Plant Heat Shock Proteins | Encyclopedia MDPI

Plant Heat Shock Proteins: History

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Subjects: Agriculture, Dairy & Animal Science

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Plant heat shock proteins (HSPs), as chaperones, play a pivotal role in conferring biotic and abiotic stress tolerance. Moreover, HSP also enhances membrane stability and detoxifies the reactive oxygen species (ROS) by positively regulating the antioxidant enzymes system.

heat shock factor
biotic stress
abiotic stress
protein folding
stress resistance

1. Introduction

Plants are sessile organisms and are subjected to various threats, both biotic and abiotic. These stresses, individually or in combination, result in huge losses in terms of growth, development, and yield and sometimes threaten the survival of the plant [1]. Plants continuously confront harsh environments like high/low temperatures, drought, salts, heavy metals, light, flooding and physical wounding [2,3,4,5]. Biotic stresses like pathogens (Viruses, Bacteria, Fungi) and pests such as nematodes, insects, and rodents also restrict plant productivity [6,7,8,9,10]. Negative effects of these stresses on the plant germination [11], are stunted growth [12,13], sunburn and scorching of leaves [14], loss of photosynthetic pigment, decreased production of photo-assimilates, and depletion of carbohydrate reserves which results in starvation [15,16,17,18]. Abiotic stresses also negatively affect the reproductive characteristics of plants by enhancing male sterility [19] and increasing premature flower and fruit drop [20] which results in significant low yield and quality. It has been reported that the increase in temperature by 1 °C results in a 4–10% yield decrease [21]. As a consequence of these stresses, reactive oxygen species (ROS) are produced which lead to oxidative stress and, ultimately, results in cell death. ROS could be singlet oxygen (¹O₂), superoxide radical (O₂^•−), hydrogen peroxide (H₂O₂) and hydroxyl radical (OH ⁻), which are produced in cell organelles such as mitochondria, peroxisomes and chloroplasts in oxidative stress situations and react with all types of macromolecules like pigments, proteins, lipids and DNA [22,23].

Plants respond morphologically to elevated temperature and light stress by changing the leaf orientation [13], anatomically by altering stomatal conductance and increased leaf pubescence [24,25], and phenologically by shifting and improvising the developmental stages to escape the abiotic stress condition [26]. Plants also change the metabolic processes and physiology to retain root hydraulic conductance [27], accumulation of the compatible osmolytes, such as sugars, sugar alcohols, proline and phenolic compounds under saline and water-logged conditions, as well as high temperature and water deficit conditions [28]. Moreover, plants manage to maintain photosynthetic machinery [29] by changing their assimilate partitioning a shift occurs from symplastic to apo-plastic [30]. During the onset of the stress situations, plants also improvise the hormonal balance of abscisic acid (ABA), ethylene, and salicylic acid (SA) as a signaling molecule in the systemic acquired resistance. Similarly, jasmonic acid (JA) and other steroids enhance stress tolerance and resistance [31]. Furthermore, secondary metabolites, such as isopropanioid, carotenoid, flavonoid, anthocyanin, lignin, and isoprenoids [30,32], also are produced and accumulated.

Besides these adaptations, plants also have sophisticated adaptive systems at the cellular and molecular levels. During the onset of stress, plants reduce the synthesis of normal protein production, and transcribe and translate heat shock proteins (HSPs). Added to transcriptional regulations, plants also have some sophisticated post-transcriptional modifications which help the plant to cope with these stresses, such as alternative splicing and micro RNA (miRNA). Alternative splicing, which generates multiple copies from a single gene, helps the plants to mitigate abiotic stresses [33]. One of the important plant post-transcriptional modification strategies is the miRNA, which binds to the mRNA at any point to repress translation or direct cleavage of the mRNA. Some of the miRNAs also are involved with abiotic stress tolerance [34].

2. Occurrence of HSP in Plants

The heat shock response is not unique in plants. It was first discovered in the early 1960s by an Italian scientist, F. Ritossa, in Drosophila melanogaster, while working on high-temperature stress [58,59]. HSPs were studied in Saccharomyces cerevisiae, by McAlister et al. (1980) [60], Escherichia coli, by Yamamori et al. (1982) [61], and plants (Glycine max), Lin et al. (1984) [62]. A comparison of the response in different organisms has shown that HSPs are conserved highly across organisms [63]. The evolutionary conservation of the heat shock response shows that the production of HSPs is a fundamental and essential process in all organisms [51].

