Exogenous calcium: Its mechanisms and research advances involved in plant stress tolerance

Abiotic stresses are various environmental factors that inhibit a normal plant growth and limit the crop productivity. Plant scientists have been attempting for a long time to understand how plants respond to these stresses and find an effective and feasible solution in mitigating their adverse impacts. Exogenous calcium ion as an essential element for the plant growth, development and reproduction has proven to be effective in alleviating plant stresses through enhancing its resistance or tolerance against them. With a comprehensive review of most recent advances and the analysis by VOSviewer in the researches on this focus of “exogenous calcium” and “stress” for last decade, this paper summarizes the mechanisms of exogenous calcium that are involved in plant defensive responses to abiotic stresses and classifies them accordingly into six categories: I) stabilization of cell walls and membranes; II) regulation of Na⁺ and K⁺ ratios; III) regulation of hormone levels in plants; IV) maintenance of photosynthesis; V) regulation of plant respiratory metabolism and improvement of root activities; and VI) induction of gene expressions and protein transcriptions for the stress resistance. Also, the progress and advances from the updated researches on exogenous calcium to alleviate seven abiotic stresses such as drought, flooding, salinity, high temperature, low temperature, heavy metals, and acid rain are outlined. Finally, the future research perspectives in agricultural production are discussed.

Introduction

Plants are subject to a variety of biotic or abiotic adverse attacks and stresses throughout their entire growth, development and reproduction. These adversities can force plants to suffer from a mild osmotic, oxidative and/or ionic imbalance to serious biochemical and physiological disorders such as disruption of cell membranes, reduced enzyme activity, weakened photosynthesis and respiration, and decreased uptake of mineral elements (AbdElgawad et al., 2016; Zhang et al., 2022). To some degree, plants possess limited capabilities of improving their resilience, resistance or tolerance against some mild stresses through a series of morphological, physiological and molecular adjustments, but they are not strong or sufficient to survive from the severe ones. Therefore, Seeking for exogenous substances to induce or enhance such plant positive responses against irreversible adversities have become an ultimate goal for many researchers working on this field, and a promising, realistic and feasible approach in the current research attempts. So far, many exogenous substances have proven to be beneficial and effective in alleviation of plant abiotic stresses (Feng et al., 2023).

Among exogenous substances discovered to alleviate plant stresses, calcium ion (Ca²⁺) has proven to be more effective and the cost/benefit efficient, not only as an essential nutrient for the plant growth actively involving in a various metabolic activities and as an intracellular messenger for many signal transductions, such as abscisic acid (ABA), reactive oxygen species (ROS), nitric oxide (NO), et al. (Besson-Bard et al., 2008; Marcec et al., 2019; Shabbir et al., 2022). Different parts of a plant differ in their absorption, translocation and utilization of exogenous Ca²⁺. The exogenous Ca²⁺ absorbed by roots is mainly through a mass flow of soil water to the root surface and the apoplastids and coplastids in root vascular bundles for its upward movement due to plant transpiration (Zhou and Wang, 2007). Once being applied on foliage, exogenous Ca²⁺ enters mesophyll cells mainly through stomata, hydrophilic pores in the stratum corneum, and ectoplasmic filaments distributed on the leaf surface. Once inside plants, free Ca²⁺ moves through Ca²⁺ transport systems such as the sphinoplasmic Ca²⁺ outflow system (Ca²⁺-ATPase pump), Ca²⁺/H+ reverse transporter, and cytosolic Ca²⁺ influx system so that the Ca²⁺ concentration increases rapidly in tissues where Ca²⁺ is needed for normal metabolic functions or in response to environmental changes/stresses for an internal homeostasis in plants (Zhou and Wang, 2007). Ca²⁺ also serves as a cellular messenger when the Ca²⁺ concentration in cytoplasm is different from that in intercellular space available as a Ca²⁺ source. A high concentration of Ca²⁺ in a plant seemly acts as a transmitting signal for the activation of various metabolic and molecular activities. Calcium is inert, difficult to move around in plants, hardly to be reused by cells, and prone to bind to organic acids for a further transportation to and utilization in tissues and cells that really needs it. Moreover, any stresses such as drought, high temperature, low temperature and excessive rain affecting plant transpiration can seriously further reduce the calcium absorption and movement even if soil Ca²⁺ is available, in which case, a foliar application of exogenous calcium can be critically important for the plant stress tolerance. It has been reported that Ca²⁺ can help resist adverse irritations or damages to some extent in abiotically stressed plants through five mechanisms, including the regulation of sodium/potassium ion (Na⁺/K⁺) ratio and ABA concentration, stabilization of cell walls/plasma membranes, recognition of Ca²⁺/Ca²⁺-dependent protein kinases (CDPKs) system, and initiation of specific gene expression (Gong and Wang, 2011). However, the plants under stress are less capable of absorbing and translocating Ca²⁺, which could seriously impair plant tolerance and resistance against abiotic stresses. Therefore, an external application of different Ca²⁺ supplements has become a main stream of hot research frontlines to provide a sufficient quantity of usable Ca²⁺ for crops to fight against abiotic stresses (Heidari et al., 2019).

