Functional Mechanism of Plant CBL in Regulating the Responses to Abiotic and Biotic Stresses

doi:10.13560/j.cnki.biotech.bull.1985.2024-1265

Abstract

Abstract:

Calcineurin B like protein (CBL) is a kind of specific Ca²⁺ sensor in plants, which plays a crucial role in plant growth and development, and the response to environmental stresses. CBL is composed of four typical elongation factor hands (EF-hands) domains for Ca²⁺ binding. Each EF-hand is α-helix-loop-α-helix structures composed of 12 relatively conserved amino acids. The cis-acting regulatory elements (such as W-box, MBS and G-BOX) in the promoter regionof CBL can bind with upstream transcription factors (TFs) to regulate transcription by activating or inhibiting the expression of downstream genes. CBL is involved in the regulation of signaling pathways such as abscisic acid (ABA), hormones, respiratory burst oxidases homolog (RBOH), and reactive oxygen species (ROS), to reduce water evaporation, thereby adapting various abiotic stresses. There are evidences that CBL can rapidly perceive changes in the transient intracellular Ca²⁺ signal when plants were subjected to abiotic and biotic stresses such as salt, drought, extreme temperature, nutrient stress and pathogen. CBLs not only interact with CBL-interacting protein kinase CIPK to phosphorylate downstream target proteins for calcium signal transduction, but also interact with other proteins (such as high-affinity K⁺ transporter 5, protein S-acyl transferase10 and type 2C protein phosphatases), thereby positively or negatively regulating stress tolerance in plant. Additionally, CBL mediates the growth and development of plant organs and tissues and promotes fruit ripening by regulating sugar signals. CBL also interacts with gigantea (GI) to affect the flowering time of plants. In this review, recent research findings on the discovery, structure, classification, regulatory mechanisms and roles of plant CBL in regulating the response to adversity stresses are summarized, and its future research directions are prospected, aiming to provide the gene resources and the theoretical basis for improving tolerance of crops and biological breeding to stress.

Key words: calcineurin B like protein, regulatory mechanism, protein-protein interaction, growth and development, stress tolerance, cis-acting regulatory elements, protein kinase

WANG Cong-huan, WU Guo-qiang, WEI Ming. Functional Mechanism of Plant CBL in Regulating the Responses to Abiotic and Biotic Stresses[J]. Biotechnology Bulletin, 2025, 41(7): 1-16.

Figures/Tables 6

References 112

[1]	Zhang ZB, Hu MH, Xu WW, et al. Understanding the molecular mechanism of anther development under abiotic stresses [J]. Plant Mol Biol, 2021, 105(1/2): 1-10.
[2]	Nuruzzaman Manik SM, Shi SJ, Mao JJ, et al. The calcium sensor CBL-CIPK is involved in plant’s response to abiotic stresses [J]. Int J Genomics, 2015, 2015: 493191.
[3]	Ma YC, Cheng QK, Cheng ZM, et al. Identification of important physiological traits and moderators that are associated with improved salt tolerance in CBL and CIPK overexpressors through a meta-analysis [J]. Front Plant Sci, 2017, 8: 856.
[4]	Xiong LM, Schumaker KS, Zhu JK. Cell signaling during cold, drought, and salt stress [J]. Plant Cell, 2002, 14(): S165-S183.
[5]	Zipfel C, Oldroyd GED. Plant signalling in symbiosis and immunity [J]. Nature, 2017, 543(7645): 328-336.
[6]	Kudla J, Becker D, Grill E, et al. Advances and current challenges in calcium signaling [J]. New Phytol, 2018, 218(2): 414-431.
[7]	Tang RJ, Wang C, Li KL, et al. The CBL-CIPK calcium signaling network: unified paradigm from 20 years of discoveries [J]. Trends Plant Sci, 2020, 25(6): 604-617.
[8]	Aslam M, Fakher B, Jakada BH, et al. Genome-wide identification and expression profiling of CBL-CIPK gene family in pineapple (Ananas comosus) and the role of Ac CBL1 in abiotic and biotic stress response [J]. Biomolecules, 2019, 9(7): 293.
[9]	Albrecht V, Ritz O, Linder S, et al. The NAF domain defines a novel protein-protein interaction module conserved in Ca²⁺-regulated kinases [J]. EMBO J, 2001, 20(5): 1051-1063.
[10]	Ma X, Li QH, Yu YN, et al. The CBL-CIPK pathway in plant response to stress signals [J]. Int J Mol Sci, 2020, 21(16): 5668.
[11]	Xuan YH, Kumar V, Han X, et al. CBL-INTERACTING PROTEIN KINASE 9 regulates ammonium-dependent root growth downstream of IDD10 in rice (Oryza sativa) [J]. Ann Bot, 2019, 124(6): 947-960.
[12]	Zhu XL, Wang BQ, Wang X, et al. Genome-wide identification, characterization and expression analysis of the LIM transcription factor family in quinoa [J]. Physiol Mol Biol Plants, 2021, 27(4): 787-800.
[13]	Tian K, Li Q, Zhang XM, et al. Analysis of the expression and function of the CBL-CIPK network and MAPK cascade genes in Kandelia obovata seedlings under cold stress [J]. Front Mar Sci, 2023, 10: 1113278.
[14]	Song SJ, Feng QN, Li CL, et al. A tonoplast-associated calcium-signaling module dampens ABA signaling during stomatal movement [J]. Plant Physiol, 2018, 177(4): 1666-1678.
[15]	Deng JW, Yang XY, Sun WN, et al. The calcium sensor CBL2 and its interacting kinase CIPK6 are involved in plant sugar homeostasis via interacting with tonoplast sugar transporter TST2 [J]. Plant Physiol, 2020, 183(1): 236-249.
