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",isbn:"978-1-83969-657-2",printIsbn:"978-1-83969-656-5",pdfIsbn:"978-1-83969-658-9",doi:null,price:0,priceEur:0,priceUsd:0,slug:null,numberOfPages:0,isOpenForSubmission:!0,hash:"eb6769bb88a11d0d7d681449b7e14e4a",bookSignature:"Dr. Barun Shankar Gupta",publishedDate:null,coverURL:"https://cdn.intechopen.com/books/images_new/10667.jpg",keywords:"Stoichiometry, Topology, Assembly, Entropy, Lattice Structure, Micro-Alloy, Phase Diagram, Time-Temperature-Transformation (TTT), Dispersion, Solubility and Diffusion, Interface Interactions, Ductility and Rigidity",numberOfDownloads:null,numberOfWosCitations:0,numberOfCrossrefCitations:null,numberOfDimensionsCitations:null,numberOfTotalCitations:null,isAvailableForWebshopOrdering:!0,dateEndFirstStepPublish:"March 8th 2021",dateEndSecondStepPublish:"April 5th 2021",dateEndThirdStepPublish:"June 4th 2021",dateEndFourthStepPublish:"August 23rd 2021",dateEndFifthStepPublish:"October 22nd 2021",remainingDaysToSecondStep:"11 days",secondStepPassed:!0,currentStepOfPublishingProcess:3,editedByType:null,kuFlag:!1,biosketch:"A well-known researcher in the field of surface properties investigation of polymers and composites, reviewer of several international journals on materials, member of professional bodies, and author of books.",coeditorOneBiosketch:null,coeditorTwoBiosketch:null,coeditorThreeBiosketch:null,coeditorFourBiosketch:null,coeditorFiveBiosketch:null,editors:[{id:"343769",title:"Dr.",name:"Barun Shankar",middleName:null,surname:"Gupta",slug:"barun-shankar-gupta",fullName:"Barun Shankar Gupta",profilePictureURL:"https://mts.intechopen.com/storage/users/343769/images/system/343769.jpg",biography:"Dr. Barun Shankar Gupta completed his Ph.D. from the Department of Civil & Transport Engineering, Norwegian University of Science and Technology (NTNU), Norway. Before his doctorate, he has worked as a researcher at the universities in U.S.A., France and Canada. As a technologist, he worked at the Paharpur Cooling Towers Ltd. India, which is worlds' leading process cooling equipment manufacturer. He owns a patent, a member of several scientific communities, editor of international journal, has written and presented more than twenty research articles, book, and is serving as reviewer to several international journals. 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Capsicum plants are topics crops that better grow in hotter zones [1]. They are eaten fresh, dehydrated and processed, and also as a spice. Given its vast versatility, peppers are being increasingly eaten, but also due to the fact that they are a major source of pro-vitamin A (carotene), E (α-tocopherol), and one of its main attributes is vitamin C (ascorbic acid). Mature pepper fruits are rich in carotenoids, compounds with anti-carcinogenic and antioxidant ability. Mature and immature fruits contain high contents of phenolics, especially flavonoids for which there are reports of antioxidant and other bioactive properties [2, 3, 4], and plenty of essential nutrients.
According to their culinary purposes and organoleptic features, pepper fruits are normally classified as two kinds. One is a bell pepper, which means a non-pungent, chunky sweet pepper kind, whereas chilli pepper refers to pungent chilli fruits [1]. Generally speaking, non-pungent peppers are more popular in the northern hemisphere, but more pungent chilli peppers are eaten more in tropic and subtropic areas [5].
Peppers grow in most countries on our planet, and they cover 1.93 million ha of crop-growing surface area. As a spice and vegetables, the world’s pepper production has gone from over 12 million tons in 1993 to more than 31 million in 2013 over the past 20 years [6]. China is the largest pepper producer (almost 16 million tons) and is followed by Mexico (2.3 million), Turkey (2.2 million), and Indonesia (1.8 million) (Figure 1).
World production of chillies and peppers by country (million tons) [
Peppers have adapted well to hot climates. The optimum seed germination temperature is 25–30°C. For fruit quality and growth purposes, areas with temperatures within the 21–29°C range are needed [7]. When temperature goes under 15°C or exceeds 32°C, growth can be retarded, and blossom end rot (BER), fruit-set ceases may emerge, with lower yields [8]. Generally speaking, commercial pepper varieties need friable, well-drained, sandy loam soil with pH of 6.5–7.5 for optimum production. Salt content in soil and irrigation water should be low. There are reports of a salinity resistance threshold of 1.5 dS m−1, below which no effect on growth occurs, and a 14% drop in biomass production per additional 1 dS m−1 has been found [9]. Thresholds ranging from 0 to 2 dS m−1, and slopes of salinity response curves that go from 8 to 15%, have been indicated for greenhouse peppers [10, 11]. Added organic matter increases the water-holding capacity and supplies minerals and nutrients. Peppers need high frequent soil fertility at the start of the growing cycle to supplement N. If water is lacking or excessive, flower abortion or further BER of fruits can be induced [12].
The Solanaceae family is a complex that comprises at least 98 genera and as many as 2716 species, including Capsicum [13, 14]. This family also includes other major crop types, like potato, eggplant, tomato, and tobacco. “Capsicum” comes from a Greek-based derivate of the Latin “Kapto,” which means “to bite,” and refers to heat (pungency). Capsaicin, which is a volatile molecule, is also a very stable molecule that is responsible for the pungency normally linked with certain peppers [15]. Other pepper species are non-pungent because of a single mutation, which leads to the inability to generate capsaicinoids.
The genus Capsicum has been found in the central hemisphere and in South America ever since civilization began. It is likely to have evolved from an ancestral form in Bolivia-Peru. It formed part of human diet at approximately 7500 BC [16]. Peppers were completely unknown in Europe, Africa, and Asia before Columbus landed in the Americas. During his voyage, he came across a plant with fruit that resembled the pungency of black pepper,
In the face of climate change, global food security demands increasing agricultural production on finite arable land that does not increase water use [23]. As the world’s population is estimated to increase to about 9 billion by 2050, the World Food Summit on Food Security (2009) has set a target of a 70% global food production increase. Environmental stresses are the most limiting conditions for plant exploitation and horticultural productivity worldwide [24, 25]. The most limiting factors include temperature, water availability, light, salinity, pathogens, and metal ion concentrations. Many disorders and diseases can interfere with pepper production and its quality, which can be of biotic (living) and abiotic (non-living) origin.