Plants, due to their sessile nature, have evolved different efficient strategies to ensure their generations in the challenging competitive environment. The numbers of stress related genes, including HSPs, are greater in plants than other organisms due to whole genome duplication and gene retention in their evolutionary past [64]. Additionally, plants contain chloroplasts which have their own genome and de novo protein synthesis machinery [65]. A strategy of the plant to cope with stressful situations (Figure 1), is the synthesis of normal protein reduced while the synthesis of stress-related proteins i.e., HSPs, is enhanced.

Figure 1. Exposures of plants to different biotic and abiotic stresses, adverse effects of these stresses on plants and response mechanisms of plants to these stresses.

Many HSPs have been reported in a wide range of organisms from prokaryotes to eukaryotes [63,66]. These HSPs across the organisms are conserved highly, with little difference except for HSP33, which differs in plants from that in bacteria [67]. The genes which encode different HSPs are found in different cell compartments, such as the nucleus, mitochondria, chloroplast, endoplasmic reticulum and cytosol [68]. Similarly, the accumulation of these HSPs in different parts of the cell also depends on the intensity of the stress. Nuclear HSPs, for instance, are accumulating in the cytosol at the lower and higher temperatures of 27 °C and 43 °C, respectively, while the same aggregate in chloroplast is at 37 °C [47]. Different HSPs are found and differentially expressed in different species, even in different genotypes but in the same species, as investigated by Korotaeva et al., (2001) and Nieto-Sotelo et al., (2002) [69,70] in small HSPs where five sHSPs showed response to a higher temperature (42 °C) in maize but only one expressed in wheat and rice. Likewise, HSP68 expressed in mitochondria under stress situations in potatoes, tomatoes, and soybeans [71]. Some HSPs showed a tissue-specific response to stress situations; HSP101 was expressed more in reproductive parts like tassels, ear, and endosperm, than in vegetative parts like leaves and roots in maize [72]. Some HSPs responded differently to the varying length of stresses. As Heckathorn et al., (1989) [73] reported, in HSP45, a nuclear protein accumulated in the chloroplast at a 3 h exposure to heat stress, which returned to its native state after removal of stress. Similarly, HSPs triggered differently with different development stages. HSP45, for example, showed a response in the whole plant to a stress situation, while HSP64 and -72 only showed expression in the reproductive parts i.e., pollens [74,75]. It can be deduced that these are the key regulators which show different responses to varying levels of stress in different parts of the plants.

3. Role of HSPs in Plant Defense

Plants are subjected to various biotic and abiotic stresses, singly or in combination, which adversely affect plant growth, development, and survival [86]. To cope with these stresses, plants have evolved various defense strategies i.e., physical [13], anatomical [25], and physiological [27,87]. Plants also respond to stress situations at the molecular level by altering gene expression, synthesis of stress-related biomolecules and proteins including heat stress proteins, to enable plants to ensure their generation in challenging situations.

3.1. Biotic Stress Tolerance

Plant growth, development, yield, and quality are affected adversely by several biotic factors such as pathogenic bacteria, fungi, viruses, and nematodes. Biotic factors, directly deprive their host plants of their nutrients, which result in reduced plant vigor, growth, productivity and sometimes leads to death of the host plants. Biotic stresses are major cause of pre- and post-harvest losses. Animals have an immune system, which helps them to adapt to biotic stresses such as new diseases and memorized the past infections, while plants lack such a system. Although plants lack this adaptive immune system, they have evolved several sophisticated strategies to counteract these biotic stresses [88]. These defense mechanisms are stored in the plant’s genome at the genetic level, which encode thousands of stress resistance genes. One of the adaptive systems plants employ in response to biotic stress is through regulation of HSPs (Table 2). HSP response to biotic stresses depend on the nature of the causal organisms and plant genotypes, either susceptible or resistant, and the developmental stage [6].

