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Genome-wide identification, classification, evolutionary analysis and gene expression patterns of the protein kinase gene family in wheat and Aegilops tauschii

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In this study we systematically identified and classified PKs in Triticum aestivum, Triticum urartu and Aegilops tauschii. Domain distribution and exon–intron structure analyses of PKs were performed, and we found conserved exon–intron structures within the exon phases in the kinase domain. Collinearity events were determined, and we identified various T. aestivum PKs from polyploidizations and tandem duplication events. Global expression pattern analysis of T. aestivum PKs revealed that some PKs might participate in the signaling pathways of stress response and developmental processes. QRT-PCR of 15 selected PKs were performed under drought treatment and with infection of Fusarium graminearum to validate the prediction of microarray.

Abstract

The protein kinase (PK) gene superfamily is one of the largest families in plants and participates in various plant processes, including growth, development, and stress response. To better understand wheat PKs, we conducted genome-wide identification, classification, evolutionary analysis and expression profiles of wheat and Ae. tauschii PKs. We identified 3269, 1213 and 1448 typical PK genes in T. aestivum, T. urartu and Ae. tauschii, respectively, and classified them into major groups and subfamilies. Domain distributions and gene structures were analyzed and visualized. Some conserved intron–exon structures within the conserved kinase domain were found in T. aestivum, T. urartu and Ae. tauschii, as well as the primitive land plants Selaginella moellendorffii and Physcomitrella patens, revealing the important roles and conserved evolutionary history of these PKs. We analyzed the collinearity events of T. aestivum PKs and identified PKs from polyploidizations and tandem duplication events. Global expression pattern analysis of T. aestivum PKs revealed tissue-specific and stress-specific expression profiles, hinting that some wheat PKs may regulate abiotic and biotic stress response signaling pathways. QRT-PCR of 15 selected PKs were performed under drought treatment and with infection of F. graminearum to validate the prediction of microarray. Our results will provide the foundational information for further studies on the molecular functions of wheat PKs.

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Abbreviations

PK:

Protein kinase

AGC:

PKA–PKG–PKC

CAMK:

Calcium- and calmodulin-regulated kinase

CDPK:

Calcium-dependent PKs

CK1:

Casein kinase 1

CMGC:

Cyclin-dependent kinases, mitogen-activated protein kinases, glycogen synthase kinase and cyclin-dependent-like kinases

RLK:

Receptor-like kinase

LRR:

Leucine-rich repeat

RLCK:

Receptor-like cytoplasmic kinase

TK:

Tyrosine kinase

TKL:

Tyrosine kinase-like kinase

References

  • Acharya BR et al (2007) Overexpression of CRK13, an Arabidopsis cysteine-rich receptor-like kinase, results in enhanced resistance to Pseudomonas syringae. Plant J 50:488–499

    Article  CAS  PubMed  Google Scholar 

  • Ben-Nissan G, Cui W, Kim DJ, Yang Y, Yoo BC, Lee JY (2008) Arabidopsis casein kinase 1-like 6 contains a microtubule-binding domain and affects the organization of cortical microtubules. Plant Physiol 148:1897–1907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bittner T, Campagne S, Neuhaus G, Rensing SA, Fischer-Iglesias C (2013) Identification and characterization of two wheat glycogen synthase kinase 3/ SHAGGY-like kinases. BMC Plant Biol 13:64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bittner T, Nadler S, Schulze E, Fischer-Iglesias C (2015) Two homolog wheat glycogen synthase kinase 3/SHAGGY—like kinases are involved in brassinosteroid signaling. BMC Plant Biol 15:247

    Article  PubMed  PubMed Central  Google Scholar 

  • Brenchley R et al (2012) Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491:705–710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chain F, Cote-Beaulieu C, Belzile F, Menzies JG, Belanger RR (2009) A comprehensive transcriptomic analysis of the effect of silicon on wheat plants under control and pathogen stress conditions. Mol Plant Microbe Interact 22:1323–1330

