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Functional genomics of the protein kinase superfamily from wheat

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Abstract

Protein kinases (PKs) belonging to a large superfamily play vital roles in plant development and stress tolerance, whereas only a small number of PKs have been functionally studied in wheat. Genome-wide survey and characterization of wheat PK genes (TaPKs) will be valuable in future genetic improvement program. In this study, we performed genome-wide identification of PK in wheat, containing phylogenetic evolution, gene expression pattern, and functional prediction analysis, and to explore structure–function relationship, the secondary and tertiary structures of wheat OST1 were visualized. Totally, 4479 TaPKs composed of 4446 Ser/Thr/Tyr (TaPK1 to TaPK4446) and 33 His PKs (TaHPK1 to TaHPK33) were identified in the TGACv1 assembly. According to phylogenetic analysis, wheat Ser/Thr/Tyr PKs were categorized into eight groups with 57 families and 64 subfamilies, and His PKs were classified into three families. The genes contained on average 5.07 introns, ranging from 0 to 31, and about 54.68% TaPKs exhibited relatively simpler exon–intron organization (0–4 introns). RNA-seq analysis showed 324 TaPKs were significantly differentially expressed after exposure to drought, 372 TaPKs were significantly differentially expressed after inoculation with Puccinia striiformis f. sp. tritici (Pst) and Blumeria graminis f. sp. tritici (Bgt), and a large number of TaPKs exhibited stage- or organ-specific expression patterns. Co-expression analysis showed that 1388 TaPKs were distributed in 19 modules, while 9 modules with 511 TaPKs had the most obvious tissue- or stress-specific expression trends. A suite of sexual reproduction related genes were identified in magenta module where TaPK960, TaPK7073708, TaPK4243, and TaPK4249 were related to polarized pollen tube growth, TaPK627 and TaPK629 to pollen tube guidance, and TaPK42264228 to flowering time regulation. Finally, 12 TaPKs were selected to validate their expression level through qRT-PCR. Our findings obtained will offer a clue to elaborate the roles of PKs in wheat growth and stress resistance for agricultural improvement.

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Abbreviations

ABA :

abscisic acid

Bgt :

Blumeria graminis f. sp. tritici

BRs :

brassinosteroids

CKs :

cytokinins

CV :

coefficient of variation

DEG :

differentially expressed genes

dpi :

day post-inoculation

DS1h :

in drought stress after 1 h

DS6h :

in drought stress after 6 h

ET :

ethylene

FF1 :

fruit at whole plant fruit formation stage 30 to 50%

FF2 :

Fruit at whole plant fruit formation stage 70% to final size

FR :

fruit at whole plant fruit ripening stage

GA :

gibberellin

GO :

Gene Ontology

IFL.02 :

inflorescence at 1/2 of flowers open stage

ISE.02 :

inflorescence at two nodes or internodes visible stage

ISE.99 :

inflorescence at maximum stem length reached stage

JA :

jasmonic acid

KEGG :

Kyoto Encyclopedia of Genes and Genomes

L3N :

leaf at main shoot and axillary shoots visible at three nodes stage

LCE :

leaf at cotyledon emergence stage

LF1 :

leaf at whole plant fruit formation stage 30 to 50%

PK :

protein kinase

Pst :

Puccinia striiformis f. sp. tritici

RCE :

root at cotyledon emergence stage

RLP.03 :

root at three leaves visible stage

RSE.99 :

root at maximum stem length reached stage

SA :

salicylic acid

SFL.02 :

stem at 1/2 of flowers open stage

SSE.00 :

stem at stem elongation begins stage

SSE.02 :

stem at two nodes or internodes visible stage

TaPK :

wheat protein kinase

WGCNA :

weighted gene co-expression network analysis

References

  • Aarts MG, Keijzer CJ, Stiekema WJ, Pereira A (1995) Molecular characterization of the CER1 gene of arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Plant Cell 7:2115–2127

    CAS  PubMed  PubMed Central  Google Scholar 

  • Agueci F, Rutten T, Demidov D, Houben A (2011) Arabidopsis AtNek2 kinase is essential and associates with microtubules. Plant Mol Biol Report 30:339–348

    Google Scholar 

  • Agyemang D, Axel DZ, Marie B et al (2015) Identification and characterization of an ABA-activated MAP kinase cascade in Arabidopsis thaliana. Plant J 82:232–244

