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Genome-Wide Identification of CIPK Genes in Sugar Beet (Beta vulgaris) and Their Expression Under NaCl Stress

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Abstract

Salinity is one of the major abiotic factors that limits the growth and development of plants and the productivity of crops worldwide. Calcineurin B-like protein (CBL)-interacting protein kinases (CIPKs) have been shown to play a vital role in response to salt stress in plants. Although CIPKs have been widely identified in various species, the genome-wide identification of CIPKs and their expression patterns in sugar beet (Beta vulgaris L.) are unclear. In the present study, a total of 20 BvCIPK genes were identified in the genome of sugar beet and classified into five major groups A–E based on the phylogenetic analysis, and the classification was supported by the intron/exon structures and the distribution of conserved motifs. The NAF (Asn-Ala-Phe)/FISL (Phe-Ile-Ser-Leu) and protein-phosphatase interaction (PPI) domains were found on the C-terminus of BvCIPKs. The 19 BvCIPK genes were unevenly distributed onto seven chromosomes of sugar beet, and one gene was mapped onto unassembled scaffold based on the current genome database. Furthermore, the majority of BvCIPKs were significantly up-regulated by 50 and 100 mM NaCl. Notably, the expression levels of BvCIPK15 in shoots under two levels of NaCl were 7.4- and 4.7-fold higher than those under control condition, respectively. These results implied that BvCIPKs might be involved in the salt response of sugar beet. The findings of present study may provide new insights into the further molecular dissection of biological functions for salt tolerance in sugar crops.

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References

  • Adler G, Blumwald E, Bar-Zvi D (2010) The sugar beet gene encoding the sodium/proton exchanger 1 (BvNHX1) is regulated by a MYB transcription factor. Planta 232:187–195

    Article  CAS  Google Scholar 

  • Albrecht V, Ritz O, Linder S, Harter K, Kudla J (2001) The NAF domain defines a novel protein-protein interaction module conserved in Ca2+-regulated kinases. EMBO J 20:1051–1063

    Article  CAS  Google Scholar 

  • Aslam M, Fakher B, Jakada BH, Zhao LH, Cao SJ, Cheng Y, Qin Y (2019) Genome-wide identification and expression profiling of CBL-CIPK gene family in pineapple (Ananas comosus) and the role of AcCBL1 in abiotic and biotic stress response. Biomolecules 9(7):293

    Article  CAS  Google Scholar 

  • Bailey TL, Gribskov M (1998) Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14:48–54

    Article  CAS  Google Scholar 

  • Batistic O, Kudla J (2004) Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta 219(6):915–924

    Article  CAS  Google Scholar 

  • Bjellqvist B, Hughes GJ, Pasquali C, Paquet N, Ravier F, Sanchez JC, Frutiger S, Hochstrasser DF (1993) The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences. Electrophoresis 14:1023–1031

    Article  CAS  Google Scholar 

  • Blom N, Gammeltoft S, Brunak S (1999) Sequence-and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294:1351–1362

    Article  CAS  Google Scholar 

  • Chen XF, Zhi-Min GU, Liu F, Bo-Jun MA, Zhang HS (2011) Molecular analysis of rice CIPKs involved in both biotic and abiotic stress responses. Rice Sci 18:1–9

    Article  Google Scholar 

  • Chen F, Zhang L, Cheng ZM (2017) The calmodulin fused kinase novel gene family is the major system in plants converting Ca2+ signals to protein phosphorylation responses. Sci Rep 7(1):4127

    Article  Google Scholar 

  • De Laporte AV, Ripplinger DG (2018) Economic viability of energy beets (Beta vulgaris) as advanced biofuel feedstocks. Ind Crop Prod 111:254–260