VOSviewer has been used to analyze all English literature published on the Web of science database for the last decade in the scientific research community. In this review, we also used this application to connect all important subjects (dots) under the keyword of “exogenous calcium” and “stress” to generate a hotspot map of international research reports (Figure 1). In the chart generated through VOSviewer, five research hotspots, such as “plant species”, “growth status”, “accumulation of substances”, “tolerance and response mode” are closely related to “exogenous calcium” and “stress”. As far as the application of exogenous calcium for alleviating plant stresses is concerned, most published papers are focused on the salt and drought stress while fewer studies have been conducted on the stress due to the high temperature, low temperature, flooding, heavy metal and acid rain. In terms of the mechanism pertaining to plant stress alleviation by utilization of exogenous calcium, “oxidative stress”, “photosynthesis”, “osmoregulation”, “gene and protein expression” and “membrane lipid peroxidation” have surfaced as research hotspots in recent years, among which “oxidative stress” and “photosynthesis” are the most studied areas in the past two years.

FIGURE 1

Figure 1 Hotspot analysis of English literature on “exogenous calcium” and “stress” in the last 10 years. The size of each dot represents the focal weight of each key word in the literature and the lines between two dots indicate their coupling relationships.

A number of advances have been made and many sophisticated instruments used in researches on application of exogenous calcium for plants to alleviate various stresses. Guo et al. (2021) used an inductively coupled plasma optical emission spectrometer to detect whether the exogenous calcium would increase K⁺ and Ca²⁺ abundance, decrease Na⁺ content in plants, and maintain the ion homeostasis in Gleditsia sinensis Lam. that was under salt stress through regulating the Na⁺/K⁺ ratio. He et al. (2015) applied the fluorescent and ultrastructural cytochemical method to determine if exogenous calcium had mitigated hazard effects of flooding stress on plant respiration by regulating the activity of respiratory metabolic enzymes in cucumber cells. Shi et al. (2014a) found that exogenous Ca²⁺ enhanced plant cold tolerance by promoting the differential expression of redox-related and cellular metabolism-pertaining proteins through a comparative proteomic and metabolomics analysis. Hu et al. (2018) indicated that an exogenous Ca²⁺ application not only had a positive effect on the integrity and function of plasma membrane but also alleviated peroxidative damages caused by draught stress on chloroplast and mitochondrial membranes. Exogenous Ca²⁺ have also proven to regulate the ABA content in plants under low temperature along with the hormone levels of gibberellic acid (GA), cytokinin (CTK), and indole-3-acetic acid (IAA) to maintain a balance (Liu et al., 2017). In addition, the degradation of plant chlorophylls, the damage to photosynthetic organs, and the stable performance of plant photosynthesis could be alleviated or prevented by exogenous Ca²⁺, which was demonstrated through using a portable chlorophyll fluorescence pulsometer (Li et al., 2022a). According to Gong and Wang (2011) the mode of actions with each exogenous calcium applied to alleviate plant stresses has much in common with the mechanism involving in plant responses to abiotic adversities, which is mainly through regulating ion balance, inducing expression of resistance genes and/or proteins, and increasing the enzyme activity and osmoregulatory substance content. However, the mechanisms involved in the plant stress alleviation are more complex and they are not easily or simply classified by one or two features based on regulating, modulating or participating in biological and physiological metabolisms or gene expression. For example, the mechanism associated with the recognition of Ca²⁺/CDPKs (Gong and Wang, 2011) mainly is through activating key enzymes and further inducing a series of complex physiological and biochemical responses such as production of more resistant proteins and enhancement of gene expressions for plant stress tolerance. So, the CDPKs recognition mechanism should be included into the category of the gene expression. Moreover, under flooding stress, exogenous calcium can also regulate the plant respiratory pathway to increase root activities for plants to withstand flooding stress (Yang et al., 2016; Han et al., 2019). Based on the relevant mechanisms of exogenous calcium on alleviating adversary stresses and the accumulative information shown in the hotspot analysis maps that is generated from the VOSviewer report for last 10 years, this paper intends to summarize the underlying mechanisms of exogenous Ca²⁺ involved in alleviation of plant abiotic stresses and tentatively place them into six major categories: I) stabilization of cell wall and membranes; II) regulation of Na⁺ and K⁺ ratios; III) regulation of hormone levels in plants; IV) maintenance of photosynthesis: V) regulation of plant respiratory metabolism and improvement of root activities; and VI) induction of gene expressions and protein transcriptions for the stress resistance. Since several outstanding papers have outlined other functional aspects of Ca²⁺ in plants such as its role as a signal messenger, its regulations as a molecular modulator in gene expressions, and its movement through transpiration, etc. (Edel and Kudla, 2016; Marcec et al., 2019; Wang X. et al., 2019; Liu H. et al., 2022), this review has ultimately summarized in detail the research progresses made on studies of exogenous Ca²⁺ and its effect on alleviation of seven abiotic stresses, drought, flooding, salt, high temperature, low temperature, heavy metals, and acid rain. At the end, a discussion of perspectives for developing experimental approaches that would take those mechanisms into account for use of different exogenous Ca²⁺ in increasing plant tolerance against abiotic stresses is provided.

