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Expression analysis of calcium-dependent protein kinases (CDPKs) superfamily genes in Medicago lupulina in response to high calcium, carbonate and drought

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Abstract

Aims

The aim of this study is to identify calcium dependent protein kinases (CDPKs) superfamily genes (including calcium dependent protein kinase (CDPK) genes, CDPK-related kinase (CRK) genes, and phosphoenolpyruvate carboxylase kinase-related kinase (PEPRK) genes) and to analyze their expression in response to high calcium, bicarbonate, and water deficit in Medicago lupulina.

Methods

Transcriptome sequencing databases and bioinformatics were used to identify CDPK superfamily genes. qRT-PCR analyses were used to study the expression of CDPK superfamily genes in response to high calcium, bicarbonate, water deficit, and their combined treatments.

Results

Ten MlCDPKs, four MlCRKs, and two MlPEPRKs genes were identified from transcriptome sequencing databases. The identified MlCDPK superfamily genes could be divided into six subgroups including CDPK I, CDPK II, CDPK III, CDPK IV, CRK, and PEPRK according to evolutionary relationships. Analysis of protein structure indicated that MlCDPK proteins contained a protein kinase domain and EF-hand domain. However, PEPRKs contained only a protein kinase domain while CRKs contained also degenerative EF-hands. Most of the MlCDPK superfamily genes were differentially expressed in different organs. According to their expression levels, MlCDPK superfamily genes such as MlCDPK1, MlCDPK9, and MlCDPK10 were more sensitive in response to individual treatments of high calcium, carbonate or PEG rather than their combination of treatments. The results indicated that MlCDPK superfamily genes may play an important role in response to those stresses.

Conclusions

These results provide important insight into the role of CDPKs in M. lupulina, especially in the tolerance to Karst habitats, where high calcium and carbonate and drought conditions are the dominant ecological limiting factors.

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Abbreviations

CaM:

Calmodulins

CaMK:

Calmodulin regulated kinase

CCaMK:

Calcium/calmodulin-dependent protein kinase

CaMLs:

Calmodulin-like proteins

CBL:

Calcineurin B-like proteins

CDPK:

Calcium-dependent protein kinase

CRK:

CDPK-related kinase

PEPRK:

Phosphoenolpyruvate carboxylase kinase-related kinase

PKD:

Protein kinase domain

PPCK:

Phosphoenolpyruvate carboxylase kinase

References

  • Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffmann T, Tang YY, Grill E, Schroeder JI (2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053–1057

    Article  CAS  PubMed  Google Scholar 

  • Almadanim MC, Alexandre BM, Rosa MTG, Sapeta H, Leitão AE, Ramalho JC, Lam TT, Negrão S, Abreu IA, Oliveira MM (2017) Rice calcium-dependent protein kinase OsCPK17 targets plasma membrane intrinsic protein and sucrose phosphate synthase and is required for a proper cold stress response. Plant Cell Environ 40:1197–1213

    Article  CAS  PubMed  Google Scholar 

  • Asano T, Tanaka N, Yang G, Hayashi N, Komatsu S (2005) Genome-wide identification of the rice calcium-dependent protein kinase and its closely related kinase gene families: comprehensive analysis of the CDPKs gene family in rice. Plant Cell Physiol 46:356–366

    Article  CAS  PubMed  Google Scholar 

  • Botella JR, Arteca JM, Somodevilla M, Arteca RN (1996) Calcium-dependent protein kinase gene expression in response to physical and chemical stimuli in mungbean (Vigna radiata). Plant Mol Biol 30:1129–1137

    Article  CAS  PubMed  Google Scholar 

  • Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, He P, Bush J, Cheng SH, Sheen J (2010) Differential innate immune signalling via Ca2+ sensor protein kinases. Nature 464:418–422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bundó M, Coca M (2017) Calcium-dependent protein kinase OsCPK10 mediates both drought tolerance and blast disease resistance in rice plants. J Exp Bot 68:2963–2975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campo S, Baldrich P, Messeguer J, Lalanne E, Coca M, San SB (2014) Overexpression of a calcium-dependent protein kinase confers salt and drought tolerance in rice by preventing membrane lipid peroxidation. Plant Physiol 165:688–704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng SH, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469–485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coca M, San Segundo B (2010) AtCPK1 calcium-dependent protein kinase mediates pathogen resistance in Arabidopsis. Plant J 63:526–540