    Article  Google Scholar 

  • Deng XM, Hu W, Wei SY, Zhou SY, Zhang F, Han JP, Chen LH, Li Y, Feng JL, Fang B, Luo QC, Li SS, Liu YY, Yang GX, He GY (2013) TaCIPK29, a CBL-interacting protein kinase gene from wheat, confers salt stress tolerance in transgenic tobacco. PLoS ONE 8:e69881

    Article  CAS  Google Scholar 

  • Dohm JC, Minoche AE, Holtgräwe D, Salvador CG, Zakrzewski F, Tafer H, Rupp O, Sörensen TR, Stracke R, Reinhardt R, Goesmann A, Kraft T, Schulz B, Stadler PF, Schmidt T, Gabaldón T, Lehrach H, Weisshaar B, Himmelbauer H (2014) The genome of the recently domesticated crop plant sugar beet (Beta vulgaris). Nature 505:546–552

    Article  CAS  Google Scholar 

  • Drerup MM, Schlücking K, Hashimoto K, Manishankar P, Steinhorst L, Kuchitsu K, Kudla J (2013) The calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Mol Plant 6:559–569

    Article  CAS  Google Scholar 

  • Fujita Y, Fujita AM, Satoh CR, Maruyama CK, Parvez AMM, Seki AM (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17:3470–3488

    Article  CAS  Google Scholar 

  • Ganie SA (2020) RNA chaperones: potential candidates for engineering salt tolerance in rice. Crop Sci 60:530–540

    Article  CAS  Google Scholar 

  • Ganie SA, Dey N, Mondal TK (2016) Promoter methylation regulates the abundance of osa-miR393a in contrasting rice genotypes under salinity stress. Funct Integr Genomics 16:1–11

    Article  CAS  Google Scholar 

  • Guo Y, Halfter U, Ishitani M, Zhu JK (2001) Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant Cell 13:1383–1400

    Article  CAS  Google Scholar 

  • Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194

    Article  CAS  Google Scholar 

  • Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015a) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297

    Article  Google Scholar 

  • Hu W, Xia Z, Yan Y, Ding Z, Tie W, Wang L, Zou M, Wei Y, Lu C, Hou X, Wang W, Peng M (2015b) Genome-wide gene phylogeny of CIPK family in cassava and expression analysis of partial drought-induced genes. Front Plant Sci 6:914

    Article  Google Scholar 

  • Ji H, Pardo-José M, Batelli G, Van-Oosten MJ, Bressan RA, Li X (2013) The salt overly sensitive (SOS) pathway: established and emerging roles. Mol Plant 6:275–286

    Article  CAS  Google Scholar 

  • Kanwar P, Sanyal SK, Tokas I, Yadav AK, Pandey A, Kapoor S, Pandey GK (2014) Comprehensive structural, interaction and expression analysis of CBL and CIPK complement during abiotic stresses and development in rice. Cell Calcium 56:81–95

    Article  CAS  Google Scholar 

  • Kim KN, Cheong YH, Gupta R, Luan S (2000) Interaction specificity of Arabidopsis calcineurin B-like calcium sensors and their target kinases. Plant Physiol 124:1844–1853

    Article  CAS  Google Scholar 

  • Kolukisaoglu U, Weinl S, Blazevic D, Batisti O, Kudla J (2004) Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL-CIPK signaling networks. Plant Physiol 134:43–58

    Article  CAS  Google Scholar 

  • Kong W, Yang S, Wang Y, Bendahmane M, Fu X (2017) Genome-wide identification and characterization of aquaporin gene family in Beta vulgaris. PeerJ 5:e3747

    Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  Google Scholar 

  • Lee JY, Taoka K, Yoo BC, Ben-Nissan G, Lucas K (2005) Plasmodesmal-associated protein kinase in tobacco and Arabidopsis recognizes a subset of non-cell-autonomous proteins. Plant Cell 17:2817–2831