[16]	Han JP, Köster P, Drerup MM, et al. Fine-tuning of RBOHF activity is achieved by differential phosphorylation and Ca²⁺ binding [J]. New Phytol, 2019, 221(4): 1935-1949.
[17]	Park HJ, Gámez-Arjona FM, Lindahl M, et al. S-acylated and nucleus-localized SALT OVERLY SENSITIVE3/CALCINEURIN B-LIKE4 stabilizes GIGANTEA to regulate Arabidopsis flowering time under salt stress [J]. Plant Cell, 2023, 35(1): 298-317.
[18]	Liu J, Zhu JK. A calcium sensor homolog required for plant salt tolerance [J]. Science, 1998, 280(5371): 1943-1945.
[19]	Kolukisaoglu U, Weinl S, Blazevic D, et al. Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL-CIPK signaling networks [J]. Plant Physiol, 2004, 134(1): 43-58.
[20]	Lu TT, Zhang GF, Sun LR, et al. Genome-wide identification of CBL family and expression analysis of CBLs in response to potassium deficiency in cotton [J]. PeerJ, 2017, 5: e3653.
[21]	Mo CY, Wan SM, Xia YQ, et al. Expression patterns and identified protein-protein interactions suggest that cassava CBL-CIPK signal networks function in responses to abiotic stresses [J]. Front Plant Sci, 2018, 9: 269.
[22]	Xie LL, Wu GQ, Wei M, et al. Genome-wide identification of the BvCBL genes in sugar beet (Beta vulgaris L.) and their expression under salt and drought conditions [J]. J Plant Growth Regul, 2023, 42(5): 2983-2999.
[23]	Feng XM, Wang YJ, Zhang NN, et al. Comparative phylogenetic analysis of CBL reveals the gene family evolution and functional divergence in Saccharum spontaneum [J]. BMC Plant Biol, 2021, 21(1): 395.
[24]	Wang QW, Zhao K, Gong YQ, et al. Genome-wide identification and functional analysis of the calcineurin B-like protein and calcineurin B-like protein-interacting protein kinase gene families in Chinese cabbage (Brassica rapa ssp. pekinensis) [J]. Genes, 2022, 13(5): 795.
[25]	Ma X, Gai WX, Qiao YM, et al. Identification of CBL and CIPK gene families and functional characterization of CaCIPK1 under Phytophthora capsici in pepper (Capsicum annuum L.) [J]. BMC Genomics, 2019, 20(1): 775.
[26]	Shu B, Cai D, Zhang F, et al. Identifying Citrus CBL and CIPK gene families and their expressions in response to drought and arbuscular mycorrhizal fungi colonization [J]. Biologia Plant, 2020, 64: 773-783.
[27]	Huang LY, Li ZZ, Fu QX, et al. Genome-wide identification of CBL-CIPK gene family in honeysuckle (Lonicera japonica Thunb.) and their regulated expression under salt stress [J]. Front Genet, 2021, 12: 751040.
[28]	Zhang XX, Ren XL, Qi XT, et al. Evolution of the CBL and CIPK gene families in Medicago: genome-wide characterization, pervasive duplication, and expression pattern under salt and drought stress [J]. BMC Plant Biol, 2022, 22(1): 512.
[29]	Du WX, Yang JF, Ma L, et al. Identification and characterization of abiotic stress responsive CBL-CIPK family genes in Medicago [J]. Int J Mol Sci, 2021, 22(9): 4634.
[30]	Zhu XL, Wang BQ, Wang X, et al. Identification of the CIPK-CBL family gene and functional characterization of CqCIPK14 gene under drought stress in quinoa [J]. BMC Genomics, 2022, 23(1): 447.
[31]	Qiu KL, Pan HF, Sheng Y, et al. The peach (Prunus persica) CBL and CIPK family genes: protein interaction profiling and expression analysis in response to various abiotic stresses [J]. Plants, 2022, 11(21): 3001.
[32]	Fu QJ, Hou S, Gao R, et al. Functional identification of the calcineurin B-like protein PavCBL4 in modulating salt tolerance in sweet cherry [J]. Front Plant Sci, 2023, 14: 1293167.
[33]	Mao JJ, Yuan G, Han KY, et al. Genome-wide identification of CBL family genes in Nicotiana tabacum and the functional analysis of NtCBL4A-1 under salt stress [J]. Environ Exp Bot, 2023, 209: 105311.
[34]	Jiao F, Zhang DD, Chen Y, et al. Genome-wide identification of members of the soybean CBL gene family and characterization of the functional role of GmCBL1 in responses to saline and alkaline stress [J]. Plants, 2024, 13(10): 1304.
[35]	Lv BB, Wang T, Wang M, et al. Genome-wide identification of CBL gene family in Salvia miltiorrhiza and the characterization of SmCBL3 under salt stress [J]. Plant Physiol Biochem, 2024, 207: 108384.
[36]	Cui XY, Du YT, Fu JD, et al. Wheat CBL-interacting protein kinase 23 positively regulates drought stress and ABA responses [J]. BMC Plant Biol, 2018, 18(1): 93.
[37]	Sanyal SK, Pandey A, Pandey GK. The CBL-CIPK signaling module in plants: a mechanistic perspective [J]. Physiol Plant, 2015, 155(2): 89-108.
[38]	Beckmann L, Edel KH, Batistič O, et al. A calcium sensor-protein kinase signaling module diversified in plants and is retained in all lineages of Bikonta species [J]. Sci Rep, 2016, 6: 31645.
[39]	Saito S, Hamamoto S, Moriya K, et al. N-myristoylation and S-acylation are common modifications of Ca²⁺-regulated Arabidopsis kinases and are required for activation of the SLAC1 anion channel [J]. New Phytol, 2018, 218(4): 1504-1521.