Table 2. Summary of the role of plant HSP under biotic stresses.

Biotic Factor	Plant	Pathogen	Disease Caused	HSP Response	Expression Pattern	Reference
Viruses	Arabidopsis thaliana	TVCTV, ORTV, PVX, CMV, and TuMV	Penstemon disease, red spots on leaves, deformed leaves and stunted growth	HSP17.6 HSP17.4	Up/down	[110]
	Solanum lycopersicum	TYLCV	Stunted and bushy growth and excessive branches, abnormal leaf shapes, curled inward or upward, and flower and fruit drops	HSP70 HSP90	Up/down	[109,110,111]
	Nicotiana benthamina	CNV, RCNMV, and TMV	Mosaic and discoloration on leaves of a wide-range of the host plant	HSP70 HSP90	Up	[108,112,113]
	Solanum tuberosum	SYNV and INSV	Yellow and black rings, spots and lesions on leaves, and leads to plant death	HSP18 HSP20	Up	[114]
	Oryza sativa	RSV and RBSDV	Dark green rigid leaves, white- and sometimes black-streaked strips along the leaves, veins and stem	HSP20 HSP70	Up	[7,115,116]
	Solanum tuberosum	PVY	Potato tuber necrotic rings, spots, disease and decay	HSP	Up	[117]
Bacteria	Nicotiana benthamina	Ralstonia solanacearum	Wide- range of the host, it enters the xylem of a plant and causes wilting	HSP17	Up	[103]
	Nicotiana benthamina	Ralstonia solani	Bacterial wilt by blockade of conducting vessels	HSP90	Up	[107]
	Citrus spp	Xanthomonas axonopodis pv. citri	This bacterium causes the citrus canker and spots on leaves and blemishes on fruits.	Hsp15.5	Up	[104]
	Capsicum annuum	Xanthomonas campestris pv. Vesicatoria	Causes leaf and fruit spots on peppers and tomatoes.	Hsp16 HSP20	Up	[104]
	Arabidopsis thaliana	Pseudomonas syringae	Round to irregular brown spots. These spots enlarge and blight the whole leaves.	HSP17 HSP21 HSP23	Down	[105,106]
Fungi	Oryza sativa	Magnaporthe grisea	Causes destructive disease of rice, rice blast, rice seedling blight and pitting disease.	HSP16 HSP17.4 HSP18	Up	[92]
	Solanum lycopersicum	Fusarium oxysporum	Wilting, characterized by clearing of veins, marginal necrosis, yellowing of lower leaves, adventitious roots and ultimate death of tomato plants.	HSP20	Up	[93]
		Rhizopus nigricans Ehrenb.	Rhizopus soft rot first appears as water-soaked areas, which then become sunken and gray mold and dusky black spores grow on the fruit surface of tomatoes.	HSP17.6	Up	[94]
		Oidium neolycopersici	Fungus that causes white powdery lesions and powdery mildew on tomatoes	HSP72 HSP75	Up	[99]
	Arabidopsis thaliana	Rhizoctonia solani	Fungus which causes collar rot, root rot and damping off	HSP17.4 HSP17.6	Up	[86,87]
	Malus domestica	Venturia inaequalis	Fungus causes scab disease on apples and pears	HSP21	Down	[98]
	Solanum tuberosum	Phytophthora infestans	Fungus causes late blight of potatoes	HSP17.8 HSP70	Up Up	[100] [101]
	Hordeum vulgare	Blumeria graminis f. sp. hordei	Fungus causes powdery mildew on grasses and cereals like barley.	Hsp16.9 Hsp17.5.	Up	[118]
Nematodes	Gossypium hirsutum	Roylenchulus reniformis	Stunted growth, root necrosis and the plant shows symptoms similar to nutrient and water deficiency	54 HSP	Up	[7]
	Glycine max	Meloidogyne javanica	Root knot on tropical crops, it is causes irregular galls and swollen roots	HSP22.4 HSP17.9 HSP17.9 HSP22.4	Up	[119,120]
	Glycine max	Heterodera glycines	Forms cysts on the roots of soybeans. It causes chlorosis of leaves and stem and root necrosis	HSP20	Up	[121]
	Helianthus annuus	Meloidogyne incognita	Irregular galls on the root of sunflowers	HSP17.6 HSP17.7 HSP18.6	Up	[122,123]
	Solanum lycopersicum	Meloidogyne spp.	Knots and galls on the roots of tomatoes, swollen roots and dwarf stem	HSP90	Up	[124]
	Nicotiana benthamina	Meloidogyne incognita	Root knot and galls on tobacco roots and causes wilting of leaves	HSP90	Up	[125]