    Article  CAS  PubMed  Google Scholar 

  • Dubiella U, Seybold H, Durian G, Komander E, Lassig R, Witte CP, Schulze WX, Romeis T (2013) Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc Natl Acad Sci U S A 110:8744–8749

    Article  PubMed  PubMed Central  Google Scholar 

  • Dubrovina AS, Kiselev KV, Khristenko VS, Aleynova OA (2015) VaCPK20, a calcium-dependent protein kinase gene of wild grapevine (Vitis amurensis), mediates cold and drought stress tolerance. J Plant Physiol 185:1–12

    Article  CAS  PubMed  Google Scholar 

  • Dubrovina AS, Kiselev KV, Khristenko VS, Aleynova OA (2017) The calcium-dependent protein kinase gene VaCPK29 is involved in grapevine responses to heat and osmotic stresses. Plant Growth Regul 82:79–89

    Article  CAS  Google Scholar 

  • Furumoto T, Al E (1996) Plant calcium-dependent protein kinase-related kinases (CRKs) do not require calcium for their activities. FEBS Lett 396:147–151

    Article  CAS  PubMed  Google Scholar 

  • Gao X, Chen X, Lin W, Chen S, Lu D, Niu Y, Li L, Cheng C, McCormack M, Sheen J, Shan L, He P (2013) Bifurcation of Arabidopsis NLR immune signaling via Ca2+-dependent protein kinases. PLoS Pathog 9:e1003127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao A, Wu Q, Zhang Y, Miao Y, Song C (2014) Arabidopsis calcium-dependent protein kinase CPK28 is potentially involved in the response to osmotic stress. Chin Sci Bull 59:1113–1122

  • Gao W, Xu FC, Guo DD, Zhao JR, Liu J, Guo TW, Singh PK, Ma XN, Long L, Botella JR, Song CP (2018) Calcium-dependent protein kinases in cotton: insights into early plant responses to salt stress. BMC Plant Biol 18:15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • García-Mauriño S, Monreal JA, Alvarez R, Vidal J, Echevarría C (2003) Characterization of salt stress-enhanced phosphoenolpyruvate carboxylase kinase activity in leaves of Sorghum vulgare: independence from osmotic stress, involvement of ion toxicity and significance of dark phosphorylation. Planta 216:648–655

    PubMed  Google Scholar 

  • Gargantini PR, Gonzalez-Rizzo S, Chinchilla D, Raices M, Giammaria V, Ulloa RM, Frugier F, Crespi MD (2006) A CDPK isoform participates in the regulation of nodule number in Medicago truncatula. Plant J 48:843–856

    Article  CAS  PubMed  Google Scholar 

  • Gifford JL, Walsh MP, Vogel HJ (2007) Structures and metal-ion-binding properties of the Ca2+-binding helix-loop-helix EF-hand motifs. Biochem J 405:199–221

    Article  CAS  PubMed  Google Scholar 

  • Gleason C, Chaudhuri S, Yang T, Muñoz A, Poovaiah BW, Oldroyd GED (2006) Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 441:1149–1152

    Article  CAS  PubMed  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol 29:644–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harmon AC, Gribskov M, Gubrium E, Harper JF (2001) The CDPK superfamily of protein kinases. New Phytol 151:175–183

    Article  CAS  PubMed  Google Scholar 

  • Harper JF, Breton G, Harmon A (2004) Decoding Ca2+ signals through plant protein kinases. Annu Rev Plant Biol 55:263–288

    Article  CAS  PubMed  Google Scholar 

  • Hartwell J, Wilkins MB, Jenkins GI, Nimmo HG (1996) Higher plant phosphoenolpyruvate carboxylase kinase is regulated at the level of translatable mRNA in response to light or a circadian rhythm. Plant J 10:1071–1078