[40]	Kleist TJ, Spencley AL, Luan S. Comparative phylogenomics of the CBL-CIPK calcium-decoding network in the moss Physcomitrella, Arabidopsis, and other green lineages [J]. Front Plant Sci, 2014, 5: 187.
[41]	Tang RJ, Liu H, Yang Y, et al. Tonoplast calcium sensors CBL2 and CBL3 control plant growth and ion homeostasis through regulating V-ATPase activity in Arabidopsis [J]. Cell Res, 2012, 22(12): 1650-1665.
[42]	Hashimoto K, Eckert C, Anschütz U, et al. Phosphorylation of calcineurin B-like (CBL) calcium sensor proteins by their CBL-interacting protein kinases (CIPKs) is required for full activity of CBL-CIPK complexes toward their target proteins [J]. J Biol Chem, 2012, 287(11): 7956-7968.
[43]	Steinhorst L, He GF, Moore LK, et al. A Ca²⁺-sensor switch for tolerance to elevated salt stress in Arabidopsis [J]. Dev Cell, 2022, 57(17): 2081-2094.e7.
[44]	Zhang TT, Li YX, Wang P, et al. Characterization of Dendrobium catenatum CBL-CIPK signaling networks and their response to abiotic stress [J]. Int J Biol Macromol, 2023, 236: 124010.
[45]	Meng LS, Wang YB, Yao SQ, et al. Arabidopsis AINTEGUMENTA mediates salt tolerance by trans-repressing SCABP8 [J]. J Cell Sci, 2015, 128(15): 2919-2927.
[46]	Liu SS, Yang R, Liu M, et al. PLATZ2 negatively regulates salt tolerance in Arabidopsis seedlings by directly suppressing the expression of the CBL4/SOS3 and CBL10/SCaBP8 genes [J]. J Exp Bot, 2020, 71(18): 5589-5602.
[47]	Ju CF, Zhang ZQ, Deng JP, et al. Ca²⁺-dependent successive phosphorylation of vacuolar transporter MTP8 by CBL2/3-CIPK3/9/26 and CPK5 is critical for manganese homeostasis in Arabidopsis [J]. Mol Plant, 2022, 15(3): 419-437.
[48]	Gratz R, Manishankar P, Ivanov R, et al. CIPK11-dependent phosphorylation modulates FIT activity to promote Arabidopsis iron acquisition in response to calcium signaling [J]. Dev Cell, 2019, 48(5): 726-740.e10.
[49]	Wang C, Tang RJ, Kou SH, et al. Mechanisms of calcium homeostasis orchestrate plant growth and immunity [J]. Nature, 2024, 627(8003): 382-388.
[50]	Gao C, Lu S, Zhou R, et al. The OsCBL8-OsCIPK17 module regulates seedling growth and confers resistance to heat and drought in rice [J]. Int J Mol Sci, 2022, 23(20): 12451.
[51]	Sanyal SK, Kanwar P, Yadav AK, et al. Arabidopsis CBL interacting protein kinase 3 interacts with ABR1, an APETALA2 domain transcription factor, to regulate ABA responses [J]. Plant Sci, 2017, 254: 48-59.
[52]	Zhang F, Li L, Jiao ZZ, et al. Characterization of the calcineurin B-Like (CBL) gene family in maize and functional analysis of ZmCBL9 under abscisic acid and abiotic stress treatments [J]. Plant Sci, 2016, 253: 118-129.
[53]	Hwang YS, Bethke PC, Cheong YH, et al. A gibberellin-regulated calcineurin B in rice localizes to the tonoplast and is implicated in vacuole function [J]. Plant Physiol, 2005, 138(3): 1347-1358.
[54]	Chen CX, Ma YX, Zuo LX, et al. The CALCINEURIN B-LIKE 4/CBL-INTERACTING PROTEIN 3 module degrades repressor JAZ5 during rose petal senescence [J]. Plant Physiol, 2023, 193(2): 1605-1620.
[55]	Xiao XH, Mo CY, Sui JL, et al. The calcium sensor calcineurin B-like proteins-calcineurin B-like interacting protein kinases is involved in leaf development and stress responses related to latex flow in Hevea brasiliensis [J]. Front Plant Sci, 2022, 13: 743506.
[56]	Zhang JB, Chen XX, Song YJ, et al. Integrative regulatory mechanisms of stomatal movements under changing climate [J]. J Integr Plant Biol, 2024, 66(3): 368-393.
[57]	Liu XD, Hasan MM, Fang XW. Phytocytokine SCREWs increase plant immunity through actively reopening stomata [J]. J Plant Physiol, 2022, 279: 153832.
[58]	You Z, Guo SY, Li Q, et al. The CBL1/9-CIPK1 calcium sensor negatively regulates drought stress by phosphorylating the PYLs ABA receptor [J]. Nat Commun, 2023, 14(1): 5886.
[59]	Cheong YH, Pandey GK, Grant JJ, et al. Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis [J]. Plant J, 2007, 52(2): 223-239.
[60]	Huang SG, Maierhofer T, Hashimoto K, et al. The CIPK23 protein kinase represses SLAC1-type anion channels in Arabidopsis guard cells and stimulates stomatal opening [J]. New Phytol, 2023, 238(1): 270-282.
[61]	Li J, Long Y, Qi GN, et al. The Os-AKT1 channel is critical for K⁺ uptake in rice roots and is modulated by the rice CBL1-CIPK23 complex [J]. Plant Cell, 2014, 26(8): 3387-3402.
[62]	Drerup MM, Schlücking K, Hashimoto K, et al. The Calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF [J]. Mol Plant, 2013, 6(2): 559-569.