    Article  CAS  PubMed  Google Scholar 

  • Champion A, Kreis M, Mockaitis K, Picaud A, Henry Y (2004) Arabidopsis kinome: after the casting. Funct Integr Genomics 4:163–187

    Article  CAS  PubMed  Google Scholar 

  • Choulet F et al (2014) Structural and functional partitioning of bread wheat chromosome 3B. Science 345:1249721

    Article  PubMed  Google Scholar 

  • Christov NK, Christova PK, Kato H, Liu Y, Sasaki K, Imai R (2014) TaSK5, an abiotic stress-inducible GSK3/shaggy-like kinase from wheat, confers salt and drought tolerance in transgenic Arabidopsis. Plant Physiol Biochem 84:251–260

    Article  CAS  PubMed  Google Scholar 

  • Cloutier S, Wang Z, Jordan MC (2008) Gene expression of plant defence pathways using Lr1 transgenic lines and the Affymetrix wheat chip. Sydney University Press, Sydney

    Google Scholar 

  • De Smet I, Voss U, Jurgens G, Beeckman T (2009) Receptor-like kinases shape the plant. Nat Cell Biol 11:1166–1173

    Article  PubMed  Google Scholar 

  • Ederli L et al (2011) The Arabidopsis thaliana cysteine-rich receptor-like kinase CRK20 modulates host responses to Pseudomonas syringae pv. tomato DC3000 infection. J Plant Physiol 168:1784–1794

    Article  CAS  PubMed  Google Scholar 

  • Feldman M, Levy AA (2009) Genome evolution in allopolyploid wheat—a revolutionary reprogramming followed by gradual changes. J Genet Genom 36:511–518

    Article  CAS  Google Scholar 

  • Gao LL, Xue HW (2012) Global analysis of expression profiles of rice receptor-like kinase genes. Mol Plant 5:143–153

    Article  CAS  PubMed  Google Scholar 

  • Ghorbel M, Zaidi I, Robe E, Ranty B, Mazars C, Galaud JP, Hanin M (2015) The activity of the wheat MAP kinase phosphatase 1 is regulated by manganese and by calmodulin. Biochimie 108:13–19

    Article  CAS  PubMed  Google Scholar 

  • Hanks SK, Hunter T (1995) Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 9:576–596

    CAS  PubMed  Google Scholar 

  • Hanks SK, Quinn AM, Hunter T (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42–52

    Article  CAS  PubMed  Google Scholar 

  • Hao L, Wen Y, Zhao Y, Lu W, Xiao K (2015) Wheat mitogen-activated protein kinase gene TaMPK4 improves plant tolerance to multiple stresses through modifying root growth, ROS metabolism, and nutrient acquisitions. Plant Cell Rep 34:2081–2097

    Article  CAS  PubMed  Google Scholar 

  • Ji H, Pardo JM, 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  PubMed  Google Scholar 

  • Jiang Z et al (2013) RLP1.1, a novel wheat receptor-like protein gene, is involved in the defence response against Puccinia striiformis f. sp. tritici. J Exp Bot 64:3735–3746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kadam S et al (2012) Genomic associations for drought tolerance on the short arm of wheat chromosome 4B. Funct Integr Genom 12:447–464

    Article  CAS  Google Scholar 

  • Kozik A, Kochetkova E, Michelmore R (2002) GenomePixelizer–a visualization program for comparative genomics within and between species. Bioinformatics 18:335–336

    Article  CAS  PubMed  Google Scholar 

  • Krupnova T et al (2009) Microtubule-associated kinase-like protein RUNKEL needed  for cell plate expansion in Arabidopsis cytokinesis. Curr Biol 19:518–523

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • Larkin MA et al (2007) Clustal W and clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Lee WS, Rudd JJ, Hammond-Kosack KE, Kanyuka K (2014) Mycosphaerella graminicola LysM effector-mediated stealth pathogenesis subverts recognition through both CERK1 and CEBiP homologues in wheat. Mol Plant Microbe Interact 27:236–243

