Calcineurin B-like Proteins in Plants under Salt Stress: History
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Contributor:
Oluwaseyi Setonji Hunpatin
,
Guang Yuan
,
Tongjia Nong
,
Chuhan Shi
,
Xue Wu
,
Haobao Liu
,
Yang Ning
,
Qian Wang

Salinity stands as a significant environmental stressor, severely impacting crop productivity. Plants exposed to salt stress undergo physiological alterations that influence their growth and development. Meanwhile, plants have also evolved mechanisms to endure the detrimental effects of salinity-induced salt stress. Within plants, Calcineurin B-like (CBL) proteins act as vital Ca2+ sensors, binding to Ca2+ and subsequently transmitting signals to downstream response pathways. CBLs engage with CBL-interacting protein kinases (CIPKs), forming complexes that regulate a multitude of plant growth and developmental processes, notably ion homeostasis in response to salinity conditions.

  • salinity
  • salt stress
  • calcineurin B-like proteins
  • CBL-interacting protein kinases
  • salt tolerance

1. Introduction

Salinity is a severe factor affecting the yield of crops [1]. The buildup of excess soluble salts like Na+ and Cl− in the soil is what causes salinity [2]. Saline soil can be practically identified when the electrical conductivity (EC) of the soil sample from the selected area is greater than 4 dSm−1 and the exchangeable Na+ concentration is 15% [3]. At this point, the soil has a NaCl concentration of around 40 mM. According to the Food and Agricultural Organization (FAO), industrialization, excessive fertilization, increased use of irrigation water of poor quality, soil salinization, and natural causes like salt intrusion in coastal zones as a result of rising sea levels are all contributing factors that will cause salinity to affect about 20% of agricultural farmland significantly more in the coming years [4]. There has been an increase in the emigration of farmers from coastal areas [5], which is proof that soil salinity has far-reaching effects, not only on plants but also on humans who benefit directly or indirectly from plants’ productivity. Salt stress affects plants in several ways, and chief among them is a decline in growth and development [6][7]. Researchers are seeking ways to alleviate the impact caused by salt.
Being stationary organisms, plants have evolved mechanisms to sense environmental cues such as salt stress and respond accordingly for adaptation. Perception of these stimuli always triggers the creation of temporary changes in cytoplasmic calcium ion concentration, known as Ca2+ signatures [8][9]. This Ca2+ signature plays a crucial role in the signaling transduction processes of stress tolerance in plants. Various proteins, such as Calcium-dependent protein kinases (CDPKs), Calmodulin-like proteins (CMLs), Calmodulins (CAMs), and Calcineurin B-like proteins (CBLs), serve as calcium sensors that recognize Ca2+ signatures in plant cells and finally trigger transcriptional and metabolic responses to these stresses by modifying the downstream protein targets [10][11].

2. Effects of Salt Stress in Plants

The effects of salt stress in plants can be detrimental and manifest at multiple levels, from molecular and physiological to morphological and ecological.

2.1. Phenotypes of Salt Stress in Plants

Salt stress hinders cell expansion and division in plants, resulting in diminished growth and overall biomass [12][13]. Elevated salt levels induce leaf chlorosis, causing the leaves to be yellow or brown due to disrupted chlorophyll synthesis, alongside leaf withering and abscission [14]. Plants undergoing salt stress often display modifications in root architecture, such as reduced root length, fewer lateral roots, and increased root diameter, aiming to enhance water and nutrient absorption from the soil [15][16]. Salt stress also changes the gravitropism of the root system [17]. Reproductive development is adversely impacted by salt stress, leading to a reduction in flowering, fruit set, and seed yield [18][19].

2.2. Physiological Effects of Salt Stress in Plants

Salt stress causes osmotic and ionic stresses which are the consequences of limited water uptake by plants growing in saline soil [20] (Figure 1).
Figure 1. A schematic diagram showing the physiological impacts of salt stress in plants.
Osmotic stress: The buildup of salts in the soil increases the osmotic potential of the soil solution. This means that the water potential in the soil is reduced, making it more difficult for plants to take up water from the soil [21]. Osmotic potential is a measure of the ability of a solution to draw water into itself [22]. In a saline environment, the osmotic potential of the soil solution is less than that of the plant cells. As a result, water from the plant cells moves towards the soil, causing dehydration and reducing turgor pressure within the plant cells. Due to the higher osmotic potential in the soil (lower water potential), water is less available to the plant roots. Plants need to exert more energy to absorb water against this osmotic gradient. The reduced water uptake leads to the dehydration of plant cells. Dehydration affects various cellular processes, including photosynthesis, enzyme activity, and metabolism [23][24]. It also disrupts the normal expansion necessary for growth and development. The effects of a water deficit in plants include diminished cell turgor and reduced water usage efficiency [8]. Turgor pressure refers to the pressure exerted by the contents of a cell against its surrounding cell wall. When cells lose water due to reduced water uptake, turgor pressure decreases.
Ionic stress: Ionic stress occurs as a result of the accumulation of salts, particularly Na+ and Cl−, in the plant tissue [25]. This disrupts the normal ionic balance and homeostasis within the plant cells, leading to various physiological and metabolic disturbances. Plants absorb water and essential nutrients, including ions, from the soil through their roots. Under normal conditions, plants maintain a delicate balance of ions, such as K+, Ca2+, and Mg2+, to ensure proper cellular functions and water uptake. However, in a saline environment, the concentration of Na+ and Cl− increases, upsetting the balance. Elevated Na+ levels can cause toxicity in plants [26] and can hinder critical processes like enzyme activation, photosynthesis, and osmotic regulation [20][21][24].
Oxidative stress: Reactive oxygen species (ROS) buildup brought on by salt stress leads to oxidative damage in plants and causes oxidative stress [27]. In plants, ROS are manufactured in organelles like peroxisomes, chloroplasts, mitochondria, and the apoplast [28]. Leakage of electrons from the electron transport chain (ETC) during salt stress causes the production of mitochondrial ROS, which can then be transformed to H2O2 by Manganese Superoxide Dismutase Mn-SOD [29]. ROS are generated in peroxisomes as a result of increased photorespiration during salt stress and reduced photosynthetic activity in the chloroplasts during salt stress leads to the formation of ROS [30][31].