[63]	Postiglione AE, Muday GK. The role of ROS homeostasis in ABA-induced guard cell signaling [J]. Front Plant Sci, 2020, 11: 968.
[64]	Förster S, Schmidt LK, Kopic E, et al. Wounding-induced stomatal closure requires jasmonate-mediated activation of GORK K⁺ channels by a Ca²⁺ sensor-kinase CBL1-CIPK5 complex [J]. Dev Cell, 2019, 48(1): 87-99.e6.
[65]	Sun WN, Xia LJ, Deng JW, et al. Evolution and subfunctionalization of CIPK6 homologous genes in regulating cotton drought resistance [J]. Nat Commun, 2024, 15(1): 5733.
[66]	Reed RC, Bradford KJ, Khanday I. Seed germination and vigor: ensuring crop sustainability in a changing climate [J]. Heredity, 2022, 128(6): 450-459.
[67]	Guiboileau A, Sormani R, Meyer C, et al. Senescence and death of plant organs: nutrient recycling and developmental regulation [J]. C R Biol, 2010, 333(4): 382-391.
[68]	Yang Y, Zhang C, Tang RJ, et al. Calcineurin B-like proteins CBL4 and CBL10 mediate two independent salt tolerance pathways in Arabidopsis [J]. Int J Mol Sci, 2019, 20(10): 2421.
[69]	Jiang H, Ma QJ, Zhong MS, et al. The apple palmitoyltransferase MdPAT16 influences sugar content and salt tolerance via an MdCBL1-MdCIPK13-MdSUT2.2 pathway [J]. Plant J, 2021, 106(3): 689-705.
[70]	Li MD, Mao ZL, Zhao ZQ, et al. CBL1/CIPK23 phosphorylates tonoplast sugar transporter TST2 to enhance sugar accumulation in sweet orange (Citrus sinensis) [J]. J Integr Plant Biol, 2025, 67(2): 327-344.
[71]	Cuéllar T, Azeem F, Andrianteranagna M, et al. Potassium transport in developing fleshy fruits: the grapevine inward K⁺ channel VvK1.2 is activated by CIPK-CBL complexes and induced in ripening berry flesh cells [J]. Plant J, 2013, 73(6): 1006-1018.
[72]	Zhou LM, Lan WZ, Chen BQ, et al. A calcium sensor-regulated protein kinase, CALCINEURIN B-LIKE PROTEIN-INTERACTING PROTEIN KINASE19, is required for pollen tube growth and polarity [J]. Plant Physiol, 2015, 167(4): 1351-1360.
[73]	Mähs A, Steinhorst L, Han JP, et al. The calcineurin B-like Ca²⁺ sensors CBL1 and CBL9 function in pollen germination and pollen tube growth in Arabidopsis [J]. Mol Plant, 2013, 6(4): 1149-1162.
[74]	Tian MK, Li Q, Liu N, et al. Ca²⁺-induced CpCBL8-CpCIPK9 module negatively regulates dormancy breaking and cold tolerance in winter-flowering wintersweet [J]. Hortic Plant J, 2025, 11(2): 877-890.
[75]	Held K, Pascaud F, Eckert C, et al. Calcium-dependent modulation and plasma membrane targeting of the AKT2 potassium channel by the CBL4/CIPK6 calcium sensor/protein kinase complex [J]. Cell Res, 2011, 21(7): 1116-1130.
[76]	Yin XC, Xia YQ, Xie Q, et al. The protein kinase complex CBL10-CIPK8-SOS1 functions in Arabidopsis to regulate salt tolerance [J]. J Exp Bot, 2020, 71(6): 1801-1814.
[77]	Yan Y, He M, Guo JR, et al. The CBL1/9-CIPK23-AKT1 complex is essential for low potassium response in cassava [J]. Plant Physiol Biochem, 2021, 167: 430-437.
[78]	Xie Q, Yang Y, Wang Y, et al. The calcium sensor CBL10 negatively regulates plasma membrane H⁺-ATPase activity and alkaline stress response in Arabidopsis [J]. Environ Exp Bot, 2022, 194: 104752.
[79]	Qu MQ, Sun Q, Chen NN, et al. Functional characterization of a new salt stress response gene, PeCBL4, in Populus euphratica Oliv [J]. Forests, 2023, 14(7): 1504.
[80]	Mao JJ, Yuan JP, Mo ZJ, et al. Overexpression of NtCBL5A leads to necrotic lesions by enhancing Na⁺ sensitivity of tobacco leaves under salt stress [J]. Front Plant Sci, 2021, 12: 740976.
[81]	Chen L, Ren F, Zhou L, et al. The Brassica napus calcineurin B-Like 1/CBL-interacting protein kinase 6 (CBL1/CIPK6) component is involved in the plant response to abiotic stress and ABA signalling [J]. J Exp Bot, 2012, 63(17): 6211-6222.
[82]	Chen PH, Yang J, Mei QL, et al. Genome-wide analysis of the apple CBL family reveals that Mdcbl10.1 functions positively in modulating apple salt tolerance [J]. Int J Mol Sci, 2021, 22(22): 12430.
[83]	Liu CY, Wang YP, Yao J, et al. Genome-wide investigation of the CBL-CIPK gene family in oil persimmon: evolution, function and expression analysis during development and stress [J]. Horticulturae, 2023, 9(1): 30.
[84]	Chen XX, Ding YL, Yang YQ, et al. Protein kinases in plant responses to drought, salt, and cold stress [J]. J Integr Plant Biol, 2021, 63(1): 53-78.
