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Temporal role of the receptor-like cytoplasmic kinase gene Stpk-V in wheat-Blumeria graminis f. sp. tritici interaction by RNA-seq analysis

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Abstract

Wheat powdery mildew (Pm) caused by Blumeria graminis f. sp. tritici (Bgt) is a widespread epidemic disease in wheat. Haynaldia villosa, a diploid wild relative of wheat, has been widely utilized in wheat breeding for Pm resistance as a broad-spectrum resistance (BSR) resource. A previous study reported a Serine/threonine protein kinase-V (Stpk-V) gene from H. villosa showing BSR to wheat Pm. To deduce the defense network regulated by Stpk-V, we performed temporal RNA-seq of Stpk-V transgenic line (OEStpk-V) and its receptor wheat variety Yangmai 158 during Bgt infection. Gene Ontology enrichment indicated ROS were rapidly activated in OEStpk-V at 1 h after inoculation (hai). The qRT-PCR confirmed the upregulated transcription of ROS related genes OxO and POD, and suppression of ROS scavenging genes SOD and CAT. Besides, four transcription factors genes (WRKY, MYB, ERF, NAC) related to the ROS defense pathway were also enriched. Kyoto encyclopedia of genes and genomes enrichment revealed a remarkable reprogramming of the Ca2+ signalling pathway in OEStpk-V at 1 and 3 hai. qRT-PCR confirmed significantly induced transcription of CDPKs, CALMs, CMLs, and CNGCSs in OEStpk-V. Weighted gene co-expression network analysis classified Stpk-V to the same module in which the Ca2+ signalling related genes were included. Our results indicated that the reprogramming of the ROS accumulation and Ca2+ signalling at initial infection stages plays a crucial role in the Stpk-V regulatory network during wheat-Bgt interaction.

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Data availability

All data generated in this study are included in the paper and the supporting information files.

Code availability

Not applicable.

Abbreviations

Pm:

Powdery mildew

BSR:

Broad-spectrum resistance

WGCNA:

Weighted gene co-expression network analysis

GO:

Gene ontology

KEGG:

Kyoto encyclopedia of genes and genomes

RLKs:

Receptor-like kinases

RLCKs:

Receptor-like cytoplasmic kinases

NLR:

Nucleotide binding and leucine‐rich repeat receptor

Bgt :

Blumeria graminis F. sp. tritici

AGT:

Appressoria germ tube

APP:

Apical appressorium

PGT:

Primary germ tube

SH:

Secondary hyphae

HA:

Hyphal appressoria

DEGs:

Differentially expressed genes

ROS:

Reactive oxygen species

References

  • Adachi H, Nakano T, Miyagawa N, Ishihama N, Yoshioka M, Katou Y, Yaeno T, Shirasu K, Yoshioka H (2015) WRKY transcription factors phosphorylated by MAPK regulate a plant immune NADPH oxidase in Nicotiana benthamiana. Plant Cell 27(9):2645–2663. https://doi.org/10.1105/tpc.15.00213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Averyanov A (2009) Oxidative burst and plant disease resistance. Front Biosci 1:142–152. https://doi.org/10.2741/E14

    Article  Google Scholar 

  • Baudin M, Hassan JA, Schreiber KJ, Lewis JD (2017) Analysis of the ZAR1 immune complex reveals determinants for immunity and molecular interactions. Plant Physiol 174(4):2038–2053. https://doi.org/10.1104/pp.17.00441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bennett FGA (1984) Resistance to powdery mildew in wheat: a review of its use in agriculture and breeding programmes. Plant Pathol 33(3):279–300. https://doi.org/10.1111/j.1365-3059.1984.tb01324.x

    Article  Google Scholar 

  • Bindschedler LV, Minibayeva F, Gardner SL, Gerrish C, Davies DR, Bolwell GP (2001) Early signalling events in the apoplastic oxidative burst in suspension cultured French bean cells involve cAMP and Ca2+. New Phytol 151(1):185–194. https://doi.org/10.1046/j.1469-8137.2001.00170.x

    Article  CAS  PubMed  Google Scholar 

  • Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406. https://doi.org/10.1146/annurev.arplant.57.032905.105346

