1. Ca²⁺ Signaling and Plant Thermotolerance

The rapid rise in CO₂ levels on Earth is causing global warming, leading to more frequent extreme high-temperature (HT) events. Heat is a major factor in reducing crop yields. It disrupts homeostasis, affects seed germination, and alters (and ultimately stunts) plant growth [1]. Without sufficient adaptation, genetic enhancements, and fertilization, every one degree Celsius increase in global mean temperature could lead to significant reductions in global wheat, rice, and maize yields (averaging 6.0%, 3.2%, and 7.4%, respectively) [2]. Therefore, understanding the molecular mechanisms underlying plant responses to HT stress is vital for improving agricultural production and ensuring future food security.

HT can elevate the intracellular concentration of calcium (Ca²⁺), a common second messenger in both animal and plant cells. Plants exposed to HT can experience heat shock (HS), which triggers a rise in cytosolic Ca²⁺ and disrupts the oscillations in Ca²⁺ levels [3]. Ca²⁺ plays a critical role in maintaining the normal physiological functions of plant cells and is involved in various physiological processes in plants. Additionally, as a ubiquitous second messenger, Ca²⁺ participates in plant responses to various stressors. Thus, understanding the impact of Ca²⁺ on plant thermotolerance is essential for the development of heat-resistant crops [4, 5].

Ca²⁺ is a versatile intracellular signal; information is encoded based on temporal and spatial patterns of Ca²⁺ concentration changes. These patterns are decoded by Ca²⁺-sensing effectors such as Ca²⁺-permeable channels and Ca²⁺-binding proteins to initiate specific cellular responses [5]. The induction of the Ca²⁺ signal represents the most rapid response to elevated temperatures in plants. In one study, the cytosolic Ca²⁺ concentration in wheat peaked within 10–15 min of a sudden temperature increase from 24 to 36 °C before returning gradually to baseline as the HS response (HSR) continued [6].

Ca²⁺ entry into the cytoplasm is facilitated by several families of protein channels, including cyclic nucleotide-gated channels (CNGCs), glutamate (Glu) receptor-like channels (GLRs), annexins, and mechanosensitive (MS) channels. Each of these channel types plays a crucial role in promoting an influx of Ca²⁺. Furthermore, plants possess various Ca²⁺-binding proteins that decode and transmit the primary Ca²⁺ signal to elicit specific cellular responses. These proteins include calmodulins (CaMs), CaM-like proteins (CMLs), Ca²⁺-dependent protein kinases (CDPKs or CPKs), Ca²⁺- and CaM-dependent protein kinases (CCaMKs), calcineurin B-like proteins (CBLs), and CBL-interacting protein kinases (CIPKs). When these proteins bind Ca²⁺, they undergo conformational changes that allow them to initiate downstream signaling events via interactions with other proteins or molecules. This mechanism enables plants to translate variations in the intracellular Ca²⁺ concentrations into specific cellular responses, including changes in gene expression, enzyme activity, or ion channel activity [7-9].

Recent studies have focused on understanding how plants detect Ca²⁺ increases due to HS, and many studies have identified crucial molecules and signaling pathways involved. Here, we review the latest findings on thermosensing in different crop species.

2. Ca²⁺-Permeable Channels Perceive Elevated Temperatures

Presently, the identity of a definitive thermosensor in plants remains elusive. It is hypothesized that Ca²⁺ channels located in the plasma membrane (PM) are crucial players in perceiving elevated temperatures. These channels could be activated directly or indirectly, leading to increased cytoplasmic Ca²⁺ levels. Consequently, thermosensors may function as Ca²⁺ channels, directly modulating Ca²⁺ signaling in response to external stimuli. Alternatively, they may act as regulatory elements that influence the membrane lipid composition, which is closely linked to Ca²⁺ channel activity. Another possibility is that they operate as GLRs, initiating an influx of Ca²⁺ in response to external stimuli.

Genome sequencing has revealed that plants lack typical animal Ca²⁺ channels such as voltage-dependent Ca²⁺ channels, transient receptor potential channels, purinergic P2X receptor channels, and cysteine loop channels. Instead, they have expanded families of CNGCs, GLRs, annexins, reduced hyperosmolarity-induced [Ca²⁺] increase channels (OSCAs), “Mid1-complementing activity” channels (MCAs), two-pore channels (TPCs), MS-like channels (MSLs), and Piezo channels (MSPs). In the context of HSR, we will explore several potential candidates among these Ca²⁺-permeable ion channels (Figure 1).

Figure 1. calcium (Ca²⁺) channels involved in sensing heat. (By Figdraw).