    Article  CAS  Google Scholar 

  • Hrabak EM, Chan CW, Gribskov M et al (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666–680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu WJ, Chen J, Liu TW, Wu Q, Wang WH, Liu X, Shen ZJ, Simon M, Chen J, Wu FH, Pei ZM, Zheng HL (2014) Proteome and calcium-related gene expression in Pinus massoniana needles in response to acid rain under different calcium levels. Plant Soil 380:285–303

    Article  CAS  Google Scholar 

  • Hu ZJ, Lv XZ, Xia XJ, Zhou J, Shi K, Yu JQ, Zhou YH (2016) Genome-wide identification and expression analysis of calcium-dependent protein kinase in tomato. Front Plant Sci 7:1–11

    CAS  Google Scholar 

  • Ivashuta S, Liu J, Liu J, Lohar DP, Haridas S, Bucciarelli B, VandenBosch KA, Vance CP, Harrison MJ, Gantt JS (2005) RNA interference identifies a calcium-dependent protein kinase involved in Medicago truncatula root development. Plant Cell 17:2911–2921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jauregui E, Du L, Gleason C, Poovaiah BW (2017) W342F mutation in CCaMK enhances its affinity to calmodulin but compromises its role in supporting root nodule symbiosis in Medicago truncatula. Front Plant Sci 8:1–9

    Article  Google Scholar 

  • Jaworski K, Pawełek A, Kopcewicz J, Szmidtjaworska A (2012) The calcium-dependent protein kinase (PnCDPK1) is involved in Pharbitis nil flowering. J Plant Physiol 169:1578–1585

    Article  CAS  PubMed  Google Scholar 

  • Kanchiswamy CN, Takahashi H, Quadro S, Maffei ME, Bossi S, Bertea C, Zebelo SA, Muroi A, Ishihama N, Yoshioka H, Boland W, Takabayashi J, Endo Y, Sawasaki T, Arimura G (2010) Regulation of Arabidopsis defense responses against Spodoptera littoralis by CPK-mediated calcium signaling. BMC Plant Biol 10:97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khuri S, Bakker FT, Dunwell JM (2001) Phylogeny, function, and evolution of the Cupins, a structurally conserved, functionally diverse superfamily of proteins. Mol Biol Evol 18:593–605

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, Doke N, Yoshioka H (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19:1065–1080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong XP, Lv W, Jiang SS, Zhang D, Cai GH, Pan JW, Li DQ (2013) Genome-wide identification and expression analysis of calcium-dependent protein kinase in maize. BMC Genomics 14:1–15

    Article  CAS  Google Scholar 

  • Leclercq J, Ranty B, Sanchez-Ballesta MT, Li Z, Jones B, Jauneau A, Pech JC, Latché A, Ranjeva R, Bouzayen M (2005) Molecular and biochemical characterization of LeCRK1, a ripening-associated tomato CDPK-related kinase. J Exp Bot 56:25–35

    CAS  PubMed  Google Scholar 

  • Li RJ, Hua W, Lu YT (2006) Arabidopsis cytosolic glutamine synthetase AtGLN1;1 is a potential substrate of AtCRK3 involved in leaf senescence. Biochem Biophys Res Commun 342:119–126

    Article  CAS  PubMed  Google Scholar 

  • Li AL, Zhu YF, Tan XM, Wang X, Wei B, Guo HZ, Zhang ZL, Chen XB, Zhao GY, Kong XY, Jia JZ, Mao L (2008) Evolutionary and functional study of the CDPK gene family in wheat (Triticum aestivum). Plant Mol Biol 66:429–443

    Article  CAS  PubMed  Google Scholar 

  • Liu HT, Gao F, Li GL, Han JL, Liu DL, Sun DY, Zhou RG (2008a) The calmodulin-binding protein kinase 3 is part of heat-shock signal transduction in Arabidopsis thaliana. Plant J 55:760–773

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Liu X, Liao C (2008b) Daytime deposition and nighttime dissolution of calcium carbonate controlled by submerged plants in a karst spring-fed pool: insights from high time-resolution monitoring of physico-chemistry of water. Environ Geol 55:1159–1168