[85]	Meng D, Dong BY, Niu LL, et al. The pigeon pea CcCIPK14-CcCBL1 pair positively modulates drought tolerance by enhancing flavonoid biosynthesis [J]. Plant J, 2021, 106(5): 1278-1297.
[86]	Song ZH, Dong BY, Yang Q, et al. Screening of CBL genes in pigeon pea with focus on the functional analysis of CBL4 in abiotic stress tolerance and flavonoid biosynthesis [J]. Environ Exp Bot, 2020, 177: 104102.
[87]	Yu QH, Zheng QL, Shen W, et al. Grape CIPK18 acts as a positive regulator of CBF cold signaling pathway by modulating ROS homeostasis [J]. Environ Exp Bot, 2022, 203: 105063.
[88]	Gao HL, Wang CQ, Li LL, et al. A novel role of the calcium sensor CBL1 in response to phosphate deficiency in Arabidopsis thaliana [J]. J Plant Physiol, 2020, 253: 153266.
[89]	Xiao C, Zhang H, Xie F, et al. Evolution, gene expression, and protein-protein interaction analyses identify candidate CBL-CIPK signalling networks implicated in stress responses to cold and bacterial infection in citrus [J]. BMC Plant Biol, 2022, 22(1): 420.
[90]	Liu H, Wang YX, Li H, et al. Genome-wide identification and expression analysis of calcineurin B-like protein and calcineurin B-like protein-interacting protein kinase family genes in tea plant [J]. DNA Cell Biol, 2019, 38(8): 824-839.
[91]	Wang Y, Chen YF, Wu WH. Potassium and phosphorus transport and signaling in plants [J]. J Integr Plant Biol, 2021, 63(1): 34-52.
[92]	Tang RJ, Zhao FG, Garcia VJ, et al. Tonoplast CBL-CIPK calcium signaling network regulates magnesium homeostasis in Arabidopsis [J]. Proc Natl Acad Sci USA, 2015, 112(10): 3134-3139.
[93]	Mogami J, Fujita Y, Yoshida T, et al. Two distinct families of protein kinases are required for plant growth under high external Mg²⁺ concentrations in Arabidopsis [J]. Plant Physiol, 2015, 167(3): 1039-1057.
[94]	Ligaba-Osena A, Fei ZJ, Liu JP, et al. Loss-of-function mutation of the calcium sensor CBL1 increases aluminum sensitivity in Arabidopsis [J]. New Phytol, 2017, 214(2): 830-841.
[95]	Zhang ZQ, Fu DL, Xie DX, et al. CBL1/9-CIPK23-NRAMP1 axis regulates manganese toxicity [J]. New Phytol, 2023, 239(2): 660-672.
[96]	Yan Y, He XY, Hu W, et al. Functional analysis of MeCIPK23 and MeCBL1/9 in cassava defense response against Xanthomonas axonopodis pv. manihotis [J]. Plant Cell Rep, 2018, 37(6): 887-900.
[97]	Liu P, Duan YH, Liu C, et al. The calcium sensor TaCBL4 and its interacting protein TaCIPK5 are required for wheat resistance to stripe rust fungus [J]. J Exp Bot, 2018, 69(18): 4443-4457.
[98]	Yang S, Li J, Lu J, et al. Potato calcineurin B-like protein CBL4, interacting with calcineurin B-like protein-interacting protein kinase CIPK2, positively regulates plant resistance to stem canker caused by Rhizoctonia solani [J]. Front Microbiol, 2023, 13: 1032900.
[99]	Su WH, Huang L, Ling H, et al. Sugarcane calcineurin B-like (CBL) genes play important but versatile roles in regulation of responses to biotic and abiotic stresses [J]. Sci Rep, 2020, 10(1): 167.
[100]	Zhou HP, Shi HF, Yang YQ, et al. Insights into plant salt stress signaling and tolerance [J]. J Genet Genomics, 2024, 51(1): 16-34.
[101]	El-Dakak R, El-Aggan W, Badr G, et al. Positive salt tolerance modulation via vermicompost regulation of SOS1 gene expression and antioxidant homeostasis in Viciafaba plant [J]. Plants, 2021, 10(11): 2477.
[102]	Zhao SS, Zhang QK, Liu MY, et al. Regulation of plant responses to salt stress [J]. Int J Mol Sci, 2021, 22(9): 4609.
[103]	Zhang HM, Zhu JH, Gong ZZ, et al. Abiotic stress responses in plants [J]. Nat Rev Genet, 2022, 23(2): 104-119.
[104]	Kaya C, Uğurlar F, Adamakis IS. Molecular mechanisms of CBL-CIPK signaling pathway in plant abiotic stress tolerance and hormone crosstalk [J]. Int J Mol Sci, 2024, 25(9): 5043.
[105]	Wassie M, Song SR, Cao LW, et al. A Medicago truncatula calcineurin B-like protein, MtCBL13 confers drought sensitivity in Arabidopsis through ABA-dependent pathway [J]. Environ Exp Bot, 2023, 206: 105141.
[106]	Aslam M, Fakher B, Ashraf MA, et al. Plant low-temperature stress: signaling and response [J]. Agronomy, 2022, 12(3): 702.
[107]	Xu YF, Chu CC, Yao SG. The impact of high-temperature stress on rice: Challenges and solutions [J]. Crop J, 2021, 9(5): 963-976.
[108]	Liu H, Liu Q, Gao XH, et al. Role of nitrogen sensing and its integrative signaling pathways in shaping root system architecture [J]. Front Agr Sci Eng, 2022, 9(3): 316-332.
[109]	Tang RJ, Zhao FG, Yang Y, et al. A calcium signalling network activates vacuolar K⁺ remobilization to enable plant adaptation to low-K environments [J]. Nat Plants, 2020, 6(4): 384-393.