2.1. Heat Sensing via CNGCs

CNGCs are non-specific cation channels that regulate the flow of Ca²⁺ by binding to ligands such as cAMP and cGMP. CNGCs are activated in response to various abiotic and biotic stresses [10, 11]. Plant and animal CNGCs belong to the K-selective shaker channel family and share similarities in their amino acid sequences and overall structures [12]. They possess cyclic nucleotide-binding domains and one or more CaM-binding domains at their cytosolic N- and C-termini [13, 14].⁺

HS induces PM fluidization, allowing an influx of Ca²⁺ into the cytoplasm. Furthermore, nucleotide cyclases can elevate cAMP and cGMP levels under HS conditions, further promoting the influx of Ca²⁺ and activating associated signaling pathways. CNGCs were initially discovered in barley [15]; subsequent studies identified 20 and 16 CNGCs in the genomes of Arabidopsis and rice, respectively [16, 17]. Currently, plant CNGCs are known to participate in a range of biological processes [18-21].

2.2. Heat Sensing via GLRs

In mammals, ionotropic Glu receptor cation channels (iGluRs) respond to the neurotransmitter Glu, initiating Ca²⁺ signal cascades [22]. The first evidence of Glu signaling in plants was uncovered by Lam et al. [23], who identified the AtGLR gene family in Arabidopsis. Through sequence analysis and comparisons, homologous Glu receptor variants have been identified in dicot and monocot species [24-26]. The Arabidopsis genome contains 20 GLRs, while the rice and poplar genomes harbor 13 and 61 GLRs, respectively [27, 28]. Plant GLRs display significant sequence and structural homologies with animal iGluRs, including high degrees of amino acid sequence identity in their channel and ligand-binding domains [29].

2.3. Heat Sensing via Annexins

Annexins, an evolutionarily conserved family of proteins present in a variety of organisms, are renowned for their ability to bind to Ca²⁺ and phospholipids. They play pivotal roles in a plethora of cellular processes [30, 31]. Annexins exhibit peroxidase and ATPase/GTPase activities and are associated with the regulation of Ca²⁺ channels [32]. Their functions encompass a wide range of intracellular and extracellular phenomena, including vesicular trafficking, organization of the membrane–cytoskeleton, exocytosis, endocytosis, phagocytosis, ion channel regulation, and apoptosis [33]. The genomes of Arabidopsis, rice, and wheat contain 8, 10, and 25 annexin genes, respectively [34-36]. Annexins feature a conserved protein core domain capable of binding both Ca²⁺ and phospholipids alongside an N-terminal domain that varies in sequence and length among different annexins [37].

In plants, annexins participate in environmental stress responses, and they play roles in growth, development, and signaling [38]. Some plant annexins regulate the level of free cytosolic Ca²⁺, and certain annexins can form Ca²⁺-permeable channels in lipid bilayers or vesicles [39]. Moreover, plant annexins may possess peroxidase activity or ATPase/GTPase activity, each contributing to functional specificity [40]. Annexins play a broad regulatory role in diverse biochemical and cellular processes, including Ca²⁺ channel regulation, and in plant growth, development, and biotic and abiotic environmental stress responses [40].

2.4. Heat Sensing via OSCAs

Recently discovered MS Ca²⁺ channels called OSCAs have the ability to detect and respond to changes in osmotic pressure, regardless of whether it originates externally or internally. OSCAs are essential for regulating the flow of Ca²⁺ in plants; thus, they play a crucial role in plant growth and adaptation to environmental stress. OSCA1, the first OSCA identified in Arabidopsis thaliana, is responsible for raising cytosolic Ca²⁺ levels by triggering an influx of Ca²⁺. In fact, this channel is responsible for the increase in intracellular Ca²⁺ triggered by multiple stimuli in plants [41]. In total, 15, 11, 12, and 62 OSCA genes have been identified in Arabidopsis [41], rice [42], maize [43], and cotton [44], respectively.

2.5. The Functions of MSLs, MCAs, and MSPs in Plants following HT Treatment

In addition to OSCAs, plants possess several other types of MS ion channels, including MSLs, MCAs, and MSPs. These channels are permeable to Ca²⁺ and play crucial roles in enabling plants to respond to mechanical stimuli and changes in osmotic pressure.

MSLs are MS ion channels found in both bacteria and plants. In Arabidopsis, MSL2 and MSL3 are essential to protect plastids against bursting inside leaf epidermal cells during growth under conditions of high osmotic pressure [45]. MSL8 responds to PM distortion during pollen grain rehydration and germination [46]. Additionally, MSL10 and MSL9 exhibit MS ion channel activity in root protoplasts [47]. In rice, most OsMSL genes are expressed during reproductive growth, suggesting their involvement in plant growth, development, and stress responses [48].