    Article  CAS  PubMed  Google Scholar 

  • Lehti-Shiu MD, Shiu SH (2012) Diversity, classification and function of the plant protein kinase superfamily. Philos Trans R Soc Lond B Biol Sci 367:2619–2639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lehti-Shiu MD, Zou C, Hanada K, Shiu SH (2009) Evolutionary history and stress regulation of plant receptor-like kinase/pelle genes. Plant Physiol 150:12–26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li AL et al (2008) Evolutionary and functional study of the CDPK gene family in wheat (Triticum aestivum L.). Plant Mol Biol 66:429–443

    Article  CAS  PubMed  Google Scholar 

  • Lin W, Ma X, Shan L, He P (2013) Big roles of small kinases: the complex functions of receptor-like cytoplasmic kinases in plant immunity and development. J Integr Plant Biol 55:1188–1197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ling HQ et al (2013) Draft genome of the wheat a-genome progenitor Triticum urartu. Nature 496:87–90

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Chen N, Grant JN, Cheng ZM, Stewart CN Jr, Hewezi T (2015) Soybean kinome: functional classification and gene expression patterns. J Exp Bot 66:1919–1934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma J, Stiller J, Wei Y, Zheng YL, Devos KM, Dolezel J, Liu C (2014) Extensive pericentric rearrangements in the bread wheat (Triticum aestivum L.) genotype “Chinese Spring” revealed from chromosome shotgun sequence data. Genom Biol Evol 6:3039–3048

    Article  CAS  Google Scholar 

  • Ma J et al (2015) Putative interchromosomal rearrangements in the hexaploid wheat (Triticum aestivum L.) genotype ‘Chinese Spring’ revealed by gene locations on homoeologous chromosomes. BMC Evol Biol 15:37

    Article  PubMed  PubMed Central  Google Scholar 

  • Manning G, Plowman GD, Hunter T, Sudarsanam S (2002) Evolution of protein kinase signaling from yeast to man. Trends Biochem Sci 27:514–520

    Article  CAS  PubMed  Google Scholar 

  • Mao X, Zhang H, Tian S, Chang X, Jing R (2010) TaSnRK2.4, an SNF1-type serine/threonine protein kinase of wheat (Triticum aestivum L.), confers enhanced multistress tolerance in Arabidopsis. J Exp Bot 61:683–696

    Article  CAS  PubMed  Google Scholar 

  • Marcussen T et al (2014) Ancient hybridizations among the ancestral genomes of bread wheat. Science 345:1250092

    Article  PubMed  Google Scholar 

  • Mohannath G et al (2014) A complex containing SNF1-related kinase (SnRK1) and adenosine kinase in Arabidopsis. PLoS ONE 9:e87592

    Article  PubMed  PubMed Central  Google Scholar 

  • Motose H et al (2011) NIMA-related kinases 6, 4, and 5 interact with each other to regulate microtubule organization during epidermal cell expansion in Arabidopsis thaliana. Plant J 67:993–1005

    Article  CAS  PubMed  Google Scholar 

  • Niu E, Cai C, Zheng Y, Shang X, Fang L, Guo W (2016) Genome-wide analysis of CrRLK1L gene family in Gossypium and identification of candidate CrRLK1L genes related to fiber development. Mol Genet Genom 291:1137–1154

    Article  CAS  Google Scholar 

  • Nowack MK et al (2012) Genetic framework of cyclin-dependent kinase function in Arabidopsis. Dev Cell 22:1030–1040

    Article  CAS  PubMed  Google Scholar 

  • Ouyang SQ et al (2010) Receptor-like kinase OsSIK1 improves drought and salt stress tolerance in rice (Oryza sativa) plants. Plant J 62:316–329

    Article  CAS  PubMed  Google Scholar 

  • Pitzschke A, Schikora A, Hirt H (2009) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12:421–426