    Article  CAS  PubMed  Google Scholar 

  • Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, He P, Bush J, Cheng S-H, Sheen J (2010) Differential innate immune signalling via Ca2+ sensor protein kinases. Nature 464(7287):418–422. https://doi.org/10.1038/nature08794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burdon JJ, Thrall PH (2009) Coevolution of plants and their pathogens in natural habitats. Science 324(5928):755–756. https://doi.org/10.1126/science.1171663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao A, Xing L, Wang X, Yang X, Wang W, Sun Y, Qian C, Ni J, Chen Y, Liu D, Wang X, Chen P (2011) Serine/threonine kinase gene Stpk-V, a key member of powdery mildew resistance gene Pm21, confers powdery mildew resistance in wheat. Proc Natl Acad Sci USA 108(19):7727–7732. https://doi.org/10.1073/pnas.1016981108

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen B, Niu F, Liu WZ, Yang B, Zhang J, Ma J, Cheng H, Han F, Jiang YQ (2016) Identification, cloning and characterization of R2R3-MYB gene family in canola (Brassica napus L.) identify a novel member modulating ROS accumulation and hypersensitive-like cell death. DNA Res 23(2):101–114. https://doi.org/10.1093/dnares/dsv040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chigri F, Flosdorff S, Pilz S, Kölle E, Dolze E, Gietl C, Vothknecht UC (2012) The Arabidopsis calmodulin-like proteins AtCML30 and AtCML3 are targeted to mitochondria and peroxisomes, respectively. Plant Mol Biol 78(3):211–222. https://doi.org/10.1007/s11103-011-9856-z

    Article  CAS  PubMed  Google Scholar 

  • Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11(8):539–548. https://doi.org/10.1038/nrg2812

    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 USA 110(21):8744–8749. https://doi.org/10.1073/pnas.1221294110

    Article  PubMed  PubMed Central  Google Scholar 

  • Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LS, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39(6):863–876. https://doi.org/10.1111/j.1365-313X.2004.02171.x

    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(1):e1003127. https://doi.org/10.1371/journal.ppat.1003127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geng S, Zhao Y, Tang L, Zhang R, Sun M, Guo H, Kong X, Li A, Mao L (2011) Molecular evolution of two duplicated CDPK genes CPK7 and CPK12 in grass species: a case study in wheat (Triticum aestivum L.). Gene 475(2):94–103. https://doi.org/10.1016/j.gene.2010.12.015

    Article  CAS  PubMed  Google Scholar 

  • Giri J, Vij S, Dansana PK, Tyagi AK (2011) Rice A20/AN1 zinc-finger containing stress-associated proteins (SAP1/11) and a receptor-like cytoplasmic kinase (OsRLCK253) interact via A20 zinc-finger and confer abiotic stress tolerance in transgenic Arabidopsis plants. New Phytol 191(3):721–732. https://doi.org/10.1111/j.1469-8137.2011.03740.x

    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) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7):644–652. https://doi.org/10.1038/nbt.1883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greenham K, Guadagno CR, Gehan MA, Mockler TC, Weinig C, Ewers BE, McClung CR (2017) Temporal network analysis identifies early physiological and transcriptomic indicators of mild drought in Brassica rapa. Elife 6:e29655. https://doi.org/10.7554/eLife.29655

    Article  PubMed  PubMed Central  Google Scholar 

  • Griffey CA (1993) Effectiveness of adult-plant resistance in reducing grain yield loss to powdery mildew in winter wheat. Plant Dis 77(6):618–622. https://doi.org/10.1094/pd-77-0618

    Article  Google Scholar 

  • Guo L, Guo C, Li M, Wang W, Luo C, Zhang Y, Chen L (2014) Suppression of expression of the putative receptor-like kinase gene NRRB enhances resistance to bacterial leaf streak in rice. Mol Biol Rep 41(4):2177–2187. https://doi.org/10.1007/s11033-014-3069-x