    Google Scholar 

  • Anne G, Virginie S, Francine G et al (2006) Lectin receptor kinases participate in protein-protein interactions to mediate plasma membrane-cell wall adhesions in Arabidopsis. Plant Physiol 140:81–90

    Google Scholar 

  • Ashwani P, Anupama S, Manoj K et al (2006) Whole-genome analysis of Oryza sativa reveals similar architecture of two-component signaling machinery with Arabidopsis. Plant Physiol 142:380–397

    Google Scholar 

  • Bemis SM, Lee JS, Shpak ED, Torii KU (2013) Regulation of floral patterning and organ identity by Arabidopsis ERECTA-family receptor kinase genes. J Exp Bot 64:5323–5333

    CAS  PubMed  Google Scholar 

  • Bouwmeester K, Govers F (2009) Arabidopsis L-type lectin receptor kinases: phylogeny, classification, and expression profiles. J Exp Bot 60:4383–4396

    CAS  PubMed  Google Scholar 

  • Brandt B, Schroeder JI (2012) Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action. Proc Natl Acad Sci U S A 109:10593–10598

    CAS  PubMed  PubMed Central  Google Scholar 

  • Briggs WR, Christie JM (2002) Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci 7:204–210

    CAS  PubMed  Google Scholar 

  • Candace M, Romanowsky Shawn M, Barron Yoshimi D et al (2010) Calcium-dependent protein kinases regulate polarized tip growth in pollen tubes. Plant J Cell Mol Biol 59:528–539

    Google Scholar 

  • Chang C, Kwok SF, Bleecker AB, Meyerowitz EM (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262(80):539–544

    CAS  PubMed  Google Scholar 

  • Chen K, Durand D, Farach-Colton M (2000) NOTUNG: a program for dating gene duplications and optimizing gene family trees. J Comput Biol 7:429–447

    CAS  PubMed  Google Scholar 

  • Chenyu S, Cheng Q, Hongyan R et al (2015) Ethylene mediates brassinosteroid-induced stomatal closure via Gα protein-activated hydrogen peroxide and nitric oxide production in Arabidopsis. Plant J 82:280–301

    Google Scholar 

  • Christophe B, Pierre-Olivier DF, Clara B et al (2006) Identification of features regulating OST1 kinase activity and OST1 function in guard cells. Plant Physiol 141:1316–1327

    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

    CAS  PubMed  Google Scholar 

  • Clavijo BJ, Venturini L, Schudoma C, et al (2017). An improved assembly and annotation of the allohexaploid wheat genome identifies complete families of agronomic genes and provides genomic evidence for chromosomal translocations. Genome Res 27:885–896

  • Clouse SD (2011) Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 23:1219–1230

    CAS  PubMed  PubMed Central  Google Scholar 

  • Conglin H, Shuo D, Hua Z et al (2011) CIPK7 is involved in cold response by interacting with CBL1 in Arabidopsis thaliana. Plant Sci 181:57–64

    Google Scholar 

  • Deng X, Zhou S, Hu W et al (2013) Ectopic expression of wheat TaCIPK14, encoding a calcineurin B-like protein-interacting protein kinase, confers salinity and cold tolerance in tobacco. Physiol Plant 149:367–377

    CAS  PubMed  Google Scholar 

  • Deping H, Cun W, Junna H et al (2012) A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis. Plant Cell 24:2546–2561

    Google Scholar 

  • DeYoung BJ, Bickle KL, Schrage KJ et al (2010) The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J 45:1–16

    Google Scholar 

  • Dongtao R, Yidong L, Kwang-Yeol Y et al (2008) A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc Natl Acad Sci U S A 105:5638–5643

    Google Scholar 

  • Elich TD, Chory J (1997) Phytochrome: if it looks and smells like a histidine kinase, is it a histidine kinase? Cell 91:713–716

    CAS  PubMed  Google Scholar 

  • Enugutti B, Schneitz K (2013) Genetic analysis of ectopic growth suppression during planar growth of integuments mediated by the Arabidopsis AGC protein kinase UNICORN. BMC Plant Biol 13:1–9

    Google Scholar 

  • Fabien J, Xiaohua Y, Shunyuan X, June MK (2011) Two Arabidopsis guard cell-preferential MAPK genes, MPK9 and MPK12, function in biotic stress response. Plant Signal Behav 6:1875–1877

    Google Scholar 

  • Fatemeh DN (2014) Identification of transcription factors linked to cell cycle regulation in Arabidopsis. Plant Signal Behav 9:e972864. https://doi.org/10.4161/15592316.2014.972864