Capsicum plants can be attacked by distinct pathogens. The most troublesome and important pests and diseases are: fungal diseases, like
(A) overview of a pepper field infected by
Biotic stresses can bring about physiological changes in pepper plants, e.g., ion-flux change, electrolyte leakage, activation of defensive responses, and hypersensitive cell death [26]. These effects can result in smaller yields and worse quality. One of the most hazardous biotic factors is soil diseases, especially for intensive farming, where soil-borne pathogens can build up if crop rotations are limited. The main injuries to roots of these soil pathogens include smaller foliar size, thin weak stems, wilting, depressed flowering, worse fruit quality, and shorter plant life spans [27]. Initial symptoms are quite visible on leaves when plant roots have been completely infected. Farmer’s only feasible option is taking preventive measures, which involve soil treatments for the next crop season. As soil fumigation with methyl bromide (MB) is forbidden, other alternatives need to be taken [28]. Fumigants are an option, but vast amounts can be applied that might result in phytotoxicity [29, 30]. Furthermore, the long-term use of fumigants may lead to changes in the microfauna of soil, which not always favors cultivated plants [31]. Steam treatment is not toxic and effectively kills pathogens, but is not an economically feasible option everywhere as it requires suitable steaming machinery, and also fuel and water [32]. Soil solarization is used frequently in countries with a warm climate [33], but soil must be covered for 4–6 weeks with hot periods to stop vegetable production. Another alternative is biological control, which involves selecting organisms based on their ability to control diseases, which can be used for aerial plagues.
Another possibility is plant biotic resistance. To enhance crop tolerance, many attempts have been made by traditional breeding programs. Although commercial success is limited given trait complexity, commercial cultivars with some tolerance are found. In the present-day, vast efforts have been made to genetically transform plants to improve their tolerance. Although some increased tolerance to pathogens has been reported in transgenic peppers [34, 35] other approaches to achieve resistance must be currently considered as genetic engineering means in plants has been poorly accepted by the public [36].
One way to reduce or avoid lost production is to graft sensitive plants onto robust rootstocks. Several
During the growth cycle of peppers, as with other plants, many unfavorable environmental conditions can occur, such as salinity, drought, extreme temperatures, moisture, light, mineral deficiencies or toxicities, pH, and pollutants, which can all diminish plant yields [21, 40, 41]. Close to 82% of the potential crop yields is lost yearly from abiotic stress, and the quantity of available productive arable lands continues to drop worldwide, which forces farmers and farms to move to places with a higher abiotic stress potential [42].
In the Mediterranean Region, one of the most important abiotic stresses is salinity, which is usually present in both soil and water, as well water scarcity, but improving these environmental conditions through crop management is very difficult.
Some other abiotic stresses include: low temperature because it affects pepper vegetative development and reproduction as it disturbs how flower female organs function, and the amount of viable pollen grains per flower [43, 44]; high temperature and radiation promote stunted growth, a lower photosynthetic rate, increased respiration, and poor water and ion uptake [24, 26]. Therefore, using different shading screens is considered an alternative to overcome these problems [45, 46]. Likewise, heating is used to avoid chilling and frost injury, and cooling is employed to avoid high air temperatures [21].
Water scarcity is believed to be a major threat for the twenty-first century (UNESCO, 2012). During their life cycles, plants are subjected to periods of soil and atmospheric water deficit. Indeed, about only 15% of agricultural land is irrigated worldwide, but irrigated lands make up nearly 50% of the world’s food production [47]. Drought, along with salinity, is one of the most important causes of low yields worldwide [48]. Adapted cultivars can improve the synchronization between crop water demand and soil supply. For all these reasons, we need to know plant responses to water scarcity, which are complex, and involve deleterious and/or adaptive changes [49].
As soil dries, its matric potential becomes more negative [50]. Plants can continue to absorb water only as long as their water potential (Ψw) is lower (more negative) than that of soil. The water potential is the total of both the solute potential (Ψs) and the turgor potential (Ψp): thus: Ψw = Ψs + Ψp [51]. In this way, one of the important pathways to enhance water stress tolerance is through osmotic adjustment, which maintains the leaf turgor required for stomatal opening, and to hence sustain photosynthesis and growth [52, 53]. Plants accumulate various types of compatible solutes, such as sugars, proline, glycinebetaine, or potassium [53, 54] to lower the osmotic potential and to absorb water. Basically, cells’ accumulation of solutes is a process by which the water potential can lower without being linked to an accompanying reduction in turgor or a reduced cell volume.
Stomatal closure and reduced transpiration rates are prompt responses under drought stress because they lower the water potential of plant tissues. As a result, photosynthesis lowers, mediated by diminished CO2 availability that is caused by: (a) diffusion limitations via the mesophyll and/or stomata [55], known as stomatal effects; (b) altered CO2 fixation reactions, mediated by reduced Rubisco activity, known as non-stomatal [56]. With water stress, as energy accumulates in plants, which consume less light energy through photosynthetic carbon fixation, reactive oxygen species (ROS) generation increases [57, 58]. Accumulation of sorbitol, mannitol, and proline, and the formation of radical scavenging compounds, e.g., ascorbate, glutathione, and α-tocopherol, can help plants to cope with water stress [59]. Such compounds play a dual role as the non-enzymatic antioxidants needed by plants to counteract the inhibitory metabolic effects of the ROS generated under water stress [60], and also in stabilizing proteins and enzymes, and in protecting membrane integrity [61]. Besides these physiological responses, plants also undergo morphological changes [62], like stunted growth and, consequently, smaller yields.
Generally, pepper plants are sensitive to water deficit due to big leaf areas and higher stomata conductance [63, 64, 65]. In the pepper production industry, drought imposes huge reductions in crop yields and quality, with significant economic losses of up to 70% [64, 66, 67]. The two most critical moisture stress stages in peppers are the initial establishment of transplanted plants and the stage prior to blossoming [17]. Thus, reduced yields and smaller fruits are frequently recorded under moisture stress conditions. Moreover, this scenario limits the water applied to peppers during rapid growth periods to reduce final yields [68].
Salinity can be disastrous because it can have many direct and indirect harmful effects. It inhibits seed germination, induces physiological dysfunctions and often kills non halophyte plants, even at low concentrations, and also limits agricultural development [69, 70]. Salinization transforms fertile and productive land into barren land, and often leads to habitat and biodiversity loss [71]. Salt accumulating in excessive amounts in cultivated soils is a common problem, especially under irrigated conditions, which threatens food production globally [72, 73]. The indiscriminate use of large quantities of chemical fertilizers and overexploitation of aquifers have dramatically multiplied the surface area affected by salinity [27]. Today to a greater or lesser extent, a third of all irrigated lands worldwide is affected by salinity [74], which means smaller yields.
Salt stress has two components that negatively affect plant growth: osmotic component and ionic component. A high salt concentration lowers the water potential in soil, and results in water stress in plants, known as the osmotic salinity component. The accumulation of given toxic ions represents the ionic component [75].