Advances in application of exogenous Ca²⁺ under abiotic stresses

Drought stress

Recent studies on the drought alleviation by exogenous Ca²⁺ were conducted on 15 plant species and outlined in detail (Table 1), concluding that it actively involved in keeping water content and balance under check through the mechanism I, III, IV and VI when water deficit is encountered in plants under drought stress. Drought stress is one of the most important adversities causing crop yield reduction worldwide (Iqbal et al., 2020), causing imbalance in water metabolism in plants, affecting photosynthesis and bringing adverse effects on plant growth and development. Qin et al. (2019) found that exogenous Ca²⁺ help promote plants under drought stress to accumulate endogenous Ca²⁺, especially free Ca²⁺ content in datura plants that bind the calmodulin and thus directly or indirectly regulate intracellular related enzyme activities and cellular functions to improve seed germination. Hu et al. (2018) found that exogenous Ca²⁺ treatment under drought stress can stabilize the structure and function of chloroplast, mitochondrial and endosomal systems in chloroplasts, maintain net photosynthetic rate and gas exchange, alleviate the degradation of photosynthate, and ensure the normal operation of PSII. Li et al. (2012) found that exogenous Ca²⁺ could reduce the stomatal aperture of honeysuckle for adaptation to drought conditions. In addition, Naeem et al. (2017) indicated that the exogenous Ca²⁺ treatment could increase the relative water content in maize and compensate a water deficit caused by drought to some extent.

TABLE 1

Table 1 List of optimal concentrations of exogenous calcium used to alleviate drought stress on different plants.

Flooding stress

Recent research findings have demonstrated that exogenous Ca²⁺ (CaCl₂ only) is partially or completely participated in all structural, physiological, biochemical and genetic adjustments against flooding stress that causes temporary or prolonged hypoxia in crop roots due to lack of oxygen. The impairments or damages of hypoxia mainly include a blockage of the mitochondrial electron transport chain, a reduced aerobic respiration and an enhanced anaerobic respiration. Thus, a large amount of toxic ethanol, acetic acid, pyruvic acid and other substances are subsequently produced and accumulated in plants. Recent studies have proven that the exogenous Ca²⁺ treatment could have: 1) effectively minimized the ethanol, acetic acid and pyruvate content to mitigate their toxic effects in peony plants under flooding stress through reducing activities of the lactate dehydrogenase (LDH) and pyruvate decarboxylase (PDC), and increasing the alcohol dehydrogenase (ADH), malate dehydrogenase (MDH), and glucose-6-phosphate dehydrogenase (G-6-PDH) (Fan, 2019); 2) improved the catalytic capacity of pepper pentose phosphate so to produce more adenosine-triphosphate (ATP) and nicotinamide adenine dinucleotide (NADPH) and to improve plant respiratory metabolism (Yang et al., 2016); 3) promoted glycolysis and the accumulation of enzymes in the tricarboxylic acid cycle by reducing the peroxidation level of cucumber seedlings and enhanced the activity of mitochondrial antioxidant enzymes to promote the metabolism of cucumber roots and the transport of Ca²⁺ and K⁺ plasma, thus improving the hypoxia tolerance of cucumber (He et al., 2015); and 4) reduced polyamine degradation in muskmelon seedlings under anoxic conditions by promoting nitrate uptake and accelerating its conversion to amino acids, heat-stable proteins, or polyamines (Gao et al., 2011). Relevant studies of exogenous Ca²⁺ in mitigation of plant flooding stress are conducted on five crop species (Table 2).

TABLE 2

Table 2 List of optimal concentrations of exogenous calcium used to alleviate flooding stress on different plants.