    Article  CAS  Google Scholar 

  • Feng L, Gao Z, Xiao G, Huang R, Zhang H (2014) Leucine-rich repeat receptor-like kinase FON1 regulates drought stress and seed germination by activating the expression of ABA-responsive genes in rice. Plant Mol Biol Report 32:1158–1168

    CAS  Google Scholar 

  • Fionn ML, Galvan-Ampudia Carlos S, Julkowska Magdalena M et al (2012) The Snf1-related protein kinases SnRK2.4 and SnRK2.10 are involved in maintenance of root system architecture during salt stress. Plant J 72:436–449

    Google Scholar 

  • Florina V, Silvia R, Americo R et al (2009) Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis. Plant Cell 21:3170–3184

    Google Scholar 

  • Gili B-N, Weier C, Dong-Jin K et al (2008) Arabidopsis casein kinase 1-like 6 contains a microtubule-binding domain and affects the organization of cortical microtubules. Plant Physiol 148:1897–1907

    Google Scholar 

  • Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor–like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011

    PubMed  Google Scholar 

  • Guan Y, Zhang S (2014) Two mitogen-activated protein kinases, MPK3 and MPK6, are required for funicular guidance of pollen tubes in Arabidopsis. Plant Physiol 165:528–533

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ha Y, Shang Y, Nam KH (2016) Brassinosteroids modulate ABA-induced stomatal closure in Arabidopsis. J Exp Bot 67:6297–6308

    CAS  PubMed  PubMed Central  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 

  • He X, Tian J, Yang L, Huang Y, Zhao B, Zhou C, Ge R, Shen Y, Huang Z (2012) Overexpressing a glycogen synthase kinase gene from wheat, TaGSK1, enhances salt tolerance in transgenic Arabidopsis. Plant Mol Biol Report 30:807–816

    CAS  Google Scholar 

  • Hiroaki F, Paul EV, Jian-Kang Z (2011) Arabidopsis decuple mutant reveals the importance of SnRK2 kinases in osmotic stress responses in vivo. Proc Natl Acad Sci U S A 108:1717–1722

    Google Scholar 

  • Hon WC, Mckay GA, Thompson PR et al (1997) Structure of an enzyme required for aminoglycoside antibiotic resistance reveals homology to eukaryotic protein kinases. Cell 89:887–895

    CAS  PubMed  Google Scholar 

  • Hongqing G, Lei L, Huaxun Y et al (2009) Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Plant Signal Behav 106:7648–7653

    Google Scholar 

  • Hwang I, Chen HC, Sheen J (2002) Two-component signal transduction pathways in Arabidopsis. Plant Physiol 129:500–515

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ikematsu S, Tasaka M, Torii KU, Uchida N (2017) ERECTA-family receptor kinase genes redundantly prevent premature progression of secondary growth in the Arabidopsis hypocotyl. New Phytol 213:1697–1709

    CAS  PubMed  Google Scholar 

  • Ito T, Ng K-H, Lim T-S, Yu H, Meyerowitz EM (2007) The homeotic protein AGAMOUS controls late stamen development by regulating a jasmonate biosynthetic gene in Arabidopsis. Plant Cell 19:3516–3529

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Jinrong W, Xue-Cheng Z, David N et al (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20:471–481

    Google Scholar 

  • Jung CG, Hwang SG, Park YC, Park HM, Kim DS, Park DH, Jang CS (2015) Molecular characterization of the cold- and heat-induced Arabidopsis PXL1 gene and its potential role in transduction pathways under temperature fluctuations. J Plant Physiol 176:138–146

    CAS  PubMed  Google Scholar 

  • Kamiyoshihara Y, Iwata M, Fukaya T, Tatsuki M, Mori H (2010) Turnover of LeACS2, a wound-inducible 1-aminocyclopropane-1-carboxylic acid synthase in tomato, is regulated by phosphorylation/dephosphorylation. Plant J 64:140–150

    CAS  PubMed  Google Scholar 

  • Kanaoka Masahiro M, Torii Keiko U (2010) FERONIA as an upstream receptor kinase for polar cell growth in plants. Proc Natl Acad Sci U S A 107:17461–17462

    CAS  PubMed  PubMed Central  Google Scholar 

  • Krupa A, Srinivasan N (2005) Diversity in domain architectures of Ser/Thr kinases and their homologues in prokaryotes. BMC Genomics 6:129

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9:9. https://doi.org/10.1186/1471-2105-9-559