    Article  CAS  PubMed  Google Scholar 

  • Held K, Pascaud F, Eckert C, Gajdanowicz P, Hashimoto K, Corratge-Faillie C, Offenborn JN, Lacombe B, Dreyer I, Thibaud JB, Kudla J (2011) Calcium-dependent modulation and plasma membrane targeting of the AKT2 potassium channel by the CBL4/CIPK6 calcium sensor/protein kinase complex. Cell Res 21(7):1116–1130. https://doi.org/10.1038/cr.2011.50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • International Wheat Genome Sequencing C, investigators IRp, Appels R, Eversole K, Feuillet C, Keller B, Rogers J, Stein N, investigators Iw-gap, Pozniak CJ, Stein N, Choulet F, Distelfeld A, Eversole K, Poland J, Rogers J, Ronen G, Sharpe AG, Whole-genome s, assembly, Pozniak C, Ronen G, Stein N, Barad O, Baruch K, Choulet F, Keeble-Gagnere G, Mascher M, Sharpe AG, Ben-Zvi G, Josselin AA, Hi Cd-bs, Stein N, Mascher M, Himmelbach A, Whole-genome assembly quality c, analyses, Choulet F, Keeble-Gagnere G, Mascher M, Rogers J, Balfourier F, Gutierrez-Gonzalez J, Hayden M, Josselin AA, Koh C, Muehlbauer G, Pasam RK, Paux E, Pozniak CJ, Rigault P, Sharpe AG, Tibbits J, Tiwari V, Pseudomolecule a, Choulet F, Keeble-Gagnere G, Mascher M, Josselin AA, Rogers J, RefSeq genome s, gene a, Spannagl M, Choulet F, Lang D, Gundlach H, Haberer G, Keeble-Gagnere G, Mayer KFX, Ormanbekova D, Paux E, Prade V, Simkova H, Wicker T, Automated a, Choulet F, Spannagl M, Swarbreck D, Rimbert H, Felder M, Guilhot N, Gundlach H, Haberer G, Kaithakottil G, Keilwagen J, Lang D, Leroy P, Lux T, Mayer KFX, Twardziok S, Venturini L, Manual gene c, Appels R, Rimbert H, Choulet F, Juhasz A, Keeble-Gagnere G, Subgenome comparative a, Choulet F, Spannagl M, Lang D, Abrouk M, Haberer G, Keeble-Gagnere G, Mayer KFX, Wicker T, Transposable e, Choulet F, Wicker T, Gundlach H, Lang D, Spannagl M, Phylogenomic a, Lang D, Spannagl M, Appels R, Fischer I, Transcriptome a, data RN-s, Uauy C, Borrill P, Ramirez-Gonzalez RH, Appels R, Arnaud D, Chalabi S, Chalhoub B, Choulet F, Cory A, Datla R, Davey MW, Hayden M, Jacobs J, Lang D, Robinson SJ, Spannagl M, Steuernagel B, Tibbits J, Tiwari V, van Ex F, Wulff BBH, Whole-genome m, Pozniak CJ, Robinson SJ, Sharpe AG, Cory A, Histone mark a, Benhamed M, Paux E, Bendahmane A, Concia L, Latrasse D, tags BACcMI-BW-GP, Rogers J, Jacobs J, Alaux M, Appels R, Bartos J, Bellec A, Berges H, Dolezel J, Feuillet C, Frenkel Z, Gill B, Korol A, Letellier T, Olsen OA, Simkova H, Singh K, Valarik M, van der Vossen E, Vautrin S, Weining S, Chromosome LTCm, physical mapping quality c, Korol A, Frenkel Z, Fahima T, Glikson V, Raats D, Rogers J, mapping RH, Tiwari V, Gill B, Paux E, Poland J, Optical m, Dolezel J, Cihalikova J, Simkova H, Toegelova H, Vrana J, Recombination a, Sourdille P, Darrier B, Gene family a, Appels R, Spannagl M, Lang D, Fischer I, Ormanbekova D, Prade V, family CBFg, Barabaschi D, Cattivelli L, Dehydrin gene f, Hernandez P, Galvez S, Budak H, family NLRg, Steuernagel