Salt stress

Up to date, 19 plant species have been evaluated for their tolerance against different salt stresses through using various forms of exogenous Ca²⁺ in different application methods such as watering, hydroponic, soaking and foliar spray. The outcome from those studies showed that their overall mechanisms are diversified and complex mainly to maintain the ion balance and avoid the plant osmosis from impairment. Salt stress causes an ionic imbalance in plants due to the accumulation of Na⁺ and a great loss of Ca²⁺ and K⁺. It also causes osmotic impairments resulting in an oxidative disturbance by an excessive accumulation of ROS that affected the photosynthesis-related activities of electron transportation, phosphorylation, and dark reaction-involved enzymes (Shu et al., 2012; Manaa et al., 2014). Guo et al. (2021) found that exogenous Ca²⁺ promoted the function of K⁺ channels and its uptake through the root plasma membrane, reduced the permeability of the plasma membrane for Na⁺ pumping so to decrease the accumulation of passive Na⁺ inward flow. Li et al. (2022a) indicated that the exogenous Ca²⁺ treatment could increase the maximum photochemical efficiency (Fv/Fm) under salt stress in Mongolian pines and 10 mM exogenous Ca²⁺ could promote the growth of Salix matsudana Koidz seedlings and increase their stomatal conductance, transpiration rate (Tr) and net photosynthetic rate. Li et al. (2022c) also showed that exogenous Ca²⁺ significantly up-regulated genes encoding phospholipase C, inositol-3-phosphate synthase, and phosphatidylserine decarboxylase to stabilize cell membranes, up-regulated the expression of PsbQ, PsbP, and Psb28 subunits on encoded PSII, and protected PSII to increase photosynthetic rate of Pennisetum Giganteum, revealing the connections between the gene regulation and biochemical metablisms. Zehra et al. (2012) found that the concentration of exogenous Ca²⁺ required for alleviation of salt stress in Phragmites karka seeds varied. Relevant studies on exogenous Ca²⁺ mitigation of salt stress in plants involved 19 plant species, as detailed in Table 3.

TABLE 3

Table 3 List of optimal concentrations of exogenous calcium used to alleviate salinity stress in different plants.

High temperature stress

While being applied to plants, exogenous Ca²⁺ can prevent or mitigate a possible light damage caused by high temperature that assumingly disrupts the photosynthetic function of plants and severely affects their photosynthesis efficiency. Wang et al. (2022) found that the exogenous Ca²⁺ treatment significantly increased the chlorophyll (Chl) content, net photosynthetic rate (An), Tr, stomatal conductance (Gs), and antioxidant enzyme activities such as SOD, POD, ascorbate peroxidase (APX), and proline (Pro), as well as the content of osmoregulatory substances such as soluble sugars and soluble proteins to improve the heat tolerance of rosebay. Sun et al. (2015) indicated that exogenous Ca²⁺ could increase the ribulose-1,5-bisphosphate carboxylase (Rubisco) activity and leaf Fv/Fm of Capsicum fructescens L. to alleviate the photoinhibition to enhance the stomatal conductance and carbon assimilation efficiency. Tiwari et al. (2016) demonstrated that the exogenous Ca²⁺ treatment upregulated the levels of heat shock genes groEL and groES to maintain cell viability under high temperature stress. Bhatia and Asthir (2014) concluded that the exogenous Ca²⁺ treatment maintained the growth of wheat seedlings under high temperature stress by altering the carbohydrate metabolism in wheat seeds and increasing the total sugars through reducing sugar-metabolism-related a-amylase and β-amylase activities. In addition, Naeem et al. (2020) showed that exogenous Ca²⁺ was also involved in the process of adjusting leaf surface structure and configuration to dissipate heat by regulating the conductance of plant stomata for the purpose of alleviating heat stress in plants. Relevant studies on exogenous Ca²⁺ mitigation of heat stress in plants involved 11 plant species, as detailed in Table 4.

TABLE 4

Table 4 List of optimal concentrations of exogenous calcium used to alleviate heat stress in different plants.

Low temperature stress

Low temperature as one of the main abiotic stresses reduces the cell membrane fluidity and enzyme activities before the temperature reaches a freezing point, inhibits plant physiological metabolic activities, and affects seed germination and seedling growth through the mechanism I, III, IV, VI as described in Table 5. The exogenous Ca²⁺ treatment could help leaves adjust their structure and configuration, promote the operation of cyclic electron transport and enhance the lutein cyclic de-cyclic oxidation in cells to alleviate photoinhibition in tomato plants (Zhang et al., 2014). It also mitigated the damage to chloroplasts due to the low temperature and promote the export of nonstructural carbohydrates to maintain normal plant photosynthesis in peanut seedlings (Wu et al., 2020b). Zhang et al. (2020) indicated that an exogenous application of CaCl₂ significantly increased chlorophyll fluorescence indicators (Fv/Fo, Fv/Fm) and the photosynthetic rate in maize, while Liu J et al. (2022) demonstrated that the same treatment onto onion plants reduced cell wall porosity and lowered intracellular ice nucleus temperature. Shi et al. (2014a) concluded that adding exogenous Ca²⁺ enhanced ROS scavenging through increasing the activity of antioxidant enzymes and non-enzymatic GSH to maintain intracellular ROS at a low level. Relevant studies on exogenous Ca²⁺ in mitigation of low temperature stress in plants have been reported on nine plant species (Table 5).

TABLE 5

Table 5 List of optimal concentrations of exogenous calcium used to alleviate low temperature stress in different plants.