The relative degree of each salt effect caused by different salinity levels and its consequences on crop production are not clearly understood [67]. Saline soils induced by protected culture are complex and can include high concentrations of K+, Na+, Ca2+, Mg2+, SO42−, NO3−, and Cl−, which differ from the saline soils induced by seawater, in which NaCl is the most soluble and widespread salt [52, 76]. High Na+ concentrations lower Ca2+ and K+ uptakes, which leads to reduced stomatal conductance that results in lower CO2 concentrations and, consequently, lower photosynthesis. High Cl− concentrations cause chlorophyll degradation and reduce actual quantum yields of PSII electron transport [77].
Salinity causes membrane destabilization [78], nutrient imbalances [79] and irreversible harm to plant tissues and cells [80]. It is well-accepted that growth inhibition by salt stress is linked with alterations to the hydric relationships in plants as a result of osmotic effects with certain ionic consequences.
Salt tolerance mechanisms include: (i) salt exclusion: plants limit salt accumulation in tissues by inhibiting root uptake. Some salt transport restriction strategies to sensitive tissues or organs have also evolved [81]. Plants’ ability to regulate the transport and uptake of salts depends on these mechanisms: root cells’ selectivity of uptake; preferential loading of K+ instead of Na+ onto the xylem by stele cells; salts removed from the xylem in upper root parts, leaf sheaths, and the stem according to the exchange of both K+ and Na+; (ii) salt excretion: halophytes often have anatomical structures, like salt bladders and salt glands, that are designed to eliminate any excess salt ions from plants to their environment; and (iii) intracellular ion compartmentation. The sequestration of ions or salts into leaf and/or shoot vacuoles is typically attributed to dicotyledonous halophytes. Such accumulation depends on tonoplast Na+/H+ antiporters and vacuolar H+-translocating transporters that are induced by saline environments [82]. One immediate salt stress effect is cell alkalinization, which is linked with the Na+/H+ antiporters activity of tonoplast vesicles [78]. Here different types of compatible organic solutes and potassium ions, like proline and soluble sugar, accumulate in the cytoplasm to avoid dehydration and to maintain the osmotic-ionic balance between both two compartments [83], and to also stabilize subcellular structures, e.g., proteins and membranes [52, 84]. It has been observed in tolerant salt plants after the initial loss of cellular turgor that plants are able to induce an osmotic adjustment to the lower external water potential by compartmentalizing toxic ions in the vacuole and then synthesizing compatible solutes in the cytoplasm [78].
Pepper, and
Blossom end rot (BER) is a serious disorder known to affect peppers that grow under different environmental stresses. BER symptoms are linked with membrane leakage of cell solutes, cell plasmolysis, and membrane breakdown [88, 89, 90]. Thus fruit surfaces display water-soaked symptoms, and the tissue at the distal fruit portion ends up becoming discolored and necrotic. BER causes premature ripening and enhances fruit softening, which result in small-sized fruits [91] (Figure 3). In internal fruit tissues, BER develops in the necrotic region of the parenchymal tissue surrounding young seeds, and also in the distal placenta [89]. It is predominantly viewed that the cause of BER is inadequate calcium translocation to the fruit tip for rapid fruit expansion, which takes place under conditions that favor rapid fruit growth, e.g., bright light and high temperature. Hence, cell integrity is impaired with consequent tissue disintegration [92]. Since Ca2+ is thought to play a key role, BER is termed a “calcium-related disorder” [93]. BER incidence is related to environmental factors, like high salinity, water scarcity, high temperature, and ammonia nutrition, which contribute to Ca2+ deficiency [91, 94, 95]. However, a close relationship between calcium levels and BER cannot always be demonstrated [90]. Lantos [96] has shown that applying calcium does not necessarily reduce the yield losses caused by calcium deficiency.
Overview of the pepper fruits affected by BER (right) and details of necrotic tissue (left).
The influence of stress on BER which occurs in peppers is partly based on not only increased NAD(P)H oxidase (an oxygen radicals-generating enzyme) activity, but also on higher ROS production, e.g., superoxide radicals, hydroxyl radicals, and singlet oxygen (O2) in fruit apoplasts [91, 92, 97]. ROS are known to trigger cell death, which is characterized by the progressive loss of membrane integrity to result in cytoplasm swelling, and also in the release of cellular constituents [98], including loss of Ca2+ ions, which may explain the lower Ca2+ concentrations found mainly in the apoplast [88]. A certain amount of stress, caused by either a single or an interaction of several environmental factors, like high relative humidity, pathogenic stem diseases, and dry or saline soils, may have a negative effect on calcium uptake [99], which does not always end in a corresponding degree of BER [90].
Two phytohormone types appear to especially interfere with BER affection, and also in opposite directions: abscisic acid (ABA) and bioactive gibberellins (GAs). The antagonism action between vegetative growth and Ca2+ has been reported by Lyon et al. [100]. Low Ca2+ in the nutrient medium has been indicated to result in very extensive root systems, which suggests great GA activity. Accordingly, a low Ca2+ supply might have caused the high BER incidence more indirectly through enhanced GA activity [88]. ABA, as an antagonist to GAs, is known for reducing plant susceptibility to stress; e.g., by promoting Ca2+ transport to fruits. Applying ABA to highly stressed tomato plants has been recently demonstrated to alleviate BER symptoms [101].
From a practical point of view, GA-signaling can be reduced by, for example, root restriction [102], by applying growth-retarding chemicals, and also by ABA [103, 104].
Basically, BER development involves several steps: stress enhances ROS production; ROS leads to lipid peroxidation with greater membrane leakiness which, in turn, leads to the rapid vacuolation of parenchyma cells and to loss of ions, which includes water-soluble apoplastic Ca2+. This situation is also aggravated when plants are grown vigorously, when GAs levels are high and when ABA is low. All these are typical BER symptoms [94]. Thus final Ca2+ deficiency can be considered a result, but not the cause, of only BER.
To control BER solutions, reducing susceptibility to stress and alleviating stress severity are necessary by: (i) proper selection of suited production sites. However, this is not always possible, and environmental conditions are unpredictable; (ii) improving management practices, e.g., shade or applying calcium fruit sprays. However, not enough evidence is available to recommend their use to manage BER; or spraying ABA, which remains unavailable as a commercial solution (no commercial formulation and side effects); (iii) breeding and selecting stress-resistant cultivars. Sadly, programs are slow and obtaining a variety that collects commercial fruit attributes and a robust radicular system is difficult; (iv) robust rootstocks inducing higher production in horticultural crops, which leads to a larger leaf area in grafted tomato plants [105], maintains a greater net CO2 assimilation in grafted cucumber plants [106, 107], and has also shown a vigorous root system that increases the absorption of water and minerals in pepper-grafted plants [108]. Thus, grafting susceptible plants onto robust rootstocks to reduce their susceptibility to stress can reduce the fruits affected by BER, maintain water uptake, contribute to better plant nutrition; consequently, calcium deficiency can diminish [109, 110, 111].