While the direct involvement of these channels in the HSR has not been extensively studied, their potential role in such responses warrants further investigation.

3. Ca²⁺-Binding Protein Involvement in the HSR

Under HS conditions, the intracellular Ca²⁺ concentration in plants increases, primarily due to an influx of Ca²⁺ from outside the cell or the release of Ca²⁺ from intracellular stores [49, 50]. This rise serves as a pivotal “signal” that triggers a complex signal transduction cascade. This signal, in conjunction with downstream effector proteins, including CaMs, CMLs, CBLs, and CDPKs/CPKs, serves as a molecular code that must be interpreted by the cell. Together, these proteins create a sophisticated signaling network that transmits stress signals and orchestrates a multitude of responses in plants [51]. In this section, we will concentrate on candidate Ca²⁺-binding proteins that were reported to be involved in the HSR in crops.

3.1. CaMs in HS Signaling

CaMs, highly conserved sensor proteins containing EF-hand motifs, are found in various plant organelles. In total, 9, 5, and 8 CaM genes have been identified in Arabidopsis [52, 53], rice [54], and maize [55], respectively. CaMs are ubiquitously expressed in all eukaryotic cells and possess a dumbbell-shaped structure. They are multifunctional, consisting of two globular lobes at the N- and C-termini connected by a flexible central linker. Each lobe contains a pair of EF-hand motifs capable of binding Ca²⁺ ions with positive cooperativity [56]. The EF-hand motif in CaM is characterized by a helix–loop–helix (D-X-D) conformation, consisting of 12 amino acid residues, totaling 36 amino acid residues across both motifs. In the D-X-D motif, the 14th and 16th positions are fixed, while the 15th position can be occupied by any amino acid [57]. These motifs are involved in interactions with a diverse array of downstream target proteins, including ion channels, pumps, antiporters, kinases, phosphatases, transcription factors, and enzymes involved in metabolic pathways. Arabidopsis CaM isoforms CaM1/4, CaM2/3/5, CaM6, and CaM7 were found to bind to CNGC6 to varying degrees, and this binding was dependent on the presence of Ca²⁺ and IQ6, an atypical isoleucine–glutamine motif in CNGC6. Knockout of CaM2, CaM3, CaM5, and CaM7 genes led to a marked increase in PM inward Ca²⁺ current under HS conditions; however, knockout of CaM1, CaM4, and CaM6 genes had no significant effect on PM Ca²⁺ current [58].In some instances, these motifs function as transcription factors, recognizing and binding to target genes, thereby modulating stress responses in plants.

3.2. CMLs in HS Signaling

CMLs differ from CaMs in their length and the number of EF-hand motifs they possess. While CaMs typically contain four EF-hand motifs, CMLs can have varying numbers, ranging from one to six. CMLs are termed “CaM-like” due to their 15% amino acid identity with CaM. These proteins play a crucial role in physiological responses to various stresses, including salinity, drought, heat, and cold. In Arabidopsis, 50 CMLs have been identified, compared with 32 in rice [59].

3.3. CDPKs in HS Signaling

CDPKs, or CPKs, belong to a class of protein kinases that possess four C-terminal EF-hand motifs, which enable them to sense changes in intracellular Ca²⁺ levels. CDPKs are effector proteins that play pivotal roles in regulating a wide range of physiological processes, including environmental stress responses, in various plant cell types [60]. CDPKs consist of several domains, including a variable N-terminal domain, a serine/threonine protein kinase domain, an autoinhibitory junction domain (JD), and a C-terminal CML regulatory domain (CaMLD) connected by a tether. The CaMLD is composed of four EF-hand Ca²⁺-binding motifs. At low Ca²⁺ concentrations, the C-lobe of a CDPK already contains Ca²⁺ and interacts with the JD, stabilizing its conformation. The JD forms a helical structure that blocks substrate access by being buried within the active site of the kinase domain due to an intramolecular interaction. When the concentration of Ca²⁺ rises, both the N-lobe and C-lobe of the CaMLD interact with the JD, leading to a substantial conformational change that releases the active site [61].

The CDPK family is diverse, with multiple members and isoforms across plant species. Recent whole-genome expression analyses have shed light on the transcriptional regulation of CDPKs in response to various stresses, including HS, in important crop species [62-67]. These findings provide valuable insight into the functional roles of CDPKs and their potential utility in enhancing the thermotolerance of crops.