    Article  CAS  Google Scholar 

  • Lawlor DW, Paul MJ (2014) Source/sink interactions underpin crop yield: the case for trehalose 6-phosphate/SnRK1 in improvement of wheat. Front Plant Sci 5:418. https://doi.org/10.3389/fpls.2014.00418

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee SJ, Lee MH, Kim JI, Kim SY (2015) Arabidopsis putative MAP kinase kinase kinases Raf10 and Raf11 are positive regulators of seed dormancy and ABA response. Plant Cell Physiol 56:84–97

    CAS  PubMed  Google Scholar 

  • Lehtishiu MD, Shiu SH (2012) Diversity, classification and function of the plant protein kinase superfamily. Philos Trans R Soc London 367:2619–2639

    CAS  Google Scholar 

  • Leonie S, Anette M, Till I et al (2015) Vacuolar CBL-CIPK12 Ca(2+)-sensor-kinase complexes are required for polarized pollen tube growth. Curr Biol 25:1475–1482

    Google Scholar 

  • Leydon A, Beale K, Woroniecka K et al (2013) Three MYB transcription factors control pollen tube differentiation required for sperm release. Curr Biol Cb 23:1209–1214

    CAS  PubMed  Google Scholar 

  • Li CH, Sun Y (2014) The receptor-like kinase SIT1 mediates salt sensitivity by activating MAPK3/6 and regulating ethylene homeostasis in rice. Plant Cell 26:2538–2553

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Ding Y, Shi Y, Zhang X, Zhang S, Gong Z, Yang S (2017) MPK3- and MPK6-mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis. Dev Cell 43:630–642

    CAS  PubMed  Google Scholar 

  • Liang Y, Kangcheng W, Peng G et al (2014) GsLRPK, a novel cold-activated leucine-rich repeat receptor-like protein kinase from Glycine soja, is a positive regulator to cold stress tolerance. Plant Sci 215-216:19–28

    Google Scholar 

  • Li-Na Z, Li-Ke S, Wen-Zheng Z et al (2013) Ca2+-dependent protein kinase11 and 24 modulate the activity of the inward rectifying K+ channels in Arabidopsis pollen tubes. Plant Cell 25:649–661

    Google Scholar 

  • Lingan K, Honghai G, Mingze S (2015) Signal transduction during wheat grain development. Planta 241:789–801

    Google Scholar 

  • Lionel N, Rajendra B, Patrick A et al (2008) DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr Biol 18:650–655

    Google Scholar 

  • Liu J, Zhong S, Guo X, Hao L, Wei X, Huang Q, Hou Y, Shi J, Wang C, Gu H, Qu LJ (2013) Membrane-bound RLCKs LIP1 and LIP2 are essential male factors controlling male-female attraction in Arabidopsis. Curr Biol 23:993–998

    CAS  PubMed  Google Scholar 

  • Liu Z, Xin M, Qin J et al (2015) Temporal transcriptome profiling reveals expression partitioning of homeologous genes contributing to heat and drought acclimation in wheat (Triticum aestivum L.). BMC Plant Biol 15:1–20

    Google Scholar 

  • Liu S, Hua L, Dong S et al (2016) OsMAPK6, a mitogen-activated protein kinase, influences rice grain size and biomass production. Plant J 84:672–681

    Google Scholar 

  • Lu C-A, Lin C-C, Lee K-W, Chen JL, Huang LF, Ho SL, Liu HJ, Hsing YI, Yu SM (2007) The SnRK1A protein kinase plays a key role in sugar signaling during germination and seedling growth of rice. Plant Cell 19:2484–2499

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ma H, Chen J, Zhang Z, Ma L, Yang Z, Zhang Q, Li X, Xiao J, Wang S (2017) MAPK kinase 10.2 promotes disease resistance and drought tolerance by activating different MAPKs in rice. Plant J Cell Mol Biol 92:557–570

    CAS  Google Scholar 

  • Marie B, Matthew RW, Matthew M et al (2010) Differential innate immune signalling via Ca(2+) sensor protein kinases. Nature 464:418–422

    Google Scholar 

  • Martínez-Noël G, Nagaraj VJ, Caló G, Wiemken A, Pontis HG (2007) Sucrose regulated expression of a Ca2+-dependent protein kinase (TaCDPK1) gene in excised leaves of wheat. Plant Physiol Biochem 45:410–419

    PubMed  Google Scholar 

  • Morrone D, Chen X, Coates RM, Peters RJ (2010) Characterization of the kaurene oxidase CYP701A3, a multifunctional cytochrome P450 from gibberellin biosynthesis. Biochem J 431(3):337–344. https://doi.org/10.1042/BJ20100597