B, Jones JDG, Witek K, Wulff BBH, Yu G, family PPRg, Small I, Melonek J, Zhou R, Prolamin gene f, Juhasz A, Belova T, Appels R, Olsen OA, family WAKg, Kanyuka K, King R, Stem solidness QTLt, Nilsen K, Walkowiak S, Pozniak CJ, Cuthbert R, Datla R, Knox R, Wiebe K, Xiang D, Flowering locus Cgt, Rohde A, Golds T, Genome size a, Dolezel J, Cizkova J, Tibbits J, MicroRna, t RNAa, Budak H, Akpinar BA, Biyiklioglu S, Genetic m, mapping, Muehlbauer G, Poland J, Gao L, Gutierrez-Gonzalez J, N'Daiye A, libraries BAC, chromosome s, Dolezel J, Simkova H, Cihalikova J, Kubalakova M, Safar J, Vrana J, Bac pooling BAClr, access, Berges H, Bellec A, Vautrin S, sequence I, data r, access, Alaux M, Alfama F, Adam-Blondon AF, Flores R, Guerche C, Letellier T, Loaec M, Quesneville H, Physical m, sequences BA-b, sequencing AB, assembly, Pozniak CJ, Sharpe AG, Walkowiak S, Budak H, Condie J, Ens J, Koh C, Maclachlan R, Tan Y, Wicker T, sequencing BB, assembly, Choulet F, Paux E, Alberti A, Aury JM, Balfourier F, Barbe V, Couloux A, Cruaud C, Labadie K, Mangenot S, Wincker P, D D, mapping Dp, Gill B, Kaur G, Luo M, Sehgal S, mapping ALp, Singh K, Chhuneja P, Gupta OP, Jindal S, Kaur P, Malik P, Sharma P, Yadav B, mapping ASp, Singh NK, Khurana J, Chaudhary C, Khurana P, Kumar V, Mahato A, Mathur S, Sevanthi A, Sharma N, Tomar RS, B DBB, maps DI-BW-GPp, Rogers J, Jacobs J, Alaux M, Bellec A, Berges H, Dolezel J, Feuillet C, Frenkel Z, Gill B, Korol A, van der Vossen E, Vautrin S, mapping ALp, Gill B, Kaur G, Luo M, Sehgal S, mapping DSp, sequencing BAC, assembly, Bartos J, Holusova K, Plihal O, sequencing DB, assembly, Clark MD, Heavens D, Kettleborough G, Wright J, A physical mapping BACsa, annotation, Valarik M, Abrouk M, Balcarkova B, Holusova K, Hu Y, Luo M, sequencing BB, assembly, Salina E, Ravin N, Skryabin K, Beletsky A, Kadnikov V, Mardanov A, Nesterov M, Rakitin A, Sergeeva E, sequencing BB, assembly, Handa H, Kanamori H, Katagiri S, Kobayashi F, Nasuda S, Tanaka T, Wu J, mapping Ap, sequencing BAC, Appels R, Hayden M, Keeble-Gagnere G, Rigault P, Tibbits J, B physical mapping BACs, assembly, Olsen OA, Belova T, Cattonaro F, Jiumeng M, Kugler K, Mayer KFX, Pfeifer M, Sandve S, Xun X, Zhan B, sequencing DB, assembly, Simkova H, Abrouk M, Batley J, Bayer PE, Edwards D, Hayashi S, Toegelova H, Tulpova Z, Visendi P, mapping DLp, sequencing BAC, Weining S, Cui L, Du X, Feng K, Nie X, Tong W, Wang L, Figures, Borrill P, Gundlach H, Galvez S, Kaithakottil G, Lang D, Lux T, Mascher M, Ormanbekova D, Prade V, Ramirez-Gonzalez RH, Spannagl M, Stein N, Uauy C, Venturini L, Manuscript writing t, Stein N, Appels R, Eversole K, Rogers J, Borrill P, Cattivelli L, Choulet F, Hernandez P, Kanyuka K, Lang D, Mascher M, Nilsen K, Paux E, Pozniak CJ, Ramirez-Gonzalez RH, Simkova H, Small I, Spannagl M, Swarbreck D, Uauy C (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361(6403):7191. https://doi.org/10.1126/science.aar7191