Heavy metal stress

All researches on exogenous Ca²⁺ in alleviation of heavy metal stress in plants have indicated that additional Ca²⁺ limits the uptake, movement and distribution of excessive heavy metals that might accumulate to a toxic level through five mechanisms except the mechanism V summarized in Table 6. Most studies have been focused on alleviation of Cd toxicity by an exogenous Ca²⁺ application. López-Climent et al. (2014) determined that exogenous Ca²⁺ had attenuated the Cd uptake in citrus through enhancing the metabolism to detoxicate harmful ions, which promoted the GSH synthesis, and thus increased endogenous GSH levels of the phytochelatin (PC) biosynthesis for the Cd detoxication. According to Shi et al. (2014b), exogenous Ca²⁺ increased the mitotic index and decreased the chromosomal aberration rate of Wedelia trilobata L. to transport Cd out of stressed cells. Li et al. (2021) suggested that exogenous Ca(OH)₂ was more effective than CaCl₂ in increasing the quantity of the Ca²⁺ channel protein (CC), ATPase, cationic/H⁺ antiporter (CAXs) and membrane transporter protein in Panax notoginseng plants under Cd stress. A proper application of Ca(OH)₂ was also reported to increase soil pH, decrease the toxicity of heavy metals, and reduced the uptake of Cd by plants (Zu et al., 2020). Issam et al. (2012) pretreated the Faba bean (Vicia faba L.) foliage with exogenous Ca²⁺ and proved that the membrane integrity and lipid/fatty acid distribution were protectively stabilized to tolerate heavy metal stress. Jiang et al. (2022) hypothesized that exogenous Ca²⁺ might have reduced the toxicity of Pb through depositing Pb²⁺ in the cell wall, which might had nothing to do with soil properties. Relevant studies on exogenous Ca²⁺ mitigation of heavy metal stress in plants involved 11 plant species, as detailed in Table 6.

TABLE 6

Table 6 List of optimal concentrations of exogenous calcium used to alleviate heavy metal stress in different plants.

Acid rain stress

Exogenous Ca²⁺ has been tried and studied on for its possible application when plants are under an acid rain situation. So far, Ca²⁺ has proven to be effective through the mechanism I, III, IV and VI. Acid rain is defined as any precipitation with a pH less than 5.6 due to a large amount of acid substances accumulated in the atmosphere mainly through human activities. Damages caused by acid rain on plant leaves directly breakdown the protective surface of leaves, destroy the integrity of inner plant cell membranes, and cause the organelle dysfunction. A persisted and long duration of acid rain can lead to a serious and catastrophic impairments on plant structural compositions (Zhang et al., 2021), but there have been limited studies working on use of the exogenous Ca²⁺ to improve plant cell membranes. One of them indicated that exogenous Ca²⁺ increased the H - ATPase activity with the soybean plasma membrane, kept the membranes unharmed, and initiated the GmPHA1 gene expression to generate more nutrient uptakes such as N, P, K, and Mg to keep chlorophylls from degradation (Liang and Zhang, 2018). Exogenous Ca²⁺ was also found to change the quantity of different forms of calcium such as water-soluble organic calcium, calcium pectinate, and calcium phosphate in Brassica napus against the acid rain stress (Cong, 2018). Also, while being evaluated on six forest tree species, exogenous Ca²⁺ was able to reduce the negative effects of acid rain stress imposed on the seed germination, seedling growth, leaf chlorophyll content, and plant photosynthesis (Liu et al., 2011).

Some perspectives on future research

As we have discussed above, draught, flooding, salt, high and low temperature, heavy metals and acid rain are seven commonly encountered abiotic stresses and the plant responses to those stresses are somehow related to one or several structural, physiological, biochemical and/or molecular mechanisms pertaining to the plant tolerance. With this review, we have gained sufficient understanding of basic and various underlying mechanisms that are involved in plant stress tolerance through using exogenous Ca²⁺, however, more and thorough researches should focus on its mitigating effect and its associated tolerant genes and use them in crop breeding for more resilient varieties and cultivars against extreme abiotic conditions. Also, all abiotic stresses are variables and their impact on plant growth are different and difficult to predict, so plants would adjust themselves constantly to adapt those fluctuations, indicating the quantity, method and timing of using different type of exogenous Ca²⁺ can be critically important in maximizing the Ca²⁺ efficacy.

