molecular

[109] Chen Q, Vierling E. Analysis of conserved domains identifies a unique structural feature of a chloroplast heat shock protein. Molecular & General

[110] Nakamoto H, Suzuki N, Roy SK. Constitutive expression of a small heat-shock protein confers cellular thermotolerance and thermal protection

[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

to the photosynthetic apparatus in cyanobacteria. FEBS Letters.

of America. 2001;**98**:3098-3103

2000;**483**:169-174

2010;**26**:21-25

2001;**88**:950-955

Biology. 1991;**42**:579-620

Genetics. 1991;**226**:425-431

*HSPs under Abiotic Stresses DOI: http://dx.doi.org/10.5772/intechopen.93787*

*Abiotic Stress in Plants*

1994;**35**:1207-1219

2001;**113**:443-451

2008;**34**:271-277

1999;**79**:425-449

[87] Yabe N, Takahashi T, Komeda Y. Analysis of tissue-specific expression of *Arabidopsis thaliana* HSP90-family gene HSP81. Plant & Cell Physiology.

proteins protect electron transport in chloroplasts and mitochondria during stress. American Zoologist.

[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.

[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

[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.

[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

Plant Journal. 1999;**20**:89-99

2007;**39**:818-831

1999;**39**:865-876

2007;**64**:294-306

[88] Sung DY, Kaplan F, Guy CL. Plant Hsp70 molecular chaperones: Protein structure, gene family, expression and function. Physiologia Plantarum.

[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.

[91] Fink AL. Chaperone-mediated protein folding. Physiological Reviews.

Evolution. 2004;**21**:498-505

[92] Nikolaidis N, Nei M. Concerted and nonconcerted evolution of the Hsp70 gene superfamily in two sibling species of nematodes. Molecular Biology and

[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.

[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.

[96] Heckathorn SA, Downs CA, Coleman JS. Small heat shock

2011;**39**:4889-4897

Microbiological Reviews. 1993;**57**:402-414

**350**

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 in *Gossypium 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

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**353**

**Chapter 17**

Stress

**Abstract**

stress resistance

**1. Introduction**

Plant Growth and

Morphophysiological

*Fuchun Xie, Rahul Datta and Dong Qin*

Modifications in Perennial

Ryegrass under Environmental

Perennial ryegrass (*Lolium perenne* L.) is a popular and important cool-season

turfgrass used in parks, landscapes, sports fields, and golf courses, and it has significant ecological, environmental, and economic values. It is also widely used as forage and pasture grass for animals around the world. However, the growth of perennial ryegrass is often affected by various abiotic stresses, which cause declines in turf quality and forage production. Among abiotic stresses, drought, salinity, temperature, and heavy metal are the most detrimental factors for perennial ryegrass growth in different regions, which result in growth inhibition, cell structure damage, and metabolic dysfunction. Many researches have revealed a lot useful information for understanding the mechanism of tolerance to adverse stresses at morphophysiological level. In this chapter, we will give a systematic literature review about morphological and physiological changes of perennial ryegrass in response to main stress factors and provide detail aspects of improving perennial ryegrass resistance based on research progress. Understanding morphophysiological response in perennial ryegrass under stress will contribute to improving further insights on fundamental mechanisms of perennial ryegrass stress tolerance and providing valuable information for breeding resistance cultivars of perennial ryegrass.

**Keywords:** perennial ryegrass, morphology, physiology, abiotic stress,

Urban green areas have important various functions contributing to the quality of human health. Well-kept lawns enhance the esthetic value of the entire city and are involved in phytoremediation, leading to an improvement in the quality of the air and soil [1–4]. Perennial ryegrass (*Lolium perenne* L.) is an important and widespread perennial cool-season grass cultivated in temperate climates, originating in Europe, temperate Asia, and North Africa [5]. Perennial ryegrass is commonly used in home lawns, sport fields, and parks with rapid growth and establishing rate, and other elements for ecosystem service due to its massive root system, superior regeneration,

#### **Chapter 17**

*Abiotic Stress in Plants*

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