Turnip vein clearing virus (TVCTV), Oilseed rape virus (ORTV), Potato virus X (PVX), Cucumber mosaic virus (CMV), Turnip mosaic virus (TuMV), Tomato yellow leaf curl virus (TYLCV), Cucumber Necrosis Virus (CNV), Red clover necrotic mosaic virus (RCNMV), Tobacco mosaic virus (TMV), Sonchus yellow net virus (SYNV), Impatiens necrotic spot virus (INSV), Rice stripe virus (RSV), Rice black Streaked dwarf Virus (RBSDV), Potato virus Y (PVY).

.2. Abiotic Stress Tolerance

Abiotic stresses are extreme environmental conditions like extreme temperatures, water deficit, and ion imbalance due to heavy metals and salinity, which pose a serious threat to plants survival, yield and quality. Global warming and climate change, due to industrialization, has further worsened the situation. Greenhouse gases, particularly the concentration of CO₂, is increasing constantly in the atmosphere, which is estimated to reach 520 ppm from 410 by the year 2100 [36]. Twenty per cent of the world cultivated land and almost 50% of irrigated land is affected by salinity, and yield loss up to 50% due to drought is projected by the year 2050 [128]. The world population by the year 2050 is approximated to be 9 billion [129], so, in such a situation, biotic and abiotic stress-tolerant cultivars need to be developed using transgenic and omic techniques. The role of HSPs has been studied by various scientists under different abiotic stresses (Table 3).

Table 3. Summary of studies of plant HSP and abiotic stresses.