3.4. CBLs and CIPKs in HS Signaling

CBLs comprise a distinct family of Ca²⁺ sensors in plants with essential roles in Ca²⁺ signaling pathways. Specifically, they interact with and modulate the activity of CIPKs. CBLs bear resemblance to the calcineurin B-subunit in yeast and neuronal Ca²⁺ sensors in animals [68]. CBLs possess four EF-hands, which are Ca²⁺-binding motifs found in various proteins. EF-hands are structural domains characterized by a D-X-D structure, with the loop region serving as the Ca²⁺-binding site. These domains allow proteins to function as Ca²⁺ sensors that can respond to changing levels of intracellular Ca²⁺. In the case of CBLs, the four EF-hand domains facilitate the capture of Ca²⁺ ions, enabling them to play pivotal roles in numerous plant physiological processes [69]. Notably, CBLs lack intrinsic kinase activity. To transmit signals, they must form complexes with CIPKs, which are serine/threonine kinases found in plants. CIPKs possess a functional kinase domain but remain in an inactive state because of the autoinhibition caused by an interaction between the kinase domain and regulatory domain. An inhibitory motif known as NAF/FISL blocks the active site in CIPKs, preventing substrate binding and subsequent phosphorylation. This autoinhibitory mechanism keeps CIPKs in an inactive state until they are activated by binding to a CBL. Once active, the CIPK can regulate downstream proteins. This activation process is crucial for the proper functioning of the CBL–CIPK signaling pathway in plants [70]. When plants encounter stress, such as HS, the intracellular concentration of Ca²⁺ rises. This increase enables Ca²⁺ ions to bind to the EF-hand motifs in CBLs. This binding promotes the interaction of CBLs with the NAF/FISL element in CIPKs. Consequently, the CIPKs become active and can participate in stress response pathways by phosphorylating downstream proteins.

4. Ca²⁺ Signaling Networks Mediate the Plant HSR

Ca²⁺ are ubiquitous second messengers in eukaryotes, participating in a wide array of signaling pathways and responses to various environmental conditions. As mentioned above, when plants experience HS, the cytosolic Ca²⁺ concentration rises because of an influx of Ca²⁺ facilitated by membrane-localized Ca²⁺ permeable cation channels. These ions subsequently bind to Ca²⁺-binding proteins, initiating signal transmission to their respective downstream pathways. In recent years, substantial progress has been made in understanding the mechanisms related to thermotolerance in plants.

The HSR signaling pathways in plants include the Ca²⁺ dependent, ROS, NO, HSF-HSP, HSF-independent, hydrogen sulfide (H₂S), and unfolded protein response (UPR) pathways, etc. [4, 71]. There are interactions and crossovers between different HS pathways. For example, the Ca²⁺ signaling may intersect with the ROS, NO, and HSF-HSP pathways, forming a complex signaling network [4]. Additionally, in the HSF-independent pathway, Ca²⁺ might contribute to the activation of certain transcription factors independent of HSF [72, 73]. The H₂S pathway introduces a novel dimension, suggesting that Ca²⁺ may modulate signaling events in conjunction with H₂S [74, 75]. The association of Ca²⁺ with endoplasmic reticulum (ER) stress responses suggests a potential link between Ca²⁺ and UPR [76, 77]. These propositions underscore the versatility of Ca²⁺ signaling and its potential contributions to diverse HSR pathways in plants. Future research is needed to experimentally validate these hypotheses and enhance our understanding of the intricate molecular mechanisms governing plant responses to HS.

In this section, we consider several potential downstream pathways of Ca²⁺ in response to HS in plants (Figure 2).

Figure 2. Ca²⁺ signaling pathway under heat shock (HS) (By Figdraw).

5. Conclusions and Perspectives

In addition, the complex interplay of signaling pathways, including Ca²⁺, NO, ROS, and others, deserves further investigation. Based on the above-mentioned research gaps, future research should prioritize the following areas: (1) Integration of existing pathways. There is a need to integrate various fragmented pathways into a unified primary Ca²⁺ signaling pathway associated with HS. This endeavor could result in a more comprehensive understanding of the role of Ca²⁺ signaling in heat resistance. (2) Identification of new components. Ongoing efforts should focus on identifying new components that sense Ca²⁺ signals induced by HS. This continuing exploration will contribute to an improved understanding of the HSR pathway in plants. (3) Ca²⁺ crosstalk. Understanding the crosstalk between Ca²⁺-mediated HSR and other stress-signaling pathways is essential. This knowledge can shed light on the broader regulatory network that governs plant responses to multiple stressors.

A deeper understanding of the molecular mechanisms may enable the identification of key genes and pathways so as to provide targets for genetic engineering. Moreover, marker-assisted selection, next-generation molecular breeding, precision breeding, and genome editing techniques represent powerful tools to enhance the efficiency of plant breeding programs. These methods will allow breeders to select plants with desirable traits more accurately and quickly and speed up the development of crops better suited to elevated temperatures. These improvements will be conducive to promoting sustainable agriculture.

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