Fruit cracking is yet another frequent physiological disorder that lowers marketable fruit yields, but it is not such a serious commercial problem as BER. The cracks in cracked fruits normally spread through the wall into the locule area because of repeated shrinkage. Such expansion weakens fruit cuticles [112]. Incidence is affected by environmental factors, mainly by varietal characteristics [113]. Several studies have demonstrated the importance of the environment in cuticle cracking development, like low night vapor pressure deficit [114], relative humidity [115], and temperature [116]. Fruits that display a wider expansion-shrinkage amplitude are often associated with severe cracking symptoms. The water status of fruits is a key factor to establish fruit cracking severity [21]. Some solutions can include those that minimize changes in their water status. Indeed, the same strategies used to combat BER can be adopted. Nonetheless, maintaining a consistent optimized growing environment is the best way to avoid fruit cracking.
The impact of both unpredicted climate change and climate variability on agricultural productivity is most likely to become a major constraint to achieve greater food production, which means that developing crop genotypes that withstand ambient stresses a major food security strategy. Hence, crop improvement innovations are needed [117]. They entail making furious efforts, especially by breeding companies that use conventional breeding programs. However, commercial success is extremely limited given the complex trait and practical selection tools are lacking; e.g., genetic markers have rendered these tasks inefficient and slow processes to date [84, 118, 119]. Combining suitable commercial fruit characteristics (quality and high production) and resistance to environmental factors is extremely difficult, especially when growing traditional varieties for their adaptation and traits quality since they are highly stress-sensitive [120, 121].
More recently, major efforts have been made to achieve genetic transformation [122, 123, 124]. Transferring a single gene or a few genes has led to claims of improved abiotic stress tolerance [125, 126]. However, the nature of genetically complex mechanisms of abiotic stress tolerance, and any potential detrimental side effects, makes this task most difficult [118, 127]. Lack of public acceptance of genetic engineering means that searching for other strategies to generate improved tolerances to abiotic stresses in plants is a priority [63, 128].
One environmental-friendly technique for avoiding or reducing loss in commercial yields caused by abiotic stress conditions is to graft susceptible commercial cultivars onto rootstocks that are capable of reducing the negative effect of external stress on shoots [25, 27, 129, 131]. Using grafted plants is an eco-friendly strategy that allows plants to overcome both soil-borne diseases and environmental stress [25, 110, 132].
Grafting is defined as the natural or deliberate fusion of plant parts to establish vascular continuity among them [133], as well as the resulting genetically composite organism functions as a single plant [134]. The term scion denotes the shoot piece that stems from a donor plant that will be the grafted plant’s canopy. The term rootstock indicates a plant that receives and fuses with the scion, and functions as the grafted plant’s root system.
Despite vegetable grafting being an ancient practice, grafting did not become a common practice in ornamental and herbaceous vegetables before the twentieth century [135]. Cultivating grafted horticultural plants began in Korea and Japan toward the end of 1920s by grafting watermelon plants to squash rootstocks [136]. Ever since, this technique has been employed in watermelon, melon, cucumber, eggplant, pepper, tomato, and ornamental cactus and has exponentially increased. Grafting is also utilized for untypical fruit vegetables like artichoke [137, 138]. The advantages that vegetable grafting offers are attributed mainly to rootstocks’ resistance to soil-borne diseases (fungus, nematodes, and bacterial wilt), and also to better vigor and stress tolerance. The problems related with banning methylbromide for soil fumigation purposes have led to increased vegetable grafting in the USA and Europe in recent years.
Micro- and tube-grafting and cleft approach are techniques that reliably combine pepper scions with compatible rootstocks, and the same can be stated of tomato and eggplant [139]. Recently, tube-grafting has become the most popular method type. It consists in cutting the growing rootstock tip at an angle of 45° below cotyledons and attaching it to the scion, which has been preciously cut at the same 45° angle above cotyledons, and then using a clip to fix the rootstock and scion (Figure 4).
Pepper seedling grafted by the tube-grating method.
Commercial varieties are not normally chosen to cope with abiotic stress. So, an interesting method to cope with these problems is to graft onto robust rootstocks.
Although grafting is a widespread eco-friendly technique applied in melon, tomato, or eggplant, it has been exploited less in peppers. This is basically because rootstock genotypes are lacking, which are simultaneously tolerant to biotic or abiotic stresses and can also improve commercial yields to amortize the extra costs incurred by grafting.
The main reason for grafting pepper is to improve plant vigor, disease tolerance, and uniformity, but very few commercial pepper rootstocks are available. This is because attention has been paid mainly to biotic stresses, and only the high-value pepper transplants utilized for protected cultivations are produced as grafted plants [39, 140, 141].
However, the abiotic stress incidence is very high, and increasing global climate change is forecast, while salinity and water stress are found frequently in areas where peppers are growing. It is necessary to perform several screenings to find Capsicum plants that tolerate abiotic stress so they can be used as rootstocks. In order to select the appropriate rootstocks, searching for resistances in wild pepper types is crucial to amplify genetic diversity [142]. Currently, wild species of pepper from gene banks have been screened and phenotypically characterized as being tolerant to salinity and water stress under control conditions, and then used as rootstocks in the field, where abiotic stress problems occur, and productivity of grafted plants has been evaluated [132, 143, 144].
One of the several approaches followed to cushion the impact of salinity is to graft plants onto tolerant rootstocks [10], and is a common agronomic practice in melon and tomato. Some works into these species have been conducted to elucidate the mechanisms that are involved in grafted plants’ increased salinity tolerance. Such increased tolerance is generally associated with plants’ capacity to retain or exclude, and/or accumulate toxic ions, Na+ and Cl− in rootstock roots. Hence, this action limits their transport to leaves instead of through the induction of antioxidant systems to the synthesis of osmotically active metabolites [35, 145]. Other authors have suggested that the rootstock’s influence on the salt tolerance of scions is owing to stomatal functions (changes in stomatal regulation and water relations) being more efficient controlled. What this suggests is that grafting incisions could alter the hormonal signaling between shoots and roots [146]. In other cases, the re-establishment of ionic homeostasis has explained increased tolerance [124]. Yet in grafted plants, the mechanism of resistance against salinity displays a high degree of complexity in relation to specific scion/rootstock interactions [145, 147], and may vary among species. As far as we are aware, very few studies have been conducted into pepper to elucidate whether the salt tolerance conferred by rootstocks is due, or not, to retention and/or exclusion mechanisms, as in melon or tomato, because of them being better able to alleviate the toxic effects of salts or of other processes; e.g., water relations being maintained or antioxidant capacity being enhanced.