3. Plant Response to Salinity

Plants have also developed diverse adaptive mechanisms to respond to salinity stress, including osmotic adjustment, ion exclusion, antioxidant defense systems, and morphological adaptations.

3.1. Physiological Responses and Adaptations of Plants to Salt Stress

Plants have developed a variety of physiological responses and adaptations to mitigate the harmful impact of salt stress. They regulate stomatal conductance to reduce water loss during salt stress [32], which in turn lowers transpiration and helps in water conservation. Plants often respond to salt stress by closing their stomata, which helps minimize water loss but also reduces carbon dioxide uptake, which is essential for photosynthesis [21]. Additionally, plants utilize specific mechanisms to selectively uptake ions, such as Na+, and transport them to specific tissues, like older leaves or vacuoles, to prevent their accumulation in metabolically active tissues and maintain ion homeostasis [33].
To uphold cellular turgor and osmotic balance, plants accumulate compatible solutes [34][35]. These solutes serve as osmoprotectants, shielding proteins and cellular structures from the harmful impacts of increased salt concentrations. Plants may also undergo metabolic adjustments to effectively cope with salt stress [36], such as modifying enzyme activities, energy metabolism, and carbon partitioning to optimize resource utilization during adverse conditions.

3.2. Molecular Responses and Adaptations of Plants to Salt Stress

Plants undergo alternative splicing and post-translational modifications of proteins to adapt to salt stress [37][38]. These modifications modulate protein functionality, stability, and subcellular localization, enabling plants to fine-tune their response to salt-induced changes. Additionally, epigenetic alterations such as DNA methylation, changes in histone structure, and small RNA regulation play a role in influencing gene expression and stress responses [39]. The salt stress conditions can impact the epigenetic landscape of plants, potentially affecting gene expression and contributing to their adaptation to stress. In response to salt stress, plants increase the expression of genes linked to stress responses [40][41], ion transporters, osmotic regulation, and antioxidant defense systems. These genes collectively play a crucial role in enhancing salt tolerance by aiding in ion balance, osmotic adjustment, and ROS detoxification.