    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  PubMed  Google Scholar 

  • Llop-Tous I, Dominguez-Puigjaner E, Vendrell M (2002) Characterization of a strawberry cDNA clone homologous to calcium-dependent protein kinases that is expressed during fruit ripening and affected by low temperature. J Exp Bot 53:2283–2285

    Article  CAS  PubMed  Google Scholar 

  • Lv XZ, Li HZ, Chen XX, Xiang X, Guo ZX, Yu JQ, Zhou YH (2018) The role of calcium-dependent protein kinase in hydrogen peroxide, nitric oxide and ABA-dependent cold acclimation. J Exp Bot 69:4127–4139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manimaran P, Mangrauthia SK, Sundaram RM, Balachandran SM (2015) Constitutive expression and silencing of a novel seed specific calcium dependent protein kinase gene in rice reveals its role in grain filling. J Plant Physiol 174:41–48

    Article  CAS  PubMed  Google Scholar 

  • Martín ML, Busconi L (2010) Membrane localization of a rice calcium-dependent protein kinase (CDPK) is mediated by myristoylation and palmitoylation. Plant J 24:429–435

    Google Scholar 

  • Matschi S, Werner S, Schulze WX, Legen J, Hilger HH, Romeis T (2013) Function of calcium-dependent protein kinase CPK28 of Arabidopsis thaliana in plant stem elongation and vascular development. Plant J 73:883–896

    Article  CAS  PubMed  Google Scholar 

  • Matschi S, Hake K, Herde M, Hause B, Romeis T (2015) The calcium-dependent protein kinase CPK28 regulates development by inducing growth phase-specific, spatially restricted alterations in Jasmonic acid levels independent of defense responses in Arabidopsis. Plant Cell 27:591–606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mengel K, Breininger MT, Bübl W (1984) Bicarbonate, the most important factor inducing iron chlorosis in vine grapes on calcareous soil. Plant Soil 81:333–344

    Article  CAS  Google Scholar 

  • Miller JB, Pratap A, Miyahara A, Zhou L, Bornemann S, Morris RJ, Oldroyd GE (2013) Calcium/calmodulin-dependent protein kinase is negatively and positively regulated by calcium, providing a mechanism for decoding calcium responses during symbiosis signaling. Plant Cell 25:5053–5066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monaghan J, Matschi S, Shorinola O, Rovenich H, Matei A, Segonzac C, Malinovsky FG, Rathjen JP, MacLean D, Romeis T, Zipfel C (2014) The calcium-dependent protein kinase CPK28 buffers plant immunity and regulates BIK1 turnover. Cell Host Microbe 16:605–615

    Article  CAS  PubMed  Google Scholar 

  • Myers C, Romanowsky SM, Barron YD, Garg S, Azuse CL, Curran A, Davis RM, Hatton J, Harmon AC, Harper JF (2010) Calcium-dependent protein kinases regulate polarized tip growth in pollen tubes. Plant J 59:528–539

    Article  CAS  Google Scholar 

  • Qiao ZJ, Jing T, Jin ZP, Liang YL, Zhang LP, Liu ZQ, Liu DM, Pei YX (2016) CDPKs enhance cd tolerance through intensifying H2S signal in Arabidopsis thalinan. Plant Soil 398:99–110

    Article  CAS  Google Scholar 

  • Ramos AC, Dobbss LB, Santos LA, Fernandes MS, Olivares FL, Aguiar NO, Canellas LP (2015) Humic matter elicits proton and calcium fluxes and signaling dependent on Ca2+ −dependent protein kinase (CDPK) at early stages of lateral plant root development. Chem Biol Technol Agric 2:1–12

    Article  CAS  Google Scholar 

  • Rigó G, Ayaydin F, Tietz O, Zsigmond L, Kovács H, Páy A, Salchert K, Darula Z, Medzihradszky KF, Szabados L, Palme K, Koncz C, Cséplo Á (2013) Inactivation of plasma membrane-localized CDPK-related kinase5 decelerates PIN2 exocytosis and root gravitropic response in Arabidopsis. Plant Cell 25:1592–1608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romeis T, Herde M (2014) From local to global: CDPKs in systemic defense signaling upon microbial and herbivore attack. Cur Opin Plant Biol 20:1–10