Mechanisms of the role of exogenous Ca²⁺ in plant resistance against abiotic stresses

Stabilization of cell wall and membranes

Stresses imposed on plants such as salinity, high temperature, low temperature, and drought tend to induce more reactive oxygen species (ROS) that cause a peroxidation of cell walls and membranes and change the membrane permeability, resulting in an osmotic disturbance. While being applied, exogenous Ca²⁺ mainly reduced the ion leakage (Min et al., 2021), replenished the lost Ca²⁺, induced the synthesis of osmoregulatory substances (Hu et al., 2012; Naeem et al., 2020), increased antioxidant enzyme activities such as superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) et al., (Upadhyaya et al., 2011), and promoted biosynthesis of glutathione (GSH), ascorbate, tocopherols, and other non-enzymatic antioxidants (Ashraf, 2009; Elkelish et al., 2019). All these biological and physiological responses, secondary metabolites and pertaining enzymes have proven to maintain the stability and integrity of plant cell walls and membranes. For example, exogenous Ca²⁺ would facilitate the accumulation of gamma-aminobutyric acid (GABA) and free polyamines (PAs) to alleviate cell membrane damage (Yin et al., 2015), mitigate the decline of unsaturated lipids incorporated in cell membranes through producing and supplying more unsaturated fatty acids as for retaining membrane fluidity (Liang et al., 2021), and combine with phosphate, organic phosphorus, and carboxyl groups of proteins on the cell surface to stabilize the cell membrane structure and maintain cell integrity (Hu et al., 2018).

Regulation of the Na⁺/K⁺ ratio

Both Ca²⁺ and K⁺ are ions necessary in plants for the protein synthesis, antioxidant enzyme activity, and maintenance of plasma membranes and cell walls (Assaha et al., 2017) and it has been consented that the Na⁺/K⁺ ratio is mainly regulated in response to salt stress and the key factor for plants to tolerate salt stress is to keep the Na⁺/K⁺ ratio low (Shabala and Pottosin, 2014). Ca²⁺ incorporated in the plasma membrane in plants under a salt stress is replaced by a large amount of Na⁺ that are usually available due to an excessive NaCl influx, leading to an increase in cell membrane permeability and causing an intracellular K⁺ extravasation, a high Na⁺/K⁺ ratio, and an insalubrious ionic balance (Cabot et al., 2014). An administration of exogenous Ca²⁺ cannot only control the Na⁺ entry into plants through non-selective cation channel (NSCC), reduce K⁺ efflux or leakage through both NSCC and the guard cell outward rectifying potassium channels (GORK), but also increase antioxidant enzyme activities and quantity of osmoregulatory substances to reduce the ROS accumulation that opens NSCC for ion leakage and keeps the ion homeostasis balanced in stressed plants (Rahman et al., 2016). In addition, a recent research has indicated that the salt overly sensitive (SOS) pathway was initiated by the enhanced Ca²⁺ signals that were stimulated by exogenous Ca²⁺, which promoted a Na⁺ efflux and more K⁺ uptakes through the SOS pathway in wheat (Gao et al., 2021).

Regulation of hormone levels in plants

Plant growth, development and reproduction are basically regulated by endogenous hormones and their fluctuations in plant can be influenced by and responded to changes of environment conditions (Mesejo et al., 2013). Ca²⁺ censors include calmodulins (CaMs), CaM-like proteins (CMLs), calcineurin B-like proteins (CBLs), and CDPKs. The Ca²⁺ sensor is an initial stress signal detector as well as a regulator of major plant hormone signals (Ku et al., 2018). Ca²⁺ is reportedly involved in the ABA-induced stomatal closure process (Liu H et al., 2022), with which ABA is participated in the initiation and release of Ca²⁺. In addition, both Ca²⁺ and ABA regulating kinases target the same metabolic pathway (Edel and Kudla, 2016) through regulating the biosynthesis and signal transmission of jasmonates (JAs) that subsequently adjust the Ca²⁺ level, inducing an influx of extracellular Ca²⁺, and temporarily increase its concentration in the nucleo plasma. So, Ca²⁺ signal is regarded as the most important messenger in the signal cascade (Wang X et al., 2019). Ca²⁺ can control the transport rate of Indole-3-acetic acid (IAA) and switch the direction of IAA flow to effectively amply Ca²⁺ signaling for activation of cation pumps in the plasma membrane, promotion of Ca²⁺ influx and K⁺ efflux, and induction of root gravity by interacting with IAA (Vanneste and Friml, 2013). However, the Ca²⁺ molecular basis of mechanisms involved in the signaling, Jas pathway, IAA biosynthesis are still poorly understood. Under adverse conditions, exogenous Ca²⁺ proved to alleviate potentially damaging effects caused by the stress on plant growth and development through minimizing the ABA amount and increasing the production of other hormones (e.g., IAA, GA, CTK, etc.) to enhance plant resilience under stress (Liu et al., 2017; Kamran et al., 2021; Wu et al., 2022). At present, fewer studies of exogenous calcium on its effect on changes of a variety of plant hormones have been reported but mainly focused on ABA fluctuations and their associated impacts.