    Article  CAS  PubMed  Google Scholar 

  • Placido DF, Campbell MT, Folsom JJ, Cui X, Kruger GR, Baenziger PS, Walia H (2013) Introgression of novel traits from a wild wheat relative improves drought adaptation in wheat. Plant Physiol 161:1806–1819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi LL et al (2004) A chromosome bin map of 16,000 expressed sequence tag loci and distribution of genes among the three genomes of polyploid wheat. Genetics 168:701–712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rameneni JJ, Lee Y, Dhandapani V, Yu X, Choi SR, Oh MH, Lim YP (2015) Genomic and post-translational modification analysis of Leucine-rich-repeat receptor-like kinases in Brassica rapa. PLoS ONE 10:e0142255

    Article  PubMed  PubMed Central  Google Scholar 

  • Rustenholz C et al (2011) A 3000-loci transcription map of chromosome 3B unravels the structural and functional features of gene islands in hexaploid wheat. Plant Physiol 157:1596–1608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saeed AI et al (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374–378

    CAS  PubMed  Google Scholar 

  • Sakamoto T, Deguchi M, Brustolini OJ, Santos AA, Silva FF, Fontes EP (2012) The tomato RLK superfamily: phylogeny and functional predictions about the role of the LRRII-RLK subfamily in antiviral defense. BMC Plant Biol 12:229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salamini F, Ozkan H, Brandolini A, Schafer-Pregl R, Martin W (2002) Genetics and geography of wild cereal domestication in the near east. Nat Rev Genet 3:429–441

    CAS  PubMed  Google Scholar 

  • Salse J et al (2008) Identification and characterization of shared duplications between rice and wheat provide new insight into grass genome evolution. Plant Cell 20:11–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schreiber AW et al (2009) Comparative transcriptomics in the Triticeae. BMC Genom 10:285

    Article  Google Scholar 

  • Shen W, Reyes MI, Hanley-Bowdoin L (2009) Arabidopsis protein kinases GRIK1 and GRIK2 specifically activate SnRK1 by phosphorylating its activation loop. Plant Physiol 150:996–1005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shiu SH, Bleecker AB (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132:530–543

    Article  CAS  PubMed  Google Scholar 

  • Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, Li WH (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220–1234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh A, Pandey GK (2012) Protein phosphatases: a genomic outlook to understand their function in plants. J Plant Biochem Biotechnol 21:100–107

    Article  CAS  Google Scholar 

  • Smekalova V, Doskocilova A, Komis G, Samaj J (2014) Crosstalk between secondary messengers, hormones and MAPK modules during abiotic stress signalling in plants. Biotechnol Adv 32:2–11

    Article  CAS  PubMed  Google Scholar 

  • Sutton F, Chen DG, Ge X, Kenefick D (2009) Cbf genes of the Fr-A2 allele are differentially regulated between long-term cold acclimated crown tissue of freeze-resistant and—susceptible, winter wheat mutant lines. BMC Plant Biol 9:34

    Article  PubMed  PubMed Central  Google Scholar 

  • Tian S, Mao X, Zhang H, Chen S, Zhai C, Yang S, Jing R (2013) Cloning and characterization of TaSnRK2.3, a novel SnRK2 gene in common wheat. J Exp Bot 64:2063–2080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tufan HA, McGrann GR, Magusin A, Morel JB, Miche L, Boyd LA (2009) Wheat blast: histopathology and transcriptome reprogramming in response to adapted and nonadapted Magnaporthe isolates. New Phytol 184:473–484

    Article  PubMed  Google Scholar 

  • Van Damme D et al (2011) Arabidopsis alpha Aurora kinases function in formative cell division plane orientation. Plant Cell 23:4013–4024

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y et al (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang M, Yue H, Feng K, Deng P, Song W, Nie X (2016) Genome-wide identification, phylogeny and expressional profiles of mitogen activated protein kinase kinase kinase (MAPKKK) gene family in bread wheat (Triticum aestivum L.). BMC Genom 17:668