    Article  CAS  Google Scholar 

  • Saijo Y, Hata S, Kyozuka J, Shimamoto K, Lzui K (2000) Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23:319–327

    Article  CAS  PubMed  Google Scholar 

  • Sanders D, Brownlee C, Harper JF (1999) Communicating with calcium. Plant Cell 11:691–706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun YL, Zhang DH, Zhao L, Xia CC, Chou MX (2014) Reference gene selection for real-time quantitative PCR in black medic (Medicago lupulina) root tissue under copper stress. Chin J Agric Biotechnol 22:1223–1231

  • Swainsbury DJK, Zhou L, Oldroyd GED, Bornemann S (2012) Calcium ion binding properties of Medicago truncatula calcium/calmodulin-dependent protein kinase. Biochem 51:6895–6907

    Article  CAS  Google Scholar 

  • Takeda N, Hayashi M (2012) Nuclear-localized and deregulated calcium- and calmodulin- dependent protein kinase activates rhizobial and mycorrhizal responses in Lotus japonicus. Plant Cell 24:810–822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tao XC, Lu YT (2013) Loss of AtCRK1 gene function in Arabidopsis thaliana decreases tolerance to salt. J Plant Biol 56:306–314

    Article  CAS  Google Scholar 

  • Taybi T, Patil S, Cholle R, Cushman JC (2000) A minimal serine/threonine protein kinase circadianly regulates phosphoenolpyruvate carboxylase activity in crassulacean acid metabolism-induced leaves of the common ice plant. Plant Physiol 123:1471–1482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson GA, Okuyama H (2000) Lipid-linked proteins of plants. Prog Lipid Res 39:19–39

    Article  CAS  PubMed  Google Scholar 

  • Wan B, Lin Y, Mou T (2007) Expression of rice Ca2+-dependent protein kinases (CDPKs) genes under different environmental stresses. FEBS Lett 581:1179–1189

    Article  CAS  PubMed  Google Scholar 

  • Wang JP, Munyampundu JP, Xu YP, Cai XZ (2015) Phylogeny of plant calcium and calmodulin-dependent protein kinases (CCaMKs) and functional analyses of tomato CCaMK in disease resistance. Front Plant Sci 6:1075

    PubMed  PubMed Central  Google Scholar 

  • Wang JP, Xu YP, Munyampundu JP, Liu TY, Cai XZ (2016) Calcium-dependent protein kinase (CDPK) and CDPK-related kinase (CRK) gene families in tomato: genome-wide identification and functional analyses in disease resistance. Mol Genet Genomics 291:661–676

    Article  CAS  PubMed  Google Scholar 

  • Waters BM, Amundsen K, Graef G (2018) Gene expression profiling of iron deficiency chlorosis sensitive and tolerant soybean indicates key roles for phenylpropanoids under alkalinity stress. Front Plant Sci 9:00010

    Article  Google Scholar 

  • Watillon B, Kettmann R, Boxus P, Burny A (1995) Structure of a calmodulin-binding protein kinase gene from apple. Plant Physiol 108:847–848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei S, Hu W, Deng X, Zhang Y, Liu X, Zhao X, Luo Q, Jin Z, Li Y, Zhou S, Sun T, Wang L, Yang G, He G (2014) A rice calcium-dependent protein kinase OsCPK9 positively regulates drought stress tolerance and spikelet fertility. BMC Plant Biol 14:133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan JW, Guan L, Sun Y, Zhu Y, Liu L, Lu R, Jiang MY, Tan MP, Zhang AY (2015) Calcium and ZmCCaMK are involved in brassinosteroid-induced antioxidant defense in maize leaves. Plant Cell Physiol 56:883–896

    Article  CAS  PubMed  Google Scholar 

  • Yoo BC, Harmon AC (1996) Intramolecular binding contributes to the activation of CDPK, a protein kinase with a calmodulin-like domain. Biochem 35:12029–12037

    Article  CAS  Google Scholar 

  • Zhang L, Liu BF, Liang SP, Jones RL, Lu YT (2002) Molecular and biochemical characterization of a calcium/calmodulin-binding protein kinase from rice. Biochem J 368:145–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang K, Han YT, Zhao FL, Hu Y, Gao YR, Ma YF, Zheng Y, Wang YJ, Wen YQ (2015) Genome-wide identification and expression analysis of the CDPK gene family in grape. BMC Plant Biol 15:1–19