4. CBLs Function as Calcium Sensors in Plants

CBLs are a kind of calcium sensor exclusively found in plants and are upregulated in response to multiple environmental stresses [42]. Elongation factor (EF) hand domains serve as a distinctive feature in Ca2+ sensors, including proteins like calcineurin, calmodulins, and CBL. These EF-hands, with a typical helix-loop-helix secondary structure, play a crucial role in Ca2+ binding (Figure 2). Notably, the EF-hand domains in CBLs exhibit marked differences compared to Ca2+ binding proteins such as CAMs [43]. The first EF-hand domain in CBLs consists of 14 amino acids, contrasting with the 12 amino acids found in other Ca2+ sensors [44].
Figure 2. Structures of AtCBL2. (A) Amino acid sequence of AtCBL2 and the positions of three EF-hands predicted by SMART (B); The 3D structure of AtCBL2 predicted by SWISS-MODEL.
CBL proteins comprise four EF-hands, each characterized by a conserved α-helix-loop-α-helix structure that facilitates Ca2+ binding [45][46]. These EF-hands are strategically positioned at fixed intervals, covering distances of 22, 25, and 32 amino acids from EF1 to EF4, respectively [41][43]. The loop region displays a consensus sequence of 12 residues: DKDGDGKIDFEE [45][47]. Positions 1(X), 3(Y), 5(Z), 7(-X), 9(-Y), and 12(-Z) within this sequence play a key role in coordinating Ca2+ binding [45][46]. Variations in the amino acids at these specific positions can impact the affinity for Ca2+ binding [45][48]. It is noteworthy that EF1 in CBLs features a two-amino acid insertion between position X and position Y [42][46]. Interestingly, some CBLs have been reported to possess three EF-hands [49]. To date, Arabidopsis thaliana, a model plant, has revealed the presence of ten (10) CBLs [50][51].
CBLs do not act alone, but on binding to Ca2+, they interact with a kind of kinase named CIPK. CIPKs phosphorylate the C-terminal region of the CBL protein, which contains the FSPF. Different CBLs can also interact independently with one CIPK. For example, AtCBL1 and AtCBL9 can interact with CIPK23, thereby phosphorylating AKT1 to promote K+ uptake under low-K+ conditions [52][53][54]. CBLs specifically target the plant-exclusive CIPKs family of serine-threonine kinases, characterized by an N-terminal kinase catalytic domain, a C-terminal inhibitory domain, and an NAF motif known as the FISL motif. The N-terminal kinase features a proposed activation loop with conserved serine, threonine, and tyrosine residues. CBLs bind to the FISL motif, followed by a conserved protein phosphatase interaction (PPI), inducing CIPKs to engage with protein phosphatases 2C [55][56][57][58][59][60][61]. The suggested mechanism posits that the interplay between CIPKs, 2C-type protein phosphatases, and downstream target proteins involves phosphorylation and dephosphorylation events [62]. The Salt Overly Sensitive (SOS) pathway (Figure 3) is central to cell signaling in salt stress [63].
Figure 3. A typical model of the CBL-CIPK pathway (SOS pathway): In response to salt stress, the concentration of cytoplasmic Ca2+ increases, leading to the binding of SOS3 to Ca2+. This interaction triggers molecular alterations in SOS3, allowing it to physically interact with SOS2 at its NAF/FISL motif. SOS2 undergoes phosphorylation by a kinase, resulting in its activation, and then phosphorylates SOS1. This activation of SOS1 facilitates the efflux of Na+ from the cell. Once the stress subsides, ABI2 binds to the PPI motif, leading to the dephosphorylation of both SOS2 and SOS1. (SOS3: CBL4, SOS2: CIPK24, SOS1: Salt overly sensitive 1, ABI2: PPC2 type protein phosphatase.)
Some CBLs also possess myristoylation motifs. Myristoylation is a post-translational modification that is important for the attachment of proteins to membranes [64][65]. The N-terminus of each CBL protein has a characteristic MGCXXSK/T sequence, which is a site for myristoylation. The glycine residue, which is at the second position in this sequence, is the exact point of myristoylation. The addition of a palmytoyl group to the cysteine next to the second glycine increases the affinity of the poorly attached myristoylated CBL proteins to the membrane [65][66].

5. The CBL Family and Their Functions in Some Plants under Salt Stress

It has been demonstrated that CBL10 from tomatoes (SlCBL10) contributes to improved plant growth during salt stress by modulating the balance of Na+ and Ca2+ [67]. When Slcbl10 mutant plants were subjected to short-term salt treatments, the aerial parts of both young and adult plants were severely damaged. Vegetative growth was impeded at the young stage and the leaflets exhibited chlorosis and apical collapse. Similarly, the adult plants also showed abnormal growth when subjected to short-term salt treatments. However, wild-type plants grew better than Slcbl10 mutant plants under the same conditions of salinity [67]. Also, CBL10 has been shown to enhance salt tolerance in A. thaliana, by physically interacting with CIPK8 [68]. The CBL10-CIPK8 complex then activated SOS1 to extrude Na+ from the plant, thereby relieving it of salt stress. Table 1 provides a summary of the roles played by CBLs in some salt-stressed plants.
Table 1. Summary of the functions of the CBL family in named plants.

CBL Proteins

Plant Sources

Function

CBL-CIPK Complex

References

CBL1

S. Japonica (Orchid of Nago)

Rescues plant from salt hypersensitivity

CBL1-CIPK1

[69]

A. thaliana

Increases salt tolerance

-

[70][71]

CBL2

A. thaliana

Enhances salt tolerance

CBL2-CIPK21

[72]

CBL3

A. thaliana

Enhances salt tolerance

CBL3-CIPK21

[72]

CBL4

Cucumis sativum (Cucumber)

Enhances salt tolerance

CBL4-CIPK6

[73]

Brassica napus

Enhances salt tolerance

CBL4-CIPK24

[74]

CBL5

S. italica (Foxtail millet)

Maintains Na+ homeostasis and enhances salt tolerance

CBL5-CIPK24

[75]

N. tabacum (Common tobacco)

Overexpression causes necrotic lesions

-

[76]

CBL6

T. dicoccoides (Wheat)

Enhances salt tolerance

-

[77]

CBL7

Beta vulgaris (Sugar beet)

Gene expression significantly increased under salt stress

-

[42]

CBL8

A. thaliana

Enhances tolerance under high salt stress

CBL8-CIPK24

[78]

CBL9

T. halophilla

Increases salt tolerance

CBL9-CIPK23

[79]
 

Zea mays (Maize)

Rescues plants from salt hypersensitivity

CBL9-CIPK23

[80]
 

A. thaliana

Increases salt tolerance

CBL9-CIPK23

[81]

CBL10

Solanum lycopersicum (Tomato)

Protects growing tissues from salt stress

-

[67]

A. thaliana

Enhances salt stress tolerance

CBL10-CIPK8

[68]

This entry is adapted from the peer-reviewed paper 10.3390/ijms242316958

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