    Article  Google Scholar 

  • Wei K, Wang Y, Xie D (2014) Identification and expression profile analysis of the protein kinase gene superfamily in maize development. Mol Breed 33:155–172

    Article  CAS  Google Scholar 

  • Wojcik PI, Ouellet T, Balcerzak M, Dzwinel W (2015) Identification of biomarker genes for resistance to a pathogen by a novel method for meta-analysis of single-channel microarray datasets. J Bioinform Comput Biol 13:1550013

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Zhou JM (2013) Receptor-like kinases in plant innate immunity. J Integr Plant Biol 55:1271–1286

    Article  CAS  PubMed  Google Scholar 

  • Wu Y et al. (2016) Genome-wide expression pattern analyses of the Arabidopsis leucine-rich repeat receptor-like kinases. Mol Plant 9:289–300

    Article  CAS  PubMed  Google Scholar 

  • Xing HT, Guo P, Xia XL, Yin WL (2011) PdERECTA, a leucine-rich repeat receptor-like kinase of poplar, confers enhanced water use efficiency in Arabidopsis. Planta 234:229–241

    Article  CAS  PubMed  Google Scholar 

  • Yang K, Rong W, Qi L, Li J, Wei X, Zhang Z (2013) Isolation and characterization of a novel wheat cysteine-rich receptor-like kinase gene induced by Rhizoctonia cerealis. Sci Rep 3:3021

    Article  PubMed  PubMed Central  Google Scholar 

  • Youn JH, Kim TW (2015) Functional insights of plant GSK3-like kinases: multi-taskers in diverse cellular signal transduction pathways. Mol Plant 8:552–565

    Article  CAS  PubMed  Google Scholar 

  • Zaidi I, Ebel C, Belgaroui N, Ghorbel M, Amara I, Hanin M (2016) The wheat MAP kinase phosphatase 1 alleviates salt stress and increases antioxidant activities in Arabidopsis. J Plant Physiol 193:12–21

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Mao X, Jing R, Chang X, Xie H (2011) Characterization of a common wheat (Triticum aestivum L.) TaSnRK2.7 gene involved in abiotic stress responses. J Exp Bot 62:975–988

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Han X, Shi R, Yang G, Qi L, Wang R, Li G (2013a) Arabidopsis cysteine-rich receptor-like kinase 45 positively regulates disease resistance to Pseudomonas syringae. Plant Physiol Biochem 73:383–391

    Article  CAS  PubMed  Google Scholar 

  • Zhang X et al (2013b) Arabidopsis cysteine-rich receptor-like kinase 45 functions in the responses to abscisic acid and abiotic stresses. Plant Physiol Biochem 67:189–198

    Article  CAS  PubMed  Google Scholar 

  • Zulawski M, Schulze G, Braginets R, Hartmann S, Schulze WX (2014) The Arabidopsis Kinome: phylogeny and evolutionary insights into functional diversification. BMC Genomics 15:548

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank Prof. An-Yuan Guo (Huazhong University of Science and Technology) for advice on this study, Prof. Wei Wang (Shandong Agricultural University) for providing wheat seeds (DR0621 and DS0621), and Dr. D. Garvin (USDA-ARS in the USA) for providing wheat seeds (Apogee and Apogee73S2). This work was supported by the following funds to L.R.K: National Natural Science Foundation of China (31471488), NSFC 31520103911. This work was also supported by the funds to JY: Young Teacher innovation fund of Shandong Agricultural University (140-23848).

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JY, EN and LRK conceived and designed the experiments, JY performed the experiments. PSS performed the qRT-PCR. JY, ZRW and LRK wrote and revised the manuscript.

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Correspondence to Eviatar Nevo or Lingrang Kong.

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Yan, J., Su, P., Wei, Z. et al. Genome-wide identification, classification, evolutionary analysis and gene expression patterns of the protein kinase gene family in wheat and Aegilops tauschii . Plant Mol Biol 95, 227–242 (2017). https://doi.org/10.1007/s11103-017-0637-1

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