    Article  CAS  Google Scholar 

  • Leran S, Edel KH, Pervent M, Hashimoto K, Corratge-Faillie C, Offenborn JN, Tillard P, Gojon A, Kudla J, Lacombe B (2015) Nitrate sensing and uptake in Arabidopsis are enhanced by ABI2, a phosphatase inactivated by the stress hormone abscisic acid. Sci Signal 8:ra43

    Article  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucl Acids Res 30:325–327

    Article  CAS  Google Scholar 

  • Li RF, Zhang JW, Wei JH, Wang HZ, Wang YZ, Ma RC (2009) Functions and mechanisms of the CBL–CIPK signaling system in plant response to abiotic stress. Prog Nat Sci 19(6):667–676

    Article  Google Scholar 

  • Li J, Jiang MM, Ren L, Liu Y, Chen HY (2016) Identification and characterization of CBL and CIPK gene families in eggplant (Solanum melongena L.). Mol Genet Genomics 291(4):1769–1781

    Article  CAS  Google Scholar 

  • Liu H, Wang Q, Yu M, Zhang Y, Wu Y, Zhang H (2008) Transgenic salt-tolerant sugar beet (Beta vulgaris L.) constitutively expressing an Arabidopsis thaliana vacuolar Na+/H+ antiporter gene, AtNHX3, accumulates more soluble sugar but less salt in storage roots. Plant Cell Environ 31:1325–1334

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Luan S (2003) Protein phosphatases in plants. Annu Rev Plant Biol 54:63–92

    Article  CAS  Google Scholar 

  • Luan S (2009) The CBL-CIPK network in plant calcium signaling. Trends Plant Sci 14:37–42

    Article  CAS  Google Scholar 

  • Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W (2002) Calmodulins and calcineurin B-like proteins calcium sensors for specific signal response coupling in plants. Plant Cell 14:S389–S400

    Article  CAS  Google Scholar 

  • Luan S, Lan W, Chul Lee S (2009) Potassium nutrition, sodium toxicity, and calcium signaling: connections through the CBL-CIPK network. Curr Opin Plant Biol 12(3):339–346

    Article  CAS  Google Scholar 

  • Luković J, Maksimović I, Zorić L, Nagl N, Perčić M, Polić D, Putnik-Delić M (2009) Histological characteristics of sugar beet leaves potentially linked to drought tolerance. Ind Crop Prod 30:281–286

    Article  Google Scholar 

  • Ma Y, Cheng Q, Cheng Z, Li H, Chang Y, Lin J (2017) Identification of important physiological traits and moderators that are associated with improved salt tolerance in CBL and CIPK over-expressors through a meta-analysis. Front Plant Sci 8:856

    Article  Google Scholar 

  • Mahajan S, Pandey GK, Tuteja N (2008) Calcium- and salt-stress signaling in plants: shedding light on SOS pathway. Arch Biochem Biophys 471:146–158

    Article  CAS  Google Scholar 

  • Maierhofer T, Diekmann M, Offenborn JN, Lind C, Bauer H, Hashimoto K, Al-Rasheid KA, Luan S, Kudla J, Geiger D (2014) Site-and kinase-specific phosphorylation-mediated activation of SLAC1, a guard cell anion channel stimulated by abscisic acid. Sci Signal 7:ra86

    Article  Google Scholar 

  • Mao J, Manik S, Shi S, Chao J, Jin Y, Wang Q, Liu H (2016) Mechanisms and physiological roles of the CBL-CIPK networking system in Arabidopsis thaliana. Genes 7:62

    Article  Google Scholar 

  • Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17:9–15

    Article  CAS  Google Scholar 

  • Miranda R, Alvarez-Pizarro JC, Costa JH, Paula S, Prisco JT, Gomes-Filho E (2017) Putative role of glutamine in the activation of CBL/CIPK signalling pathways during salt stress in sorghum. Plant Signal Behav 12:e1361075

    Article  Google Scholar 

  • Mo C, Wan S, Xia Y, Ren N, Zhou Y, Jiang X (2018) Expression patterns and identified protein-protein interactions suggest that cassava CBL-CIPK signal networks function in responses to abiotic stresses. Front Plant Sci 9:269