Maintenance of photosynthesis

Plants needs the chlorophyll as an life-supporting pigment for photosynthesis, and its quantity in plant leaves directly affects the photosynthetic capability to produce carbohydrates (Wu et al., 2019). Adversary stresses tend to impair the chloroplasts and cause a decrease in the chlorophyll quantity. Exogenous Ca²⁺ could prevent or minimize chlorophyll breakdowns, keep chloroplasts intact under stresses, and maintains a sufficient number of photosynthesis pertaining pigments and organelles in in leaves (Min et al., 2021; Wang et al., 2022). Ca²⁺ plays an important role in plant stomatal regulation as the second messenger in coupled with external signals in plant cells. Appropriate amount of Ca²⁺ can make plants adapt to abiotic stresses such as drought and salinity quickly by adjusting their stomatal opening/closing, optimizing their gas exchange, and improving their photosynthetic efficiency (Li et al., 2012; Li et al., 2022a). These plant adjustments and adaptations by using exogenous Ca²⁺ could be achieved through reshape, rearrangement and configuration of stomata during their differentiation and development for more efficient of gas exchange and water utilization (Zhang et al., 2019a). Moreover, adding exogenous Ca²⁺ to increase Ca²⁺ level improved the lutein cycle (Yang et al., 2013), mitigated the adversary effects on the photosystem II (PSII) inhibition, and preserved enzyme activities, reduced accumulations of carbohydrate, and uphold a normal plant photosynthesis (Tan et al., 2011).

Regulation of plant respiratory metabolism and improvement of root activities

Flooding causes anoxia of plant roots and weakens the respiratory metabolism. The stress due to flooding-initiated lack of oxygen can be lessened by the application of exogenous Ca²⁺ to improve the catalytic capacity of pentose phosphate and produce more ATP and NADPH to provide more energy for the plant respiratory metabolism (Yang et al., 2016), to promote the activity and accumulation of mitochondrial antioxidant enzymes relating to the glycolysis and tricarboxylic acid cycle (He et al., 2015), and to reduce the content of acetic acid, acetaldehyde and the activity of LDH for less lactic acid metabolism (Fan, 2019). Exogenous Ca²⁺ also proved to facilitate absorption of nitrate and accelerate its conversion into amino acids, heat stable proteins or polyamines to survive from hypoxia (Gao et al., 2011). In addition, some studies on plant salt stress also pointed out that exogenous Ca²⁺ can improve the root vitality by reducing the relative electrolyte leakage of the root, thus to improve the flooding tolerance of foxtail millets (Han et al., 2019). According to the summary of current literature, this mechanism mainly plays an active role under flooding stress, and whether it can also be activated under other stresses is unclear.

Induction of gene expressions and protein transcriptions for the stress resistance

While under the abiotic stress, the molecular mechanisms involved in plant stress tolerance are more complex and multi-layered, including stress sensing, responsive signaling, gene transcription, protein translation, and post-translational protein modification. Under various abiotic stresses, exogenous Ca²⁺ induces or activates a series of gene expressions and tolerant protein transcriptions to adjust and adapt to adversities accordingly. These research advances in that regards include but are not limited on: 1) upregulating the expression of antioxidant enzyme-related genes such as EnAPX, EnCAT2, EnGPX and stress-related genes to improve cold resistance of Elymus nutans (La-mu et al. 2021); 2) promoting the synthesis of plant proteins and preventing proteins from degradation through boosted activities of nucleoside diphosphate kinase (NDPK) and antioxidant enzymes and reduced expressions of heavy metal-related structural domain proteins such as PCR1, HMA2 and HMA4l (Zeng et al., 2017); 3) cutting down the Cd uptake of plants and promoting the Ca²⁺ internal mobility (Zeng et al., 2017); 4) stimulating ACO-1, ADH-1, CAT-2, and PK gene expression to alleviate the damage of pepper plants under flooding stress (Ou et al., 2017), and 5) inducing the expression of photosynthetic genes and stabilizing photosynthetic membrane proteins in leaves (Zhang et al., 2014). Due to the differences of gene pools in different plant species and the difficulties in monitoring those genes, the information we currently have on plant genomes is still limited, focusing only on detecting gene expressions and reflecting Ca²⁺ associated genetic changes after application of exogenous Ca²⁺, but how exactly these adjustments are induced, operated and regulated remain to be explored. In addition, how exogenous Ca²⁺ transduces Ca²⁺ signaling pathway in plants has not been determined yet.

Summary and outlook

With an extensive review of over one hundred research papers, we have sorted them according to their major mechanisms into six categories associated with the plant membranes, Na⁺ vs. K⁺ ratios, hormone regulation, gene expression and protein transcription, and photosynthesis. However, we tend to believe that this type of grouping is arbitrary, simplified and nonscientific only for the purpose of easy access and preliminary understanding of a particular aspect of main functions of exogenous Ca²⁺ that may have alleviated a certain type of plant stresses. The mechanisms involved in mitigating plant abiotic stresses through application of exogenous Ca²⁺ and their reported interrelationships are proposed and demonstrated (Figure 2) and we strongly suggest that they be perfected and completed with more fundamental information and advanced findings are available.