Salt tolerance among pepper genotypes may vary [72]. Maas [9] has indicated a salinity resistance threshold of 1.5 dS m−1, and below which they found no effect on growth, but a 14% drop in biomass production for each additional 1 dS m−1. Thresholds within the 0–2 dS m−1 range and slopes of salinity response curves that go from 8 to 15% have been reported for greenhouse peppers [10]. Another example is to use irrigation water of 4.4 dS m−1 [67], which resulted in reductions of 46% in the pepper dry biomass and of 25% in marketable pepper fruits. Guifrida et al. [109] have reported that stunted growth caused by salinity attenuates in pepper-grafted plants, compared with the non-grafted plants, is primarily associated with a low salt ions uptake. Therefore, these ions are present in the grafted plants at lower concentrations rather than leaf turgor being maintained by osmotic adjustments.
Different tolerance mechanisms to salt stress (NaCl 40–80 mM) were observed in our experiments using tolerant accessions (previously selected) like rootstocks and commercial “Adige” cultivar as a sensitive scion. Increased fruit yield under salinity when grafted onto accessions
Such traits had a weak but negative impact on photosynthesis, nitrate reductase activity, and lipid peroxidation in the grafted scion leaves compared with ungrafted plants (Adige). Tolerance to salinity in these grafted plants was expressed to maintain scions’ ion homeostasis, and can consequently improve crop yields [148, 149].
Nevertheless, by using
Marketable fruit yields (A) and the percentage of fruits affected by BER (B) under soil salinity and water conditions. Values are the mean of 50 replicates per cultivar Adige either ungrafted (A) or grafted onto the A25 genotype (A/A25). The different letters in each column denote significant differences at P < 0.05 according to the LSD test, and following a one-way ANOVA test by taking plant type as the variability factor.
CO2 assimilation (μmol CO2 m−1 s−1) of the cultivar Adige ungrafted (A) or grafted onto the A25 genotype (A/A25) under control (white bars) and salinity conditions (black bars). The values are the means of four replicates per genotype. The different letters in each column denote significant differences at P < 0.05 according to the LSD test, and following a two-way ANOVA test with plant type and NaCl treatment taken as the variability factor.
To conclude, grafting commercial varieties onto salt-tolerant rootstocks can be considered a valid strategy for ameliorating salt tolerance in peppers.
A novel perspective to enhance resistance to water stress is to use tolerant accessions as rootstocks for a given and desirable commercial cultivar. The interactions that take place among the graft, water stress, and vegetable plants have been studied mostly in cucumber, melon [151], and tomato [130, 152] by centering on the growth effects of grafting, and also on its physiological effects, and particularly on photosynthesis traits and hydric relationships [153]. Grafted plants usually show increased uptake of water and minerals compared to self-rooted plants as a result of the vigorous root system used as the rootstock [130, 154, 155]. Greater SOD and CAT activities, higher proline accumulation levels, and lower lipid peroxidation levels have been found in tobacco scions grafted onto drought-tolerant rootstocks [156]. Tomato grafted onto a drought-tolerant line has shown not only reduced growth, but also water conservation, as well as increased photosynthetic rates under mild drought conditions [152]. Similar results have been obtained by Liu et al. [157] using luffa as rootstocks when grafted with either its scion or cucumber.
However, reports on the physiological alterations of pepper after grafting and exposure to water stress are limited. Deep pepper root systems have been considered one of most important traits of tolerance. López-Marín et al. [158] have reported finding greater root growth in drought-tolerant grafted pepper plants (Hermino grafted onto Atlante) compared with scions (Herminio) ungrafted in an irrigation-deficit regime. The physiological tolerant mechanisms to overcome water stress in pepper-grafted plants are not well-known. The effect of adding 3.5% and 7% PEG (polyethylene glycol) was examined for 14 days in two drought-tolerant rootstocks (codes 12 and 14, see Section 4.1.1) to identify the physiological traits responsible for the tolerance provided by rootstocks compared with ungrafted plants [159]. In grafted plants, we observed a higher proline level (Figure 7), along with a significant decrease in the osmotic potential, which reflected the lesser reduction in RWC. Enhanced osmotic adjustment may protect leaves from excessive dehydration. However, our results indicated that the water stress effect depended on the duration and intensity of the stress level, and also on the rootstock used.
Changes in proline concentrations in leaves (mg proline g−1 DW) from the ungrafted pepper plants (cultivar “Verset”) and the cultivar grafted onto accessions 12 and 14 after adding PEG at 0% (white bars), 3.5% (gray bars) and 7% (black bars) during a 14-day exposure period. Data are the mean values ± SE for n = 6. Within each plant combination, different letters indicate significant differences at P < 0.05 (LSD test).
Considering the overall results published about grafts, grafted plants can act as an efficient tool to mitigate abiotic stress in the climate change context and a tolerant rootstock that can make water and salt stress vanish on scions to reach greater productivity and fruit quality [149]. Nonetheless, the physiological and genetic mechanisms for abiotic tolerance in grafted plants, especially in peppers, are still unknown.
This work was financed by INIA (Spain) through Project RTA2013-00022-C02-01 and the European Regional Development Fund (ERDF).
The COVID-19 pandemic caused by the SARS-CoV2 coronavirus has resulted in almost hundred of millions of infections and about two millions of deaths in 2020 [1, 2]. According to the WHO data as of January 4, 2021, there have been 85 929 428 confirmed cases of COVID-19 reported to WHO, including 1 876 100 deaths [2]. It has been shown that in patients with laboratory-confirmed COVID-19, clinical results correlate with the presence of concomitant diseases, among which hypertension and diabetes mellitus, as well as old age, atherosclerosis, cardiovascular and cerebrovascular diseases worsening prognosis [3, 4, 5, 6, 7, 8, 9]. Notably, these factors are commonly associated with the impairments in the lipid/cholesterol metabolism and transport or are their direct consequence [3, 4, 5].