[110]	Li KL, Xue H, Tang RJ, et al. TORC pathway intersects with a calcium sensor kinase network to regulate potassium sensing in Arabidopsis [J]. Proc Natl Acad Sci USA, 2023, 120(47): e2316011120.
[111]	Sood M, Kapoor D, Kumar V, et al. Mechanisms of plant defense under pathogen stress: a review [J]. Curr Protein Pept Sci, 2021, 22(5): 376-395.
[112]	Mittler R, Zandalinas SI, Fichman Y, et al. Reactive oxygen species signalling in plant stress responses [J]. Nat Rev Mol Cell Biol, 2022, 23(10): 663-679.

物种 Species	基因名称 Gene name	基因数量 Number of genes	种类 Class	生物功能 Biological function	参考文献 Reference
拟南芥Arabidopsis thaliana	AtCBL	10	十字花科 Brassicaceae	生长发育、高盐、干旱、低温、营养平衡 Growth and development， high-salt， drought， low temperature， and nutrition balance	［19］
雷蒙德氏棉 Gossypium raimondii	GrCBL	13	锦葵科 Malvaceae	/	［20］
木薯 Manihot esculenta	MeCBL	8	大戟科 Euphorbiaceae	高温、营养平衡 High-temperature， and nutrition balance	［21］
菠萝 Ananas comosus	AcCBL	8	凤梨科 Bromeliaceae	高盐、极端温度、病害 High salt， extreme temperature， and disease	［8］
辣椒 Capsicum annuum	CaCBL	9	茄科 Solanaceae	高盐 High salt	［25］
甜橙 Citrus sinensis	CsCBL	8	芸香科 Rutaceae	干旱、病害 Drought， and disease	［26］
金银花Lonicera japonica	LjCBL	6	忍冬科 Caprifoliaceae	生长和发育、高盐、干旱 Growth and development， high salt， and drought	［27］
紫花苜蓿Medicago sativa	MsCBL	10	豆科 Leguminosae	生长和发育、高盐、干旱 Growth and development， high salt， and drought	［28］
蒺藜苜蓿Medicago truncatula	MtCBL	13	豆科 Leguminosae	高盐 High salt	［29］
甜根子草Saccharum spontaneum	SsCBL	10	禾本科 Graminoceae	营养平衡 Nutrition balance	［23］
甜菜 Beta vulgaris	BvCBL	7	藜科 Chenopodiaceae	干旱 Drought	［22］
藜麦Chenopodium quinoa	CqCBL	16	藜科 Chenopodiaceae	胚胎发育、干旱、低温 Embryonic development， drought stress， and low temperature	［30］
白菜 Brassica rapa	BraCBL	18	十字花科 Brassicaceae	高盐、低温、营养平衡 High salt， low temperature， and nutrition balance	［24］
桃 Prunus persica	PprCBL	8	蔷薇科 Rosaceae	糖平衡、干旱 Sugar balance， and drought	［31］
甜樱桃 Prunus avium	PavCBL	7	蔷薇科 Rosaceae	高盐 High salt	［32］
烟草 Nicotiana tabacum	NtCBL	24	茄科 Solanaceae	高盐 High salt	［33］
大豆 Glycine max	GmCBL	15	豆科 Leguminosae	生长发育、高盐、干旱 Growth and development， high salt， and drought	［34］
丹参 Salvia miltiorrhiza	SmCBL	8	唇形科 Lamiaceae	高盐 High salt	［35］

物种 Species	基因名称 Gene name	基因数量 Number of genes	种类 Class	生物功能 Biological function	参考文献 Reference
拟南芥Arabidopsis thaliana	AtCBL	10	十字花科 Brassicaceae	生长发育、高盐、干旱、低温、营养平衡 Growth and development， high-salt， drought， low temperature， and nutrition balance	［19］
雷蒙德氏棉 Gossypium raimondii	GrCBL	13	锦葵科 Malvaceae	/	［20］
木薯 Manihot esculenta	MeCBL	8	大戟科 Euphorbiaceae	高温、营养平衡 High-temperature， and nutrition balance	［21］
菠萝 Ananas comosus	AcCBL	8	凤梨科 Bromeliaceae	高盐、极端温度、病害 High salt， extreme temperature， and disease	［8］
辣椒 Capsicum annuum	CaCBL	9	茄科 Solanaceae	高盐 High salt	［25］
甜橙 Citrus sinensis	CsCBL	8	芸香科 Rutaceae	干旱、病害 Drought， and disease	［26］
金银花Lonicera japonica	LjCBL	6	忍冬科 Caprifoliaceae	生长和发育、高盐、干旱 Growth and development， high salt， and drought	［27］
紫花苜蓿Medicago sativa	MsCBL	10	豆科 Leguminosae	生长和发育、高盐、干旱 Growth and development， high salt， and drought	［28］
蒺藜苜蓿Medicago truncatula	MtCBL	13	豆科 Leguminosae	高盐 High salt	［29］
甜根子草Saccharum spontaneum	SsCBL	10	禾本科 Graminoceae	营养平衡 Nutrition balance	［23］
甜菜 Beta vulgaris	BvCBL	7	藜科 Chenopodiaceae	干旱 Drought	［22］
藜麦Chenopodium quinoa	CqCBL	16	藜科 Chenopodiaceae	胚胎发育、干旱、低温 Embryonic development， drought stress， and low temperature	［30］