    Article  CAS  PubMed  Google Scholar 

  • Norihito N, Masaya M-K, Eriko S et al (2002) Compilation and characterization of a novel WNK family of protein kinases in Arabiodpsis thaliana with reference to circadian rhythms. J Agric Chem Soc Japan 66:2429–2436

    Google Scholar 

  • Nowack M, Harashima H, Dissmeyer N et al (2012) Genetic framework of cyclin-dependent kinase function in Arabidopsis. Dev Cell 22:1030–1040

    CAS  PubMed  Google Scholar 

  • Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL (2016) Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc 11:1650–1667

    CAS  PubMed  PubMed Central  Google Scholar 

  • Quan-Sheng Q, Yan G, Dietrich Margaret A et al (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci U S A 99:8436–8441

    Google Scholar 

  • Róbert D, Günter B, Aladár P-S et al (2007) The Arabidopsis mitogen-activated protein kinase kinase MKK3 is upstream of group C mitogen-activated protein kinases and participates in pathogen signaling. Plant Cell 19:3266–3279

    Google Scholar 

  • Saori M, Takashi M, Nami SO et al (2009) ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr Biol 19:1327–1331

    Google Scholar 

  • Shakirova F, Allagulova C, Maslennikova D, Fedorova K, Yuldashev R, Lubyanova A, Bezrukova M, Avalbaev A (2016) Involvement of dehydrins in 24-epibrassinolide-induced protection of wheat plants against drought stress. Plant Physiol Biochem 108:539–548

    CAS  PubMed  Google Scholar 

  • Shou-Ling X, Abidur R, Tobias IB, Joseph JK (2008) Two leucine-rich repeat receptor kinases mediate signaling, linking cell wall biosynthesis and ACC synthase in Arabidopsis. Plant Cell 20:3065–3079

    Google Scholar 

  • Simon C, Langlois-Meurinne M, Didierlaurent L et al (2014) The secondary metabolism glycosyltransferases UGT73B3 and UGT73B5 are components of redox status in resistance of Arabidopsis to Pseudomonas syringae pv. tomato. Plant Cell Environ 37:1114–1129

    CAS  PubMed  Google Scholar 

  • Singh A, Breja P, Khurana JP, Khurana P (2016) Wheat Brassinosteroid-Insensitive1 (TaBRI1) interacts with members of TaSERK gene family and cause early flowering and seed yield enhancement in Arabidopsis. PLoS One 11:e0153273

    PubMed  PubMed Central  Google Scholar 

  • Soon FF, Ng LM, Zhou XE et al (2012) Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science 335(80):85–88

    CAS  PubMed  Google Scholar 

  • Stephanie D, David C, Polly L et al (2009) The calmodulin-related calcium sensor CML42 plays a role in trichome branching. J Biol Chem 284:31647–31657

    Google Scholar 

  • Takahashi Y, Soyano T, Kosetsu K, Sasabe M, Machida Y (2010) HINKEL kinesin, ANP MAPKKKs and MKK6/ANQ MAPKK, which phosphorylates and activates MPK4 MAPK, constitute a pathway that is required for cytokinesis in Arabidopsis thaliana. Plant Cell Physiol 51:1766–1776

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takamitsu K, Jumpei H, Hiroshi N et al (2010) Regulation of microbe-associated molecular pattern-induced hypersensitive cell death, phytoalexin production, and defense gene expression by calcineurin B-like protein-interacting protein kinases, OsCIPK14/15, in rice cultured cells. Plant Physiol 153:678–692

    Google Scholar 

  • Tamara K, Michiko S, Luam G et al (2009) Microtubule-associated kinase-like protein RUNKEL needed for cell plate expansion in Arabidopsis cytokinesis. Curr Biol Cb 19:518–523

    Google Scholar 

  • Toshiro I, Frank W, Hao Y et al (2004) The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 430:356–360

    Google Scholar 

  • Trotta A, Suorsa M, Rantala M, Lundin B, Aro EM (2016) Serine and threonine residues of plant STN7 kinase are differentially phosphorylated upon changing light conditions and specifically influence the activity and stability of the kinase. Plant J 87:484–494

    CAS  PubMed  Google Scholar 

  • Tsuneaki A, Guillaume T, Joulia P et al (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–983

    Google Scholar 

  • Urao T, Yakubov B, Satoh R et al (1999) A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11:1743–1754

