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Journal of Integrative Agriculture  2020, Vol. 19 Issue (11): 2616-2627    DOI: 10.1016/S2095-3119(20)63160-4
Special Issue: 麦类遗传育种合辑Triticeae Crops Genetics · Breeding · Germplasm Resources
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The wheat receptor-like cytoplasmic kinase TaRLCK1B is required for host immune response to the necrotrophic pathogen Rhizoctonia cerealis
WU Tian-ci1, 2, ZHU Xiu-liang2, LÜ Liang-jie3, CHEN Xi-yong3, XU Gang-biao1, ZHANG Zeng-yan2
1 Laboratory of Forestry Genetics, Central South University of Forestry and Technology, Changsha 410004, P.R.China
2 National Key Facility for Crop Gene Resources and Genetic Improvement/Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
3 Institute for Cereal and Oil Crops, Hebei Academy of Agriculture and Forestry Sciences, Shijiazhuang 050035, P.R.China
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Receptor-like cytoplasmic kinases (RLCKs) represent a large family of proteins in plants.  In Arabidopsis and rice, several RLCKs in subfamily VII (RLCKs-VII) have been implicated in pathogen-associated molecular pattern-triggered immunity and basal resistance against bacterial and fungal pathogens.  However, little is known about roles of RLCKs-VII of the important crop common wheat (Triticum aestivum) in immune responses.  Here, we isolated a RLCK-VII-encoding gene from wheat, designated as TaRLCK1B, and investigated its role in host immune response to infection of a necrotrophic fungus Rhizoctonia cerealis that is a major pathogen of sharp eyespot, a destructive disease of wheat.  RNA-sequencing and RT-qPCR analyses showed that transcriptional level of TaRLCK1B was significantly higher in sharp eyespot-resistant wheat cultivars than in susceptible wheat cultivars.  The gene transcription was rapidly and markedly elevated in the resistant wheat cultivars by R. cerealis infection.  The TaRLCK1B protein was closely related to OsRLCK176, a rice resistance-related RLCKs-VII, with 84.03% identity.  Virus-induced gene silencing plus wheat response to R. cerealis assay results indicated that silencing of TaRLCK1 impaired resistance to R. cerealis.  Meantime, silencing of TaRLCK1 significantly elevated both the content of H2O2 (a major kind of reactive oxygen species, ROS) and the transcriptional level of the ROS-generating enzyme-encoding gene RBOH, but repressed the expression of the ROS-scavenging enzyme-encoding gene CAT1 at 18 hours after inoculation (hai) with R. cerealis.  Taken together, these data suggested that TaRLCK1B was required for the early immune