  • Jiang Y, Zeng B, Zhao H, Zhang M, Xie S, Lai J (2012) Genome-wide transcription factor gene prediction and their expressional tissue-specificities in maize. J Integr Plant Biol 54(9):616–630. https://doi.org/10.1111/j.1744-7909.2012.01149.x

    Article  CAS  PubMed  Google Scholar 

  • Kim YJ, Lin NC, Martin GB (2002) Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109(5):589–598. https://doi.org/10.1016/s0092-8674(02)00743-2

    Article  CAS  PubMed  Google Scholar 

  • Kim MJ, Ruzicka D, Shin R, Schachtman DP (2012) The Arabidopsis AP2/ERF transcription factor RAP2.11 modulates plant response to low-potassium conditions. Mol Plant 5(5):1042–1057. https://doi.org/10.1093/mp/sss003

    Article  CAS  PubMed  Google Scholar 

  • Kong Q, Sun T, Qu N, Ma J, Li M, Cheng Y-t, Zhang Q, Wu D, Zhang Z, Zhang Y (2016) Two redundant receptor-like cytoplasmic kinases function downstream of pattern recognition receptors to regulate activation of SA biosynthesis. Plant Physiol 171(2):1344–1354. https://doi.org/10.1104/pp.15.01954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurusu T, Kuchitsu K, Tada Y (2015) Plant signaling networks involving Ca(2+) and Rboh/Nox-mediated ROS production under salinity stress. Front Plant Sci 6:427. https://doi.org/10.3389/fpls.2015.00427

    Article  PubMed  PubMed Central  Google Scholar 

  • Lal NK, Nagalakshmi U, Hurlburt NK, Flores R, Bak A, Sone P, Ma X, Song G, Walley J, Shan L, He P, Casteel C, Fisher AJ, Dinesh-Kumar SP (2018) The receptor-like cytoplasmic kinase BIK1 localizes to the nucleus and regulates defense hormone expression during plant innate immunity. Cell Host Microbe 23(4):485–497. https://doi.org/10.1016/j.chom.2018.03.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9(4):357–359. https://doi.org/10.1038/nmeth.1923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323. https://doi.org/10.1186/1471-2105-12-323

    Article  CAS  Google Scholar 

  • Li A, Wang X, Leseberg CH, Jia J, Mao L (2008) Biotic and abiotic stress responses through calcium-dependent protein kinase (CDPK) signaling in wheat (Triticum aestivum L.). Plant Signal Behav 3(9):654–656. https://doi.org/10.4161/psb.3.9.5757

    Article  PubMed  PubMed Central  Google Scholar 

  • Li Z, Ao Y, Feng D, Liu J, Wang J, Wang H-B, Liu B (2017) OsRLCK 57, OsRLCK107 and OsRLCK118 positively regulate chitin- and PGN-induced immunity in rice. Rice 10(1):6. https://doi.org/10.1186/s12284-017-0145-6

    Article  PubMed  PubMed Central  Google Scholar 

  • Liang X, Zhou JM (2018) Receptor-like cytoplasmic kinases: central players in plant receptor kinase-mediated signaling. Annu Rev Plant Biol 69:267–299. https://doi.org/10.1146/annurev-arplant-042817-040540

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Zhou X, Dong N, Liu X, Zhang H, Zhang Z (2011) Expression of a wheat MYB gene in transgenic tobacco enhances resistance to Ralstonia solanacearum, and to drought and salt stresses. Funct Integr Genomics 11(3):431–443. https://doi.org/10.1007/s10142-011-0228-1

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262

    Article  CAS  PubMed  Google Scholar 

  • Molendijk AJ, Ruperti B, Singh MK, Dovzhenko A, Ditengou FA, Milia M, Westphal L, Rosahl S, Soellick T-R, Uhrig J, Weingarten L, Huber M, Palme K (2008) A cysteine-rich receptor-like kinase NCRK and a pathogen-induced protein kinase RBK1 are Rop GTPase interactors. Plant J 53(6):909–923. https://doi.org/10.1111/j.1365-313X.2007.03384.x

    Article  CAS  PubMed  Google Scholar 

  • Moon JY, Belloeil C, Ianna ML, Shin R (2019) Arabidopsis CNGC family members contribute to heavy metal ion uptake in plants. Int J Mol Sci 20(2):413. https://doi.org/10.3390/ijms20020413

    Article  CAS  PubMed Central  Google Scholar 

  • Orlandi EW, Hutcheson SW, Baker CJ (1992) Early physiological responses associated with race-specific recognition in soybean leaf tissue and cell suspensions treated with Pseudomonas syringae pv. glycinea. Physiol Mol Plant Pathol 40(3):173–180. https://doi.org/10.1016/0885-5765(92)90058-4