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vaid N, Pandey P, Srivastava VK, Tuteja N (2015) Pea lectin receptor-like kinase functions in salinity adaptation without yield penalty, by alleviating osmotic and ionic stresses and upregulating stress-responsive genes. Plant Mol Biol 88:193–206

    CAS  PubMed  Google Scholar 

  • Vilela B, Nájar E, Lumbreras V, Leung J, Pagès M (2015a) Casein kinase 2 negatively regulates abscisic acid-activated SnRK2s in the core abscisic acid-signaling module. Mol Plant 8:709–721

    CAS  PubMed  Google Scholar 

  • Vilela B, Pagès M, Riera M (2015b) Emerging roles of protein kinase CK2 in abscisic acid signaling. Front Plant Sci 6:966

    PubMed  PubMed Central  Google Scholar 

  • Wang X, Tang C, Deng L, Cai G, Liu X, Liu B, Han Q, Buchenauer H, Wei G, Han D, Huang L, Kang Z (2010a) Characterization of a pathogenesis-related thaumatin-like protein gene TaPR5 from wheat induced by stripe rust fungus. Physiol Plant 139:27–38

    CAS  PubMed  Google Scholar 

  • Wang Y, Liu K, Liao H et al (2010b) The plant WNK gene family and regulation of flowering time in Arabidopsis. Plant Biol 10:548–562

    Google Scholar 

  • Wang C, Lu W, He X, Wang F, Zhou Y, Guo X, Guo X (2016) The cotton mitogen-activated protein kinase kinase 3 functions in drought tolerance by regulating stomatal responses and root growth. Plant Cell Physiol 57:1629–1642

    CAS  PubMed  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

    CAS  Google Scholar 

  • Wenming W, Xuemei C (2004) HUA ENHANCER3 reveals a role for a cyclin-dependent protein kinase in the specification of floral organ identity in Arabidopsis. Development 131:3147

    Google Scholar 

  • Yamada H, Suzuki T, Terada K et al (2001) The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol 42:1017–1023

    CAS  PubMed  Google Scholar 

  • Yamauchi S, Takemiya A, Sakamoto T et al (2016) The plasma membrane H+-ATPase AHA1 plays a major role in stomatal opening in response to blue light. Plant Physiol 171:2731–2743

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yan J, Su P, Wei Z et al (2017) Genome-wide identification, classification, evolutionary analysis and gene expression patterns of the protein kinase gene family in wheat and Aegilops tauschii. Plant Mol Biol 95:1–16

    Google Scholar 

  • Yusuke K, Wataru S (2014) Phosphorylation of photosystem II core proteins prevents undesirable cleavage of D1 and contributes to the fine-tuned repair of photosystem II. Plant J Cell Mol Biol 79:312–321

    Google Scholar 

  • Zhang Y, He J, Mccormick S (2010) Two Arabidopsis AGC kinases are critical for the polarized growth of pollen tubes. Plant J 58:474–484

    Google Scholar 

  • Zhao F, Zheng YF, Zeng T, Sun R, Yang JY, Li Y, Ren DT, Ma H, Xu ZH, Bai SN (2017) Phosphorylation of SPOROCYTELESS/NOZZLE by the MPK3/6 kinase is required for anther development. Plant Physiol 173:2265–2277

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu X, Yang K, Wei X, Zhang Q, Rong W, du L, Ye X, Qi L, Zhang Z (2015) The wheat AGC kinase TaAGC1 is a positive contributor to host resistance to the necrotrophic pathogen Rhizoctonia cerealis. J Exp Bot 66:6591–6603

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760

    CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to the providers who submitted the RNA-seq data to the public expression databases which can be applied freely. We sincerely thank Cui Yin (Shanghai Majorbio Bio-pharm Technology Co., Ltd.) for her great contribution to the data analysis. We also thank Wei Zhang in our laboratory for useful discussions.

Funding

The project was supported by the Science and Technology Cooperation Project of Fujian Province, China (Grant No. 2015I0006). The funding institutions had no direct role in the study design, sample collection, analysis, and interpretation of data, nor in manuscript writing. Annual reports were submitted to the funding institutions tracking the progress of the projects.

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Correspondence to Kaifa Wei.

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Wei, K., Li, Y. Functional genomics of the protein kinase superfamily from wheat. Mol Breeding 39, 141 (2019). https://doi.org/10.1007/s11032-019-1045-9

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  • DOI: https://doi.org/10.1007/s11032-019-1045-9

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