    Article  Google Scholar 

  • Neumann GM, Thomas I, Polya GM (1996) Identification of the site on potato carboxypeptidase inhibitor that is phosphorylated by plant calcium-dependent protein kinase. Plant Sci 114:45–51

    Article  CAS  Google Scholar 

  • Niu L, Dong B, Song Z, Meng D, Fu Y (2018) Genome-wide identification and characterization of CIPK family and analysis responses to various stresses in apple (Malus domestica). Int J Mol Sci 19:2131

    Article  Google Scholar 

  • Ohta M, Guo Y, Halfter U, Zhu JK (2003) A novel domain in the protein kinase SOS2 mediates interaction with the protein phosphatase 2C AB12. Proc Natl Acad Sci USA 100:11771–11776

    Article  CAS  Google Scholar 

  • Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci 99:8436–8441

    Article  CAS  Google Scholar 

  • Ragel P, Rodenas R, Garcia-Martin E, Andres Z, Villalta I, Nieves-Cordones M, Rivero RM, Martínez V, Pardo JM, Quintero FJ, Rubio F (2015) The CBL-interacting protein kinase CIPK23 regulates HAK5-mediated high-affinity K+ uptake in Arabidopsis roots. Plant Physiol 169:2863–2873

    CAS  Google Scholar 

  • Riera M, Peracchia G, Pagès M (2001) Distinctive features of plant protein kinase CK2. Mol Cell Biochem 227(1):119–127

    Article  CAS  Google Scholar 

  • Roberts DM, Harmon AC (1992) Calcium-modulated proteins: targets of intracellular calcium signals in higher plants. Annu Rev Plant Biol Plant Mol Biol 43:375–414

    Article  CAS  Google Scholar 

  • Saito S, Uozumi N (2020) Calcium-regulated phosphorylation systems controlling uptake and balance of plant nutrients. Front Plant Sci 11:44

    Article  Google Scholar 

  • Sánchez-Barrena MJ, Martínez-Ripoll M, Albert A (2013) Structural biology of a major signaling network that regulates plant abiotic stress: the CBL-CIPK mediated pathway. Int J Mol Sci 14(3):5734–5749

    Article  Google Scholar 

  • Sanyal SK, Pandey A, Pandey GK (2015) The CBL-CIPK signaling module in plants: a mechanistic perspective. Physiol Plant 155(2):89–108

    Article  CAS  Google Scholar 

  • Sanyal SK, Rao S, Mishra LK, Sharma M, Pandey GK (2016) Plant stress responses mediated by CBL-CIPK phosphorylation network. Enzymes 40:31–64

    Article  CAS  Google Scholar 

  • Sanyal SK, Mahiwal S, Nambiar DM, Pandey GK (2020) CBL-CIPK module-mediated phosphoregulation: facts and hypothesis. Biochemical Journal 477(5):853–871

    Article  CAS  Google Scholar 

  • Schenk PW, Snaar-Jagalska BE (1999) Signal perception and transduction: the role of protein kinases. Biochem Biophys Acta 1449(1):1–24

    Article  CAS  Google Scholar 

  • Shi J, Kim KN, Ritz O, Albrecht V, Gupta R, Harter K, Luan S, Kudla J (1999) Novel protein kinases associated with calcineurin B-like calcium sensors in Arabidopsis. Plant Cell 11:2393–2405

    CAS  Google Scholar 

  • Song SJ, Feng QN, Li CL, Li E, Liu Q, Kang H, Zhang W, Zhang Y, Li S (2018) A tonoplast-associated calcium-signaling module dampens ABA signaling during stomatal movement. Plant Physiol 177(4):1666–1678