白菜 Brassica rapa	BraCBL	18	十字花科 Brassicaceae	高盐、低温、营养平衡 High salt， low temperature， and nutrition balance	［24］
桃 Prunus persica	PprCBL	8	蔷薇科 Rosaceae	糖平衡、干旱 Sugar balance， and drought	［31］
甜樱桃 Prunus avium	PavCBL	7	蔷薇科 Rosaceae	高盐 High salt	［32］
烟草 Nicotiana tabacum	NtCBL	24	茄科 Solanaceae	高盐 High salt	［33］
大豆 Glycine max	GmCBL	15	豆科 Leguminosae	生长发育、高盐、干旱 Growth and development， high salt， and drought	［34］
丹参 Salvia miltiorrhiza	SmCBL	8	唇形科 Lamiaceae	高盐 High salt	［35］

胁迫响应 Response to stress	基因名称 Gene name	物种 Species	功能 Function	参考文献References
盐胁迫 Salinity stress	AtCBL1/9/10	拟南芥 A. thaliana	提高基因表达量；SOS途径调节离子平衡；清除ROS减少细胞氧化损伤；依赖ABA和SA途径提高植物耐盐性 Increasing gene expression； SOS pathway regulates ion balance； eliminating ROS and reducing oxidative damage of cells； improving salt tolerance of plants by ABA and SA	［76-78］
	LjCBL2/4	金银花 L. japonica		［27］
	MsCBL04.1/12.1	紫花苜蓿 M. sativa		［28］
	PeCBL4	胡杨 Populus euphratica		［79］
	NtCBL5A	烟草 N. tabacum		［80］
	PavCBL4	甜樱桃 P. avium		［32］
	AcCBL1	菠萝 A. comosus		［8］
	GmCBL1	大豆 G. max		［34］
	BnCBL1	甘蓝性油菜Brassica napus		［81］
	MdCBL10.1	苹果 M. domestica		［82］
	DoCBL5/8	油柿 Diospyros oleifera		［83］
	MtCBL10	蒺藜苜蓿Medicago truncatula		［29］
	DcCBL1/4/5/6/10	铁皮石斛 D. catenatum		［44］
	BraCBL1.2/3.3/8/9.1/9.2	白菜 B. rapa		［24］
	OsCBL4/8	水稻 O. sativa		［50］
	CaCBL2/3/9	辣椒 C. annuum		［25］
	SmCBL3	丹参 S. miltiorrhiza		［35］
干旱胁迫 Drought stress	AtCBL1/5/9	拟南芥 A. thaliana	提高基因表达量；通过AKT1信号途径吸收K⁺导致植物叶片气孔关闭；介导ABA依赖的气孔运动，提高抗旱 Increasing gene expression； absorption of K⁺ through AKT1 signal pathway leads to stomatal closure of plant leaves； mediating ABA-dependent stomatal movement and improving drought resistance	［84］
	LjCBL2/3	金银花 L. japonica		［27］
	BvCBL3	甜菜 B. vulgaris		［22］
	GmCBL1	大豆 G. max		［34］
	DcCBL4	铁皮石斛 D. catenatum		［44］
	MsCBL04.1/12.1	紫花苜蓿 M. sativa		［28］
	OsCBL8	水稻 O. sativa		［50］
	CcCBL1	鸽豆 Cajanus cajan		［85-86］
	PprCBL1/2/5/6	桃 P. persica		［31］
	CqCBL13	藜麦 C. quinoa		［30］
	DoCBL5/8	油柿 Diospyros oleifera		［83］
	CsCBL1/7/8	甜橙 C. sinensis		［26］
冷胁迫 Cold stress	AcCBL1	菠萝 A. comosus	参与ABA和SA途径提高耐寒性；与CBF途径相互作用，参与基因调控和ROS平衡；与MAPK网络协同作用调控TFs Participating in ABA and SA pathway to improve cold tolerance； interacting with CBF pathway， participating in gene regulation and ROS balance； synergistic effect with MAPK network to regulate transcription factors	［8］
	BraCBL2.2/3.1/4.3/6/10.3	白菜 B. rapa		［24］
	KoCBL	秋茄树Kandelia obovate		［13］
	DcCBL1/4	铁皮石斛 D. catenatum		［44］
	VaCBL	山葡萄 Vitis amurensis		［87］
	AtCBL1	拟南芥 A. thaliana		［88］
	CqCBL8	藜麦 C. quinoa		［74］
	CuCBL5/6/8	柑橘 C. unshiu		［89］
高温胁迫 Heat stress	AcCBL1	菠萝 A. comosus	上调基因表达量；参与热应激；调控TFs抵抗高温 Up-regulating gene expression； involved in heat stress； combining transcription factors to resist high temperatures	［8］
	CsCBL4	茶树 Camellia sinensis		［90］
	MeCBL5	木薯 M. esculenta		［21］
	OsCBL8	水稻 O. sativa		［50］
	DcCBL6/10	铁皮石斛 D. catenatum		［44］
营养胁迫 Nutritional stress	AtCBL1/2/3/4/9	拟南芥 A. thaliana	参与多种信号网络；磷酸化相关蛋白和TFs削弱下游基因的表达 Participating in various signal networks； phosphorylation-related proteins and transcription factors weaken the expression of downstream genes	［7，47-48，75，91-95］
	BnCBL1	甘蓝性油菜Brassica napus		［81］
	MeCBL1/9	木薯 M. esculenta		［96］
	SsCBL01	甜根子草Saccharum spontanum		［23］
	DoCBL5	油柿 Diospyros oleifera		［83］
生物胁迫 Biotic stress	OsCBL4	水稻 O. sativa	提高基因表达量；与下游蛋白RBOHB相互作用，促进ROS增加；靶向NAC77和JAMYB以赋予对病原体的抗性 Increasing gene expression； interacting with downstream protein RBOHB to promote the increase of ROS； targeting NAC77 and JAMYB to confer resistance to pathogens	［50］