    Article  CAS  Google Scholar 

  • Qian C, Cui C, Wang X, Zhou C, Hu P, Li M, Li R, Xiao J, Wang X, Chen P, Xing L, Cao A (2017) Molecular characterisation of the broad-spectrum resistance to powdery mildew conferred by the Stpk-V gene from the wild species Haynaldia villosa. Plant Biol 19(6):875–885. https://doi.org/10.1111/plb.12625

    Article  CAS  PubMed  Google Scholar 

  • Schwizer S, Kraus CM, Dunham DM, Zheng Y, Fernandez-Pozo N, Pombo MA, Fei Z, Chakravarthy S, Martin GB (2017) The tomato kinase Pti1 contributes to production of reactive oxygen species in response to two flagellin-derived peptides and promotes resistance to Pseudomonas syringae infection. Mol Plant Microbe Interact 30(9):725–738. https://doi.org/10.1094/MPMI-03-17-0056-R

    Article  CAS  PubMed  Google Scholar 

  • Shinya T, Yamaguchi K, Desaki Y, Yamada K, Narisawa T, Kobayashi Y, Maeda K, Suzuki M, Tanimoto T, Takeda J, Nakashima M, Funama R, Narusaka M, Narusaka Y, Kaku H, Kawasaki T, Shibuya N (2014) Selective regulation of the chitin-induced defense response by the Arabidopsis receptor-like cytoplasmic kinase PBL27. Plant J 79(1):56–66. https://doi.org/10.1111/tpj.12535

    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(5):1220–1234. https://doi.org/10.1105/tpc.020834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sreekanta S, Bethke G, Hatsugai N, Tsuda K, Thao A, Wang L, Katagiri F, Glazebrook J (2015) The receptor-like cytoplasmic kinase PCRK1 contributes to pattern-triggered immunity against Pseudomonas syringae in Arabidopsis thaliana. New Phytol 207(1):78–90. https://doi.org/10.1111/nph.13345

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Sun M, Luo X, Ding X, Ji W, Cai H, Bai X, Liu X, Zhu Y (2013) A Glycine soja ABA-responsive receptor-like cytoplasmic kinase, GsRLCK, positively controls plant tolerance to salt and drought stresses. Planta 237(6):1527–1545. https://doi.org/10.1007/s00425-013-1864-6

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Sun M, Jia B, Qin Z, Yang K, Chen C, Yu Q, Zhu Y (2016) A Glycine soja methionine sulfoxide reductase B5a interacts with the Ca(2+)/CAM-binding kinase GsCBRLK and activates ROS signaling under carbonate alkaline stress. Plant J 86(6):514–529. https://doi.org/10.1111/tpj.13187

    Article  CAS  PubMed  Google Scholar 

  • Tang D, Wang G, Zhou JM (2017) Receptor kinases in plant-pathogen interactions: more than pattern recognition. Plant Cell 29(4):618–637. https://doi.org/10.1105/tpc.16.00891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants: H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11(6):1187–1194. https://doi.org/10.1046/j.1365-313X.1997.11061187.x

    Article  CAS  Google Scholar 

  • Wan S, Wang W, Zhou T, Zhang Y, Chen J, Xiao B, Yang Y, Yu Y (2018) Transcriptomic analysis reveals the molecular mechanisms of Camellia sinensis in response to salt stress. Plant Growth Regul 84(3):481–492. https://doi.org/10.1007/s10725-017-0354-4

    Article  CAS  Google Scholar 

  • Wang J, Wu G, Peng C, Zhou X, Li W, He M, Wang J, Yin J, Yuan C, Ma W, Ma B, Wang Y, Chen W, Qin P, Li S, Chen X (2016) The receptor-like cytoplasmic kinase OsRLCK102 regulates XA21-mediated immunity and plant development in rice. Plant Mol Biol Report 34(3):628–637. https://doi.org/10.1007/s11105-015-0951-1

    Article  CAS  Google Scholar 

  • Wang C, Wang G, Zhang C, Zhu P, Dai H, Yu N, He Z, Xu L, Wang E (2017) OsCERK1-mediated chitin perception and immune signaling requires receptor-like cytoplasmic kinase 185 to activate an MAPK cascade in rice. Mol Plant 10(4):619–633. https://doi.org/10.1016/j.molp.2017.01.006