At present, a lot is known about the coronavirus SARS-CoV2. It is an enveloped single-stranded RNA virus belonging to the Betacoronavirus genus of the Coronaviridae family. The virus contains a 30 kb genome encoding four major viral structural proteins: spike (S), membrane (M), envelope (E), and nucleocapsid (N) proteins [9, 10]. According to modern concepts, the cellular receptor for S protein is angiotensin converting enzyme 2 (ACE2); binding of the S protein to this receptor allows the internalization of the virus and triggers the disease. Significant progress has been made in the development of vaccines against SARS-CoV2 and mass vaccination of people in different countries begins [11, 12]; this gives hope that the pandemic will stop. However, the issues of treating patients with various forms of COVID-19 and the development of drugs based on knowledge of the mechanisms underlying this pathology still need to be addressed. This chapter is mainly focused on the lipid aspects of the interactions of coronaviruses with host cells and, in particular, draws attention to the fact that interactions with host cells of many enveloped viruses, including coronaviruses SARS-CoV and SARS-CoV2, are cholesterol dependent. Moreover, these interactions lead to significant and potentially deleterious alterations in the cholesterol status of the infected cells. These cholesterol-dependent processes play a significant role both at the stage of the virus entry and during the development of severe respiratory syndrome (SARS) and other health problems caused by coronaviruses SARS-CoV and SARS-CoV2. Therefore, understanding this component is necessary for the development of additional approaches both to prevention and treatment of these diseases, and the attempts in this direction are being made (e.g., [13, 14, 15]). This review focuses on the fact that the coronavirus S protein, which is involved in cholesterol-dependent virus–cell interactions during entry and replication stages, contains the so-called cholesterol recognition amino-acid consensus (CRAC) motifs [16, 17] that can actually mediate these interactions. A hypothesis is put forward suggesting that binding of cell membrane cholesterol by CRAC-containing S protein (and possibly by other viral proteins) and subsequent removal of cholesterol from intracellular membranes by newly formed viral particles can affect normal functioning of cellular cholesterol-dependent proteins (receptors, ion channels, enzymes, etc.) and can eventually cause cell death due to destabilization and permeabilization of cell membranes. This deteriorating effect of CRAC-containing viral proteins can be counteracted by agents that prevent binding of membrane cholesterol to viral proteins and/or compensate for the membrane cholesterol depletion produced by the forming viral particles. It is possible that specially designed CRAC-containing peptides that specifically block interactions of S protein with cholesterol can expand the range of antiviral agents.
The viral life cycle includes four steps: entry, replication, assembly, and egress [18, 19, 20, 21] (Figure 1). At the entry step, an enveloped virus binds to a target receptor, the viral envelope fuses with the host cell membrane, and the viral nucleic acids are released into the cytoplasm. At the replication step, the nucleic acid is replicated in cytoplasmic replication organelles and viral proteins are synthesized. At the assembly step, viral proteins and nucleic acids are packed into a viral particle and the viral envelope is formed. At the egress step, mature viral particles leave the cell through the cellular membrane [18, 19, 20, 21].
Life cycle of an enveloped virus as exemplified by coronavirus (based on [
Some interactions of enveloped viruses with the cell in the course of penetration and during assembly, budding, and exit of the virus from the cell are known to depend on the presence of cholesterol and lipid rafts in the membranes of the host cells [21, 22, 23, 24, 25, 26]. This has been shown for immunodeficiency viruses (HIV) [27, 28, 29, 30, 31], influenza [32, 33, 34, 35, 36, 37], herpes [38], Newcastle disease virus [39], and rotavirus [40], as well as hepatitis C virus (HCV) [41, 42, 43] and some other viruses of the Flaviviridae family (Yellow fever virus, Zika virus, Dengue virus, West Nile virus [44, 45]). For example, the vital need of cholesterol for replication of hepatitis C virus (HCV) was shown by different methods in [41, 43]. Lipid withdrawal from the medium considerably suppressed the virus replication, which was restored to normal levels upon addition of exogenous LDL. Moreover, virus replication was suppressed by knockdown or pharmacological inhibition of Niemann–Pick type C1 protein (NPC1) – cell protein mediating the endosomal cholesterol transport [41, 43].
The cholesterol dependence of virus–cell interactions has also been demonstrated for various coronaviruses [14, 15, 46, 47, 48, 49, 50, 51, 52], including SARS-CoV and SARS-CoV2 [50, 51, 52]. Li et al. 2007 [50] reported that the production of SARS-CoV particles released from the infected Vero E6 is notably suppressed following cholesterol depletion by cell pretreatment with methyl-β-cyclodextrin (mβCD), and the addition of cholesterol to the culture medium reversed this effect. Later, Glende et al. 2008 [51] showed that the removal of cholesterol from cell membranes using mβCD reduces the efficiency of infection of cells not only with the SARS-CoV but also with a non-replicating pseudotype of vesicular stomatitis virus containing the surface glycoprotein S of the SARS-CoV virus (VSV-ΔG-S), which confirms the key role of the S protein in the virus entry. The authors also reported that the cellular receptor of the SARS-CoV virus, angiotensin-converting enzyme (ACE2), is co-localized with Flotilin2 and LAMP2, the protein markers of the detergent-resistant membrane domains (rafts) [51].
The issues concerning the importance of the host cell membrane lipids, rafts, and cholesterol at different stages of the virus life cycle have been addressed in numerous comprehensive reviews, and the dependence of the viral life cycle on cellular cholesterol, as well as the impact produced by viruses on cellular lipids and cholesterol in particular is regarded as a basis for antiviral therapy [15, 30, 31, 45, 53]. For example, cholesterol-lowering treatments are considered as a possible prophylactic or preventive measures [45, 54]. However, alterations in the cell lipid status produced by viruses that have entered a cell impose more complex requirements on potential medicines.
Viruses not only depend on cholesterol but also significantly modulate the lipid composition of cell membranes [53, 55, 56, 57, 58, 59, 60, 61, 62, 63]. This occurs both at the stage of virus internalization and during the synthesis of viral proteins and intracellular assembly of new viral particles. The consequences of these changes can determine the clinical course and severity of the disease. The release of the gene material of many enveloped viruses into the cytoplasm of the cell occurs by fusion of the viral envelope with plasma membrane or with membranes of late endosomes (endolysosomes) formed during receptor-mediated endocytosis [18, 19, 20, 21, 64, 65, 66, 67, 68, 69, 70]. The inclusion of viral envelopes into the host cell membrane (either after direct fusion of after endosomal membrane recycling) should change both the lipid and protein composition of the cell membrane and cause rearrangements in the lipidic milieu and antigenic profile of the host cell membrane (Figure 1). Further, at the stage of the assembly of new viral particles, their envelopes are formed from cellular membranes [14, 15, 45, 55, 57, 58, 59, 60, 61, 62, 63, 64, 65, 67, 68]. Some viruses bud from the plasma membrane (e.g., togaviruses, rhabdoviruses, paramyxoviruses, orthmyxoviruses, and retroviruses, including HIV), others use the endoplasmic reticulum (ER) (coronaviruses and flaviviruses) or/and a Golgi complex (bunyaviruses), some (e.g., herpes virus) have more complicated budding scenario [59, 60, 61, 62]. The formation of the viral envelopes can involve lipid sorting and, in particular, accumulation in the viral envelope of cholesterol and sphingolipids that are acquired from the host cell membranes [33, 61, 62, 63, 64, 65, 69, 70]. For example, HIV-1 selectively buds from membrane domains enriched in cholesterol and sphingolipids (rafts); as a result, host cell rafts become a viral coat and the level of cholesterol and sphingolipids and the cholesterol/phospholipids ratio in the viral envelope is higher than in the plasma membrane where they originate, and also notably higher than in the intracellular membranes [53, 61, 62, 65]. Another example – bovine viral diarrhea virus (BVDV) of the Flaviviridae family budding from the endoplasmic reticulum (ER): the content of cholesterol, sphingomyelin, and hexosyl-ceramide in the BVDV particles was shown to be more than twofold higher than in the infected cells [69]. As the cholesterol concentration in the ER is significantly (several times) lower than in the plasma membrane [71, 72, 73, 74], the loss of cholesterol due to the formation of viral envelopes can be destructive for the ER membranes.