FIGURE 2

Figure 2 Plant self-responses to abiotic stresses and mechanisms of exogenous calcium involved in enhancement of plant stress tolerance. The red and green arrows indicate a promotion/increase or an inhibition/decrease, respectively.

In the process of reviewing all relevant literature, we have found that most of the studies only explored one or a few aspects of stressed plants in response to exogenous Ca²⁺ added to alleviate a stress, but the application of exogenous Ca²⁺ may have a potential to affect multiple structural, biological and physiological functions or metabolic pathways at the plant cellular level to defend plants from various stresses. Likewise, exogenous Ca²⁺ could be used with other exogenous substances to enhance plant defensiveness against one or multiple stresses that are related or associated with each other to intensify the adversary impact, such as the stress from drought, high temperature and high salinity since they are somehow correlated. Other studies have shown that exogenous Ca²⁺ is more effective when combined with other exogenous substances, which should be our research directions and objectives for our endeavor in using exogenous Ca²⁺ in the near future (Vafadar et al., 2020; Valivand and Amooaghaie, 2021). Therefore, more and more well-designed experiments to unearth the true underline mechanisms of exogenous Ca²⁺ in mitigating multiply correlated plant abiotic stresses are expected and the results derived from them should significantly help us understand how to effectively use of exogenous Ca²⁺.

It has come to a consensus that exogenous Ca²⁺ can be used to alleviate various abiotic stresses on plants through an application of leaf spray, hydroponics, seed dipping, drenching, and soil application. To avoid possible interference of NO₃^- and other nutrient anions to the experimental results, most of the existing studies on exogenous Ca²⁺ used CaCl₂ as the source calcium for a foliage spraying or through hydroponics. However, with the studies of the heavy metal stress, exogenous Ca²⁺ such as Ca(OH)₂ was mostly used in the form of mixing it into the medium or soil (Zu et al., 2020) to increase soil pH, reduced the toxicity of heavy metals, and boost the Ca²⁺ quantity both in soil and plants. In addition, different calcium anions also affect plant growth. For example, the application of exogenous CaCl₂ on chloride-phobic cowpea plants under stress could cause the accumulation of Cl^- in roots and affect the normal growth (Guimarães et al., 2011), which in turn interferes with a positive mitigating effect of Ca²⁺. Therefore, the research in the future should be needed as well to investigate the type of exogenous Ca²⁺ that is suitable for the growth and development of a specific crop with an attention to determine the amount of the usage based on the type and extent of adversary stresses.

At present, majority of the experimental studies have been carried out indoors and mainly on the plant seed germination or seedlings, however, we believe that the best way to evaluate the effect of exogenous Ca²⁺ for a practical and feasible application should be carried out in an actual crop production site to determine its mode of action, actual concentration and optimal time for application, etc., or if priming of plant seedlings for their fortified and prolonged tolerance against abiotic stresses really words in field trials.

In summary of most recent advances on exogenous Ca²⁺ applications to alleviate various plant stresses, some questions still remain unanswered in terms of: 1) how Ca²⁺ is further transported and translocated after it enters a plant; 2) how efficiently Ca²⁺ is actually utilized to function as a mitigating factor; 3) in which way the Ca²⁺mobility can be improved; 4) how to use modern molecular assays to reveal detailed and Ca²⁺-induced mechanisms pertaining to the plant tolerance against abiotic stresses; 5) what are the interactions between different biological and physiological mechanisms that are all modulated by gene expressions and protein transcriptions at the molecular level; and 6) to what degree each of the abiotic stresses causes an irreversible and permanent damage. To address those challenging questions, the modern molecular techniques and more sophisticated analytic instruments such as an fluorescence tracing technique and a laser scanning confocal microscopy analysis technique (He et al., 2015) should be used for a quantitatively and qualitatively detection of a series of changes in signaling and gene expression induced by exogenous Ca²⁺. With this review, we have sorted a series of complex physiological and biochemical responses and their underline mechanisms that were reported recently, but much more deserve further exploration by researchers to develop a low-cost and effective way to combat all kinds of stresses though using exogenous Ca²⁺.

Author contributions

Conceptualization: DF. References analysis: XW. Funding acquisition: DF. Methodology: DF, XW. Validation: DF, XS. Writing–original draft: XW, DF, JG. Writing–review & editing: XS, CZ, HL, PL. All authors contributed to the article and approved the submitted version.

Funding

This study was supported by the Natural Science Foundation of Shandong Province (No. ZR2021ME154).

Acknowledgments

We thank Nankai University and Tianjin Tianlong Technology Co., Ltd. for their joint effort in training of DF with a postdoctoral position. Our appreciation is also extended to PL with the College of Art, Weifang University of Science and Technology for her art work in completion and perfection of all figures in the manuscript.

Conflict of interest

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

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

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