	TaCBL4	小麦 Triticum aestivum		［97］
	AcCBL1	菠萝 A. comosus		［8］
	StCBL4	马铃薯Solanum tuberosum		［98］
	CsCBLs	甜橙 C. sinensis		［26，89］
	ScCBL	甘蔗 Saccharum spp.		［99］

胁迫响应 Response to stress	基因名称 Gene name	物种 Species	功能 Function	参考文献References
盐胁迫 Salinity stress	AtCBL1/9/10	拟南芥 A. thaliana	提高基因表达量；SOS途径调节离子平衡；清除ROS减少细胞氧化损伤；依赖ABA和SA途径提高植物耐盐性 Increasing gene expression； SOS pathway regulates ion balance； eliminating ROS and reducing oxidative damage of cells； improving salt tolerance of plants by ABA and SA	［76-78］
	LjCBL2/4	金银花 L. japonica		［27］
	MsCBL04.1/12.1	紫花苜蓿 M. sativa		［28］
	PeCBL4	胡杨 Populus euphratica		［79］
	NtCBL5A	烟草 N. tabacum		［80］
	PavCBL4	甜樱桃 P. avium		［32］
	AcCBL1	菠萝 A. comosus		［8］
	GmCBL1	大豆 G. max		［34］
	BnCBL1	甘蓝性油菜Brassica napus		［81］
	MdCBL10.1	苹果 M. domestica		［82］
	DoCBL5/8	油柿 Diospyros oleifera		［83］
	MtCBL10	蒺藜苜蓿Medicago truncatula		［29］
	DcCBL1/4/5/6/10	铁皮石斛 D. catenatum		［44］
	BraCBL1.2/3.3/8/9.1/9.2	白菜 B. rapa		［24］
	OsCBL4/8	水稻 O. sativa		［50］
	CaCBL2/3/9	辣椒 C. annuum		［25］
	SmCBL3	丹参 S. miltiorrhiza		［35］
干旱胁迫 Drought stress	AtCBL1/5/9	拟南芥 A. thaliana	提高基因表达量；通过AKT1信号途径吸收K⁺导致植物叶片气孔关闭；介导ABA依赖的气孔运动，提高抗旱 Increasing gene expression； absorption of K⁺ through AKT1 signal pathway leads to stomatal closure of plant leaves； mediating ABA-dependent stomatal movement and improving drought resistance	［84］
	LjCBL2/3	金银花 L. japonica		［27］
	BvCBL3	甜菜 B. vulgaris		［22］
	GmCBL1	大豆 G. max		［34］
	DcCBL4	铁皮石斛 D. catenatum		［44］
	MsCBL04.1/12.1	紫花苜蓿 M. sativa		［28］
	OsCBL8	水稻 O. sativa		［50］
	CcCBL1	鸽豆 Cajanus cajan		［85-86］
	PprCBL1/2/5/6	桃 P. persica		［31］
	CqCBL13	藜麦 C. quinoa		［30］
	DoCBL5/8	油柿 Diospyros oleifera		［83］
	CsCBL1/7/8	甜橙 C. sinensis		［26］
冷胁迫 Cold stress	AcCBL1	菠萝 A. comosus	参与ABA和SA途径提高耐寒性；与CBF途径相互作用，参与基因调控和ROS平衡；与MAPK网络协同作用调控TFs Participating in ABA and SA pathway to improve cold tolerance； interacting with CBF pathway， participating in gene regulation and ROS balance； synergistic effect with MAPK network to regulate transcription factors	［8］
	BraCBL2.2/3.1/4.3/6/10.3	白菜 B. rapa		［24］
	KoCBL	秋茄树Kandelia obovate		［13］
	DcCBL1/4	铁皮石斛 D. catenatum		［44］
	VaCBL	山葡萄 Vitis amurensis		［87］
	AtCBL1	拟南芥 A. thaliana		［88］
	CqCBL8	藜麦 C. quinoa		［74］
	CuCBL5/6/8	柑橘 C. unshiu		［89］
高温胁迫 Heat stress	AcCBL1	菠萝 A. comosus	上调基因表达量；参与热应激；调控TFs抵抗高温 Up-regulating gene expression； involved in heat stress； combining transcription factors to resist high temperatures	［8］
	CsCBL4	茶树 Camellia sinensis		［90］
	MeCBL5	木薯 M. esculenta		［21］
	OsCBL8	水稻 O. sativa		［50］
	DcCBL6/10	铁皮石斛 D. catenatum		［44］
营养胁迫 Nutritional stress	AtCBL1/2/3/4/9	拟南芥 A. thaliana	参与多种信号网络；磷酸化相关蛋白和TFs削弱下游基因的表达 Participating in various signal networks； phosphorylation-related proteins and transcription factors weaken the expression of downstream genes	［7，47-48，75，91-95］
	BnCBL1	甘蓝性油菜Brassica napus		［81］
	MeCBL1/9	木薯 M. esculenta		［96］
	SsCBL01	甜根子草Saccharum spontanum		［23］
	DoCBL5	油柿 Diospyros oleifera		［83］
生物胁迫 Biotic stress	OsCBL4	水稻 O. sativa	提高基因表达量；与下游蛋白RBOHB相互作用，促进ROS增加；靶向NAC77和JAMYB以赋予对病原体的抗性 Increasing gene expression； interacting with downstream protein RBOHB to promote the increase of ROS； targeting NAC77 and JAMYB to confer resistance to pathogens	［50］
	TaCBL4	小麦 Triticum aestivum		［97］
	AcCBL1	菠萝 A. comosus		［8］
	StCBL4	马铃薯Solanum tuberosum		［98］
	CsCBLs	甜橙 C. sinensis		［26，89］
	ScCBL	甘蔗 Saccharum spp.		［99］