For lipid sorting necessary for the virus envelope formation, various mechanisms are used to manipulate synthesis, metabolism, and transport of host lipids, cholesterol in particular, and lead to significant changes in the lipid status of the host cell. HIV-1 infection is known to induce various alteration of cellular lipids, including increased cholesterol synthesis and uptake [75], suppressed cholesterol efflux [76], as well as a shift in phospholipid synthesis to neutral lipids and peroxidation of polyunsaturated fatty acid [53, 65, 75, 76]. Hepatitis C virus (HCV) also causes massive rearrangements of intracellular membranes leading to the formation of double-membrane vesicles (DMVs) enriched with cholesterol. As was shown in [41], HCV ‘usurps’ cholesterol transporter proteins, such as NPC1, in order to deliver cholesterol to the viral replication organelle where cholesterol is needed, and blockage of this transporter suppresses the virus replication. Coronaviruses, like Flaviviruses, are assembled and bud from the membranes of Golgi complex and ER [41, 60] and also form double-membrane vesicles [77]. At the same number of newly formed viral particles, the consequences of removing cholesterol from ER membranes by double-membrane vesicles can be more severe than in the case of single membrane vesicles; a quantitative assessment of this process is necessary.
A possible mechanism stimulating the delivery of cholesterol to ER from plasma membrane during coronavirus replication was demonstrated by Wang et al. 2020 [78]. The authors reported that SARS-CoV2 activates the host cell gene encoding cholesterol 25-hydroxylase and induces the formation of 25-hydroxycholesterol, which increases cholesterol availability [79] and triggers its delivery from the plasma membrane to the endoplasmic reticulum, where cholesterol is required for the viral envelope formation. Although, as is known [14, 23, 24, 25, 26, 27, 28, 29, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 46, 47, 48, 49, 50, 51, 52, 53, 54, 55], the depletion of cholesterol in the plasma membrane suppresses the virus entry into the cell, the observed trafficking of cholesterol into the ER (normally the flow goes in the opposite direction [71, 72]) can reflect an increased uptake of cholesterol for the formation of envelopes of new viruses. After the release of newly formed viruses, this depleted cell will not be susceptible to new infection.
Thus, the formation and release of viral particles from the cell cannot but affect the composition of the host cell membranes. It can be expected that after a full replication cycle of viruses with high envelope cholesterol, the level of cholesterol in the membranes of the host cell will be reduced, and this depletion of cholesterol can lead to a significant deregulation of cholesterol-dependent processes, including intracellular signaling and metabolic pathways. At a high rate of assembly of a large number of viruses, infected cells may not be able to compensate for the loss of cholesterol in their membranes, and this can lead to cell death due to destabilization and permeabilization of cell membranes. Indeed, ample evidence indicates that lowered membrane cholesterol is associated with altered mechanical properties and increased permeability of the membrane [80, 81, 82, 83]. Some viral and bacterial proteins trigger apoptosis through lysosomal membrane permeabilization leading to release of cathepsins [81]. The human immunodeficiency virus type 1 (HIV-1) protein Nef is one of such proteins: when entering mammalian cells, it causes permeabilization of the lysosomal membrane [81]. It seems appropriate at this point to recall that permeabilization of intracellular membranes due to cholesterol depletion underlies the cytotoxic effect of some anticancer drugs [81, 84, 85, 86, 87]. As was shown by Appelqvist et al. 2011 [84], the mechanism of action of cisplatin and some other lysosomotropic drugs at least partially is based on the permeabilization of lysosomal membranes leading to cell death; cholesterol accumulation in lysosomal membranes caused by inhibition of cholesterol transporting protein NPC1 prevented the lysosome-dependent cell death [84]. Note that in the case of virus infection, inhibition of the NPC1-dependent cholesterol transport suppressed the virus replication [41] and rescued the infected cells. When NPC1 functions normally and cholesterol is delivered from lysosomal compartment to ER for the formation of viral envelopes, lysosomal membranes lose cholesterol and become leaky; in a way, virus acts like a lysosomotropic drug. Cholesterol supplementation was also shown to reverse a strong cytotoxic effect on colon cancer cells caused by a low molecular weight compound TASIN-1 producing cholesterol-dependent ER stress triggering oxidative stress and JNK-dependent apoptosis [85].
Thus, virus–cell interactions lead to significant modulations in the lipid composition of cell membranes. A decrease in cholesterol in cell membranes owing to the formation of viral envelopes can be one of the most dangerous consequences of the virus particle assembly, as the amount of cholesterol removed from the cell membranes by newly formed viruses can exceed the compensatory resources of the cell. If the delivery of cholesterol to the cells is insufficient, deregulation of cholesterol-dependent processes can lead to massive cell death, which manifests itself in the clinical course of the disease and a poor prognosis. In this connection, it should be noted that in patients infected with COVID-19, a significant decrease (several fold) in total cholesterol and low-density lipoprotein (LDL) cholesterol levels was recorded [13, 88], and cholesterol-lowering treatments (such as statins) may not be advisable for patients with life-threatening COVID-19 infection, at least until they recover from the infection [88]. Such a drop of the LDL cholesterol level in COVID-19 patients may reflect an enhanced recruitment of circulating cholesterol by the cells to compensate for its loss associated with virus reproduction. Perhaps the clinical prognosis depends on the timely and successful delivery of cholesterol required for cell membrane repair. Another direction in the development of drugs for the treatment of the disease is the search for agents that interfere with the interactions of viral proteins with cholesterol, and this search should be based on an understanding of the mechanisms of these interactions. So far, the only drugs for which clinically significant results have been demonstrated against COVID-19, are dexamethasone and some other corticosteroids [89, 90, 91]; secosteroids (vitamin D) are shown to help, too [92]. The use of dexamethasone led to a reduction in mortality to one third of hospitalized patients with severe respiratory complications from COVID-19. It seems possible that the action of steroids may be associated with the repair of a cell membrane damaged by virus-induced depletion of cholesterol.
How does the virus manage to bind and remove cholesterol from cell membranes?