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi K, Yamada K, Ishikawa K, Yoshimura S, Hayashi N, Uchihashi K, Ishihama N, Kishi-Kaboshi M, Takahashi A, Tsuge S, Ochiai H, Tada Y, Shimamoto K, Yoshioka H, Kawasaki T (2013) A receptor-like cytoplasmic kinase targeted by a plant pathogen effector is directly phosphorylated by the chitin receptor and mediates rice immunity. Cell Host Microbe 13(3):347–357. https://doi.org/10.1016/j.chom.2013.02.007

    Article  CAS  PubMed  Google Scholar 

  • Yuan P, Jauregui E, Du L, Tanaka K, Poovaiah BW (2017) Calcium signatures and signaling events orchestrate plant-microbe interactions. Curr Opin Plant Biol 38:173–183. https://doi.org/10.1016/j.pbi.2017.06.003

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Li W, Xiang T, Liu Z, Laluk K, Ding X, Zou Y, Gao M, Zhang X, Chen S, Mengiste T, Zhang Y, Zhou JM (2010) Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7(4):290–301. https://doi.org/10.1016/j.chom.2010.03.007

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Li D, Wang M, Liu J, Teng W, Cheng B, Huang Q, Wang M, Song W, Dong S, Zheng X, Zhang Z (2012) The Nicotiana benthamiana mitogen-activated protein kinase cascade and WRKY transcription factor participate in Nep1(Mo)-triggered plant responses. Mol Plant Microbe Interact 25(12):1639–1653. https://doi.org/10.1094/MPMI-11-11-0293

    Article  PubMed  Google Scholar 

  • Zhang Z, Liu Y, Huang H, Gao M, Wu D, Kong Q, Zhang Y (2017) The NLR protein SUMM2 senses the disruption of an immune signaling MAP kinase cascade via CRCK3. EMBO Rep 18(2):292–302. https://doi.org/10.15252/embr.201642704

    Article  CAS  PubMed  Google Scholar 

  • Zhou X, Wang J, Peng C, Zhu X, Yin J, Li W, He M, Wang J, Chern M, Yuan C, Wu W, Ma W, Qin P, Ma B, Wu X, Li S, Ronald P, Chen X (2016) Four receptor-like cytoplasmic kinases regulate development and immunity in rice. Plant Cell Environ 39(6):1381–1392. https://doi.org/10.1111/pce.12696

    Article  CAS  PubMed  Google Scholar 

  • Zhou W, Qian C, Li R, Zhou S, Zhang R, Xiao J, Wang X, Zhang S, Xing L, Cao A (2018) TaNAC6s are involved in the basal and broad-spectrum resistance to powdery mildew in wheat. Plant Sci 277:218–228. https://doi.org/10.1016/j.plantsci.2018.09.014

    Article  CAS  PubMed  Google Scholar 

  • Zou J-J, Wei F-J, Wang C, Wu J-J, Ratnasekera D, Liu W-X, Wu W-H (2010) Arabidopsis calcium-dependent protein kinase CPK10 functions in abscisic acid- and Ca2+-mediated stomatal regulation in response to drought stress. Plant Physiol 154(3):1232–1243. https://doi.org/10.1104/pp.110.157545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We acknowledge very gratefully the supports from the high-performance computing platform of Bioinformatics Center, Nanjing Agricultural University.

Funding

This research was supported by the grants from the National key research and development program (No. 2016YFD0101004, No. 2020YFE0202900), the International Cooperation and Exchange of the National Natural Science Foundation of China (No. 31661143005), the Agricultural Scientific Research Outstanding Talents and Their Innovative Teams Program, the Key Research and Development Major Project of Ningxia Autonomous Region (No. 2019BBF02022-04), the Jiangsu Agricultural Technology System (JATS) (No. JATS [2020] 411). The role of the funding body is to provide financial support.

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Authors and Affiliations

  1. State Key Lab of Crop Genetics and Germplasm Enhancement, Cytogenetics Institute, Nanjing Agricultural University/JCIC-MCP, Nanjing, 210095, Jiangsu, China

    Xu Zhang, Yongli Hao, Xingxing Cai, Heng Zhang, Yiming Chen, Ying Niu, Zongkuan Wang, Mengli Li, Jia Liu, Haiyan Wang, Jin Xiao, Li Sun & Xiue Wang

  2. State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou, 310021, China

    Heng Zhang

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  1. Xu Zhang
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  2. Yongli Hao
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  13. Xiue Wang
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Contributions

XW, JX, HW, ZW, and XZ conceived and designed the study; XZ, HL, HZ analyzed the data; YC, YN, LJ and ML collected the plant materials; XZ, HL performed the experiments; XZ, XC, LS, and XW wrote the manuscript. All authors have read and approved the final manuscript.