Abiotic Factors	Plant	Type of HSP	Expression Pattern	Technique Used	Reference
High temperature stress	Wheat	HSP70	up	qRT-PCR	[158]
	Wheat	HSP26	up	qRT-PCR	[183]
	Rice	HSP100	up	WB	[134]
	Rice	HSP90	up	q-PCR	[145,146,184]
	Maize	HSP101	up	SDS-PAGE	[63,65]
	Maize	HSP70, HSP17.6	up	SDS-PAGE	[139]
	Arabidopsis	HSP101	up	qRT-PCR	[127,128,129,130]
		HSP100	up	SDS-PAGE	[65]
		HSP90	up	qRT-PCR, WB	[147,185]
		HSP70	up	qRT-PCR	[186]
		HSP60 HSP70	up	qRT-PCR	[148]
	Potato	HSP70	up	qRT-PCR	[156]
	Tomato	HSP70	up	SDS-PAGE, WB	[140]
	Tomato	HSP20	up/down	qRT-PCR	[187]
	Pea	HSP17.9 HSP18.1	up	qRT-PCR	[188]
	Pea	HSP70	up	qRT-PCR	[154]
	Pepper	HSP70	up/down	qRT-PCR	[151]
		HSP70	up	qRT-PCR	[153]
		HSP60	up	qRT-PCR	[189]
		HSP20	up/down	qRT-PCR	[78]
		HSP16.4	up	qRT-PCR	[152]
	Soybean	HSP90	up	qRT-PCR	[146]
	Cabbage	HSP70	up	qRT-PCR	[155]
	Tea	All HSPs	up	qRT-PCR	[159]
	Witch grass	HSP70	up	MA, qRT-PCR	[149]
	Alfalfa	HSP70	up	qRT-PCR	[150]
	Foxtail millet	HSP20	down	qRT-PCR	[53]
	Chrysanthemum	HSP70	up	MS, qRT-PCR	[157]
Low temperature stress	Arabidopsis	HSP70	up	MS, qRT-PCR	[169]
	Tobacco	HSP70	up	MS, qRT-PCR	[161,165]
	Maize	HSP70	up	MA, qRT-PCR	[171]
	Wheat	HSP70	up	MS	[190]
		HSP90	up	MS	[175]
		HSP60 HSP21	down	MS, qRT-PCR	[167]
	Rice	HSP75 HSP95	up	MS, qRT-PCR	[180]
	Rice	HSP90	up	MS	[191]
	Barley	HSP70	up	MS	[167]
	Chicory	All HSPs	up	MS	[173]
	Rape seed	HSP90	up	qRT-PCR	[172]
	Poplar	HSP70 HSP90	up	MS	[178]
	Pea	HSP70	up	MS	[177]
	Sunflower	HSP60 HSP21	down	MS, qRT-PCR	[181]
	Tomato	HSP110 HSP70	up	qRT-PCR	[192]
	Plum	HSP20	up	qRT-PCR	[193]
	Grape	HSP18 HSP22	up	qRT-PCR	[194]
Salinity stress	Wheat	HSP70	up	MS	[195]
	Wheat	All HSPs	up		[196]
	Rice	HSP70	up	qRT-PCR	[197,198]
		HSP40	up	qRT-PCR	[165]
		ClpD1	up	qRT-PCR	[199]
	Arabidopsis	HSP90.2 HSP90.5 HSP90.7	up	qRT-PCR	[200] [146]
	Rose	17.8	up	qRT-PCR	[16]
	Soybean	HSP90 HSP70 HSP60 HSP20	up/down	MS	[201] [202]
	Poplar	HSP100 HSP90 HSP70 HSP60 HSP40 HSP20	up	qRT-PCR	[203]
Drought stress	Arabidopsis	HSP70	up	qRT-PCR	[204]
	Tobacco	HSP70 BiPs	up	qRT-PCR	[205] [176]
	Barley	HSP17.5	up	qRT-PCR	[206]
	Rice	HSP70	up	MA, MS, qRT-PCR	[207]
		HSP101	up	MS	[208]
		HSP17.7	up	qRT-PCR	[209]
	Maize	HSP70 HSP26	up	MS	[39]
	Pepper	HSP16.4	up	qRT-PCR	[152]
	Chickpea	HSP70	up	MS, qRT-PCR	[210]
	Sugarcane	HSP70	up	qRT-PCR	[211]
	Cotton	All HSPs	up	qRT-PCR, WB	[212]
	Kentucky grass	HSP70	up	MS	[160]
	Poplar	HSP70	up	MS	[213]
Light stress	Arabidopsis	HSP70	up	qRT-PCR	[214,215]
	Goose foot plant	HSP23	up	SDS-PAGE	[69]
	Chlamydomonas	HSP70	up	MA	[216]
Heavy metal stress	Tomato	HSP70	up	MS, SDS-PAGE	[217]
	Rice	HSP70 BiPs	up	MS, SDS-PAGE	[218]
	Rice	HSP80 HSP17.9	up	MA	[219]
	Poplar	HSP70	up	qRT-PCR	[212]
	Soybean	HSP26	up	qRT-PCR	[220]
	Carrot	HSP17.7	up	qRT-PCR	[221]
	Flaxseed	HSP70	up	MA, MS	[168]
	Flaxseed	HSP80	down	MA, MS	[168]
	Arabidopsis	HSP70	up	qRT-PCR, NB, MS	[222]
	Bird foot trefoil	HSP90	up	qRT-PCR	[223]
Flooding stress	Arabidopsis	HSP101 HSP70	up	qRT-PCR	[224]
	Tomato	HSP23.6	up	qRT-PCR	[225]
	Rice	HSP70	up	qRT-PCR	[226]
	Maize	HSP70	up	qRT-PCR, WB	[227]
	Soybean	HSP70	up	qRT-PCR, SDS-PAGE	[228]
	Soybean	HSP60	up	MS	[229]

Quantitative real-time polymerase chain reaction (qRT-PCR), Mass spectrometry (MS), Microarray (MA), Western blotting (WB), Northern blotting (NB), Sodium dodecyl sulfate–polyacrylamide gel electrophoresis (SDS-PAGE).

This entry is adapted from the peer-reviewed paper 10.3390/ijms20215321

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