    Article  CAS  Google Scholar 

  • Sun S, Yu JP, Chen F, Zhao TJ, Fang XH, Li YQ, Sui SF (2007) TINY, a dehydration-responsive element (DRE)-binding protein-like transcription factor connecting the DRE- and ethylene-responsive element-mediated signaling pathways in Arabidopsis. J Biol Chem 283:6261–6271

    Article  Google Scholar 

  • Sun T, Wang Y, Wang M, Li T, Zhou Y, Yang G (2015) Identification and comprehensive analyses of the CBL and CIPK gene families in wheat (Triticum aestivum L.). BMC Plant Biol 15:269

    Article  Google Scholar 

  • Szklarczyk D, Morris JH, Cook H, Kuhn M, Wyder S, Simonovic M, Santos A, Doncheva NT, Roth A, Bork P, Jensen LJ, Mering C (2017) The STRING database in 2017: quality-controlled protein–protein association networks, made broadly accessible. Nuc Acids Res 45:D362–D368

    Article  CAS  Google Scholar 

  • Tang RJ, Wang C, Li K, Luan S (2020a) The CBL-CIPK calcium signaling network: unified paradigm from 20 years of discoveries. Trends Plant Sci 25(6):604–617

    Article  CAS  Google Scholar 

  • Tang RJ, Zhao FG, Yang Y, Wang C, Li K, Kleist TJ, Lemaux PG, Luan S (2020b) A calcium signaling network activates vacuolar K+ remobilization to enable plant adaptation to low-K environments. Nat Plants 6(4):384–393

    Article  CAS  Google Scholar 

  • Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK, Kumar V, Verma R, Upadhyay RG, Pandey M, Sharma S (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci 8:161

    Article  Google Scholar 

  • Wakeel A (2013) Potassium-sodium interactions in soil and plant under saline-sodic conditions. J Plant Nutr Soil Sci 176:344–354

    Article  CAS  Google Scholar 

  • Wakeel A, Asif AR, Pitann B, Schubert S (2011) Proteome analysis of sugar beet (Beta vulgaris L.) elucidates constitutive adaptation during the first phase of salt stress. J Plant Physiol 168:519–526

    Article  CAS  Google Scholar 

  • Walker S (1995) Plant protein kinase families and signal transduction. Plant Physiol 108(2):451–457

    Article  Google Scholar 

  • Weinl S, Kudla J (2009) The CBL-CIPK Ca2+-decoding signaling network: function and perspectives. New Phytol 184:517–528

    Article  CAS  Google Scholar 

  • Wu GQ, Feng RJ, Zhang JJ (2013) Evaluation of salinity tolerance in seedlings of sugar beet (Beta vulgaris L.) cultivars using proline, soluble sugars and cation accumulation criteria. Acta Physiol Plant 35:2665–2674

    Article  CAS  Google Scholar 

  • Wu GQ, Feng RJ, Liang N, Yuan HJ, Sun WB (2015) Sodium chloride stimulates growth and alleviates sorbitol-induced osmotic stress in sugar beet seedlings. Plant Growth Regul 75:307–316

    Article  CAS  Google Scholar 

  • Wu GQ, Wang JL, Li SJ (2019) Genome-wide identification of Na+/H+ antiporter (NHX) genes in sugar beet (Beta vulgaris L.) and their regulated expression under salt stress. Genes 10:401

    Article  CAS  Google Scholar 

  • Xi Y, Liu J, Dong C, Cheng ZM (2017) The CBL and CIPK gene family in grapevine (Vitis vinifera): genome-wide analysis and expression profiles in response to various abiotic stresses. Front Plant Sci 8:978

    Article  Google Scholar 

  • Xu Z, Raza Q, Xu L, He X, Huang Y, Yi J, Zhang D, Shao HB, Ma H, Ali Z (2018) GmWRKY49, a salt responsive nuclear protein, improved root length and governed better salinity tolerance in transgenic Arabidopsis. Front Plant Sci 9:809