Corresponding authors

Correspondence to Li Sun or Xiue Wang.

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Communicated by Feibo Wu.

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Supplementary Information

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10725_2021_753_MOESM1_ESM.jpg

Supplementary file1 Fig. S1 The FPKM values of Stpk-V and its orthologous genes (Stpk-A, Stpk-B, and Stpk-D) in OEStpk-v before (Mock) and after and E26 treatment (JPG 435 kb)

10725_2021_753_MOESM2_ESM.jpg

Supplementary file2 Fig. S2 The number of differentially expressed genes (DEGs) and DEG enrichment in OEStpk-v and Yangmai 158(a)DEGs in five infectious time points in OEStpk-V and Yangmai 158. Orange represents DEGs in Yangmai 158; Blue represents DEGs in OEStpk-V; (b) Venn diagram analysis of DEGs in Yangmai 158 and OEStpk-V after E31 infection. (c)The KEGG enhancement of DEGs in OEStpk-V. Red represents up-regulated DEGs; Blue represents down-regulated DEGs; (d) GO enrichment analysis of the biological process in OEStpk-V and susceptible receptor Yangmai158 during E31 infection. (JPG 1732 kb)

10725_2021_753_MOESM3_ESM.jpg

Supplementary file3 Fig. S3 Distinct KEGG pathway of OEStpk-V and Yangmai158 after mock treatment(a) Radar Chart of up-regulated DEGs in OEStpk-V. (b) Radar Chart of down-regulated DEGs in OEStpk-V. hai: hour after Bgt inoculation. (JPG 405 kb)

10725_2021_753_MOESM4_ESM.jpg

Supplementary file4 Fig. S4 qRT-PCR and RNA-seq data in OEStpk-V and Yangmai 158 from1 hai to 24 hai after Bgt infection. The histogram represents genes expression data by qRT-PCR. Gray represents Yangmai 158, black represents OEStpk-V. The line chart represents genes expression data by RNA-seq. The dotted line represents Yangmai 158, a solid line represents OEStpk-V. hai: hour after Bgt inoculation. (JPG 601 kb)

10725_2021_753_MOESM5_ESM.jpg

Supplementary file5 Fig. S5 The heatmap of Ca2+ related DEGs expression in plant-pathogen interaction pathway after in OEStpk-V. and Yangmai 158.The color scale indicates the fold changes in gene expression. The expression value of each gene is based on the Z-score normalization value. Time points are displayed below the heatmap. hai: hour after Bgt inoculation. (JPG 549 kb)

10725_2021_753_MOESM6_ESM.jpg

Supplementary file6 Fig. S6 DAB staining to visualize H2O2 accumulation in the leaves of Yangmai 158 and OEStpk-V. Arrows indicated location of H2O2. (JPG 458 kb)

10725_2021_753_MOESM7_ESM.jpg

Supplementary file7 Fig. S7 Eigengenes adjacency heatmap and KEGG analysis of the red module containing OEStpk-V.(a) Each row and columns correspond to a module. The number of genes in each module is indicated on the left. The color of each cell at the row-column intersection indicates the correlation coefficient between the two modules. (b) KEGG enrichment DEGs in the OEStpk-V network. (JPG 646 kb)

Supplementary file8 Table S1 Quality of transcripts in different samples. (XLSX 11 kb)

Supplementary file9 Table S2 Detailed list of the genes in Ca2+ signalling according to KEGG enrichment (XLSX 11 kb)

Supplementary file10 Table S3 The primer pairs for qRT-PCR (XLSX 11 kb)

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Zhang, X., Hao, Y., Cai, X. et al. Temporal role of the receptor-like cytoplasmic kinase gene Stpk-V in wheat-Blumeria graminis f. sp. tritici interaction by RNA-seq analysis. Plant Growth Regul 95, 429–442 (2021). https://doi.org/10.1007/s10725-021-00753-1

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