    Article  CAS  Google Scholar 

  • Zhao R, Sun HL, Mei C, Wang XJ, Yan L, Liu R, Zhang XF, Wang XF, Zhang DP (2011) The Arabidopsis Ca2+-dependent protein kinase CPK12 negatively regulates abscisic acid signaling in seed germination and post-germination growth. New Phytol 192:61–73

    Article  CAS  PubMed  Google Scholar 

  • Zhou L, Lan W, Jiang Y, Fang W, Luan S (2014) A calcium-dependent protein kinase interacts with and activates a calcium channel to regulate pollen tube growth. Mol Plant 7:369–376

    Article  CAS  PubMed  Google Scholar 

  • Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, du SY, Wang XF, Wu FQ, Xu YH, Zhang XY, Zhang DP (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019–3036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Y, Yan J, Liu W, Liu L, Sheng Y, Sun Y, Scheller HV, Jiang M, Hou X, Ni L, Zhang A (2016) Phosphorylation of a NAC transcription factor by ZmCCaMK regulates abscisic acid-induced antioxidant defense in maize. Plant Physiol 171:1651–1664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zou JJ, Wei FJ, Wang C, Wu JJ, Ratnasekera D, Liu WX, Wu WH (2010) Arabidopsis calcium-dependent protein kinase CPK10 functions in abscisic acid- and Ca2+-mediated stomatal regulation in response to drought stress. Plant Physiol 154:1232–1243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zuo R, Hu R, Chai G, Xu M, Qi G, Kong Y, Zhou G (2013) Genome-wide identification, classification, and expression analysis of CDPK and its closely related gene families in poplar (Populus trichocarpa). Mol Biol Rep 40:2645–2662

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was financially supported by the Joint Fund of the Natural Science Foundation of China and the Karst Science Research Center of Guizhou Province (Grant No. U1812401), the Programme for Changjiang Scholars and Innovative Research Teams in Universities (PCSIRT–1227), the Initial Fund for Key Laboratories of Guizhou Province (2011-4005), the Major Science and Technology Project of the Education Department of Guizhou Province during the “12th Five-year Plan” (2012-005), the Joint Fund for the Department of Science and Technology of Guizhou Province and Guizhou Normal University ([2016]7209, [2010]19), the National Key Research and Development Program of China (2017YFC0506102), and the Natural Science Foundation of China (NSFC) (31570586, 31870581). We acknowledge TopEdit LLC for the linguistic editing during the preparation of this manuscript.

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Authors and Affiliations

  1. Key Laboratory for Subtropical Wetland Ecosystem Research of MOE, College of the Environment and Ecology, Xiamen University, Xiamen, Fujian, 361102, People’s Republic of China

    Xi-Min Zhang, Zhi-Jun Shen, Gui-Feng Gao & Hai-Lei Zheng

  2. The Key Laboratory for Biodiversity Conservation in Karst Mountain Area of Southwest of Forestry Ministry in China, Key Laboratory of Plant Physiology and Development Regulation, School of Life Science, Guizhou Normal University, Guiyang, Guizhou, 550001, People’s Republic of China

    Xi-Min Zhang, Lun-Xian Liu, Zhi-Meng Su, Jing Tang & Yin Yi

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Contributions

X. M. Z. designed the experiments. X. M. Z., L. X. L. and Z. M. S performed the experiments. Z. J. S. and G. F. G. analyzed transcriptome data. J. T. made the heat map. X. M. Z. wrote the paper. Y. Y. and H. L. Z. revised this paper. All authors have read and approved the manuscript.

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Correspondence to Yin Yi or Hai-Lei Zheng.

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Zhang, XM., Liu, LX., Su, ZM. et al. Expression analysis of calcium-dependent protein kinases (CDPKs) superfamily genes in Medicago lupulina in response to high calcium, carbonate and drought. Plant Soil 441, 219–234 (2019). https://doi.org/10.1007/s11104-019-04109-7

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