    Article  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94

    Article  CAS  Google Scholar 

  • Yin X, Wang Q, Chen Q, Xiang N, Yang Y, Yang Y (2017) Genome-wide identification and functional analysis of the Calcineurin B-like protein and calcineurin b-like protein-interacting protein kinase gene families in turnip (Brassica rapa var. rapa). Front Plant Sci 8:1191

    Article  Google Scholar 

  • Yin XC, Xia YQ, Xie Q, Cao YX, Wang ZY, Hao GP, Song J, Zhou Y, Jiang XY (2020) The protein kinase complex CBL10-CIPK8-SOS1 functions in Arabidopsis to regulate salt tolerance. J Exp Bot 71(6):1801–1814

    Article  CAS  Google Scholar 

  • Yu Y, Xia X, Yin W, Zhang H (2007) Comparative genomic analysis of CIPK gene family in Arabidopsis and Populus. Plant Growth Regul 52:101–110

    Article  CAS  Google Scholar 

  • Zhang H, Yang B, Liu WZ, Li H, Wang L, Wang B (2014) Identification and characterization of CBL and CIPK gene families in canola (Brassica napus L.). BMC Plant Biol 14:8

    Article  CAS  Google Scholar 

  • Zhang HW, Feng H, Zhang JW, Ge RC, Zhang LY, Wang YX, Li LG, Wei JH, Li RF (2020a) Emerging crosstalk between two signaling pathways coordinates K+ and Na+ homeostasis in the halophyte Hordeum brevisubulatum. J Exp Bot 71(14):4345–4358

    Article  CAS  Google Scholar 

  • Zhang X, Li X, Zhao R, Zhou Y, Jiao Y (2020b) Evolutionary strategies drive a balance of the interacting gene products for the CBL and CIPK gene families. New Phytol 226(5):1506–1516

    Article  CAS  Google Scholar 

  • Zhu J, Fu X, Koo DY, Zhu JK, Jenney FE, Adams MWW, Zhu Y, Shi H, Yun DJ, Hasegawa PM, Bressan RA (2007) An enhancer mutant of Arabidopsis salt overly sensitive 3 mediates both ion homeostasis and the oxidative stress response. Mol Cell Biol 27:5214–5224

    Article  CAS  Google Scholar 

  • Zhu S, Zhou X, Wu X, Jiang Z (2013) Structure and function of the CBL–CIPK Ca2+-decoding system in plant calcium signaling. Plant Mol Biol Rep 31:1193–1202

    Article  CAS  Google Scholar 

  • Zhu K, Chen F, Liu J, Chen X, Hewezi T, Cheng ZM (2016) Evolution of an intron-poor cluster of the CIPK gene family and expression in response to drought stress in soybean. Sci Rep 6:28225

    Article  CAS  Google Scholar 

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Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (Grant Nos. 31860404 and 32160466) and Lanzhou Science and Technology Planning Project (2021-1-165).

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G-QW designed the research, wrote, and revised the article. L-LX analyzed the data and revised the article. J-LW conducted the research and wrote the article. B-CW and Z-QL analyzed the data. All authors read and approved the final manuscript.

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Correspondence to Guo-Qiang Wu.

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344_2021_10545_MOESM1_ESM.xlsx

Supplementary file1 (XLSX 182 KB) Supplementary Data 1 Details of sequences, cis-acting element, motifs, protein-protein interaction of BvCIPKs, and NetPhos 3.1 results for BvCIPKs

Supplementary file2 (PDF 191 KB) Supplementary Fig. S1 Detailed information of BvCIPK motifs in sugar beet

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Wu, GQ., Xie, LL., Wang, JL. et al. Genome-Wide Identification of CIPK Genes in Sugar Beet (Beta vulgaris) and Their Expression Under NaCl Stress. J Plant Growth Regul 42, 260–274 (2023). https://doi.org/10.1007/s00344-021-10545-6

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