As was shown earlier [16, 17, 93], some proteins involved in cholesterol-dependent cell functions possess the so-called cholesterol recognition/interaction amino acid consensus (CRAC) motifs – small regions with a specific set of amino acid residues involving a branched apolar aminoacid residue (Val (V), Leu (L), or Ile (I)), aromatic residue (Tyr (Y)), and cationic aminoacid residue (Arg (R) or Lys (K)); these motif-forming amino acids are separated by short segments of any 1–5 amino acid residues. In subsequent discussions, more candidates of aromatic amino acid residues were proposed, and the general formula for the CRAC motifs presumably involved in the interaction of protein with cholesterol presently appears as follows: V/L/I–X(1–5)–W/Y/F–(X)(1–5)–R/K, where X stands for any amino acid residue [94, 95, 96, 97, 98, 99, 100]. Although the predictive value of this formula has been questioned [95, 96, 97], the presence of this motif in many proteins and its participation in the protein–cholesterol interactions has been confirmed by different methods [16, 17, 93, 94, 95]. The formula of the CRAC motif can be further developed [94]; important is the very concept of a motif mediating the interactions of cholesterol-dependent proteins with cholesterol.
CRAC motifs are found in many viral proteins, and their role in cholesterol-dependent virus–cell interactions have been demonstrated. For example, CRAC motifs are present in the HIV matrix protein р17, which was shown to participate in virus entry through the raft domains of the cell membranes [27, 101]. The α-helical domain of the hepatitis C virus nonstructural protein NS5A, which is anchored at the cytoplasmic leaflet of the endoplasmic reticulum and is involved in replication hepatitis C virus, also contains CRAC motif [102]. Importantly, peptides derived from this domain were shown to exhibit a broad-spectrum anti-viral activity. Cheng et al. 2008 [103] reported that peptide C5A containing amino acid residues 3–20 of the amphipathic α-helical N-terminal domain of hepatitis A virus protein NS5A suppressed the virus replication by more than 5 orders of magnitude. The authors did not mention the CRAC concept; however, the active peptide C5A (SWLRDIWDWICEVLSDFK) clearly contains the CRAC motif: RDIWDWICEV. Later, the antiviral activity of this peptide C5A against HIV was also demonstrated [104]. It is possible that peptide C5A, owing to the presence of the CRAC motif, binds cholesterol and competes for cholesterol binding with viral protein and thus inhibits the formation of the viral particle.
CRAC motifs are found in alpha-helices of matrix protein M1 of influenza A virus [105, 106, 107]. An important role of these CRAC motifs in the organization of the raft structure of the virion membrane was substantiated by using the method of directed point mutations in the CRAC-containing α-helices in the M1 protein [106, 107]. Further studies revealed that M1-derived peptides containing CRAC motifs LEVLMEWLKTR, NNMDKAVKLYRKLK, GLKNDLLENLQAYQKR, corresponding to α-helixes 3 (aa 39–49), 6 (aa 91–105) and 13 (aa 228–243), respectively, to a different extent modulate cholesterol-dependent interactions of cultured macrophages with 2-μm particles that mimic bacteria (phagocytic index). Of the three peptides, NNMDKAVKLYRKLK was most potent and stimulated the cell activity by 50–60% at 35 μΜ [108]. Peptide RTKLWEMLVELGNMDKAVKLWRKLKR obtained by combining two of these short peptides and containing two CRAC motifs produced much stronger and more complex effect: in a narrow range of low concentrations (1–5 μM) the peptide exerted a stimulatory effect and at 50 μM the peptide was cytotoxic [109]. Reducing the cholesterol content in the cells with methyl-β-cyclodextrin (mβCD) abolished the stimulatory component and lowered the peptide concentration required for the toxic effect. Substitution of the motif-forming amino acids abolished these effects [110]. The cytotoxic effect of the M1-derived peptide RTKLWEMLVELGNMDKAVKLWRKLKR can be explained by the binding (sequestration) of membrane cholesterol by the peptide; this can imitate removal of cholesterol from cell membranes, which occurs during the formation of the viral envelope.
S proteins of coronaviruses SARS-CoV and SARS-CoV2 also contain CRAC motifs [51, 109, 110]. For example, in the case of the S protein of coronavirus SARS-CoV, the CRAC motif YIKWPWYVW is located in the “aromatic” region of the transmembrane domain of the S-protein; this highly conserved region of the S-protein was shown to be necessary for the infection of cells with coronavirus [111, 112].
If the assumption about the essential role of sequestration and removal of membrane cholesterol by viral CRAC-containing proteins in the COVID-19 parthenogenesis is correct, then in order to prevent this destructive action for the cell, it is necessary to maintain a safe level of cholesterol in the plasma membrane. A significant decrease in total cholesterol and low-density lipoprotein (LDL) cholesterol levels in COVID-19 patients [13, 88] may be indicative of the critical loss of cholesterol by cells, and an efficient cholesterol delivery to the cholesterol-depleted cells may be helpful. Cyclodextrins are possible candidates as non-toxic cholesterol transporters [113, 114, 115, 116], which can redistribute cholesterol from endogenous and/or exogenous sources. The use of cyclodextrins increased the lifespan of NPC1−/− experimental mice [117] and improved the condition of patients with Nieman–Pick disease [118]. Another alternative is to prevent viral proteins from interacting with membrane cholesterol. At least some of the drugs that are currently tested – for example, polyphenolic substances like quercetin and saponin glycyrrhizin [119, 120] – can act at the protein/cholesterol interface and hinder cholesterol binding by the CRAC motif of the viral S protein and thus inhibit the assembly of new viral particles. Glycyrrhizin, an active component of liquorice roots, was shown to inhibit SARS-CV replication in Vero cells and replication of SARS-associated coronavirus [121, 122]. However, such agents are not very selective and can affect other cholesterol-dependent proteins and therefore cause side effects. Perhaps specially designed CRAC-peptides specifically blocking the interactions of S-protein with cholesterol will prevent the cellular cholesterol loss leading to permeabilization of membranes, oxidative stress, and cell death. The ability of CRAC-containing peptides to regulate cholesterol-dependent cell functions has been demonstrated in a number of works [17, 109, 122, 123], and studies of the antiviral activity of these peptides may be useful and promising.
The SARS-CoV2 pandemic has sparked a brainstorming session over the underlying mechanisms of viral diseases. Many assumptions have been made. This chapter considers possible consequences of cholesterol depletion in the membranes of infected cells due to the formation of cholesterol-rich viral envelopes. At a high viral load and high replication rate the reduction in the cholesterol level in the cell membranes can lead to their permeabilization and subsequent cell death, and this can be one of the factors in pathogenesis of diseases induced by SARS-CoV2. Cholesterol-recognition/interaction (CRAC) motifs in viral proteins may represent a mechanism for the binding of the viral protein with cholesterol. Substances preventing these interactions of viral proteins with cholesterol can suppress the formation of the viral envelope and therefore can be studied as possible antiviral drugs. Peptides containing CRAC motifs from viral proteins may be among these substances.
The work was partially supported by the Russian Foundation for Basic Research (project no. 18-04-01363).
The author declares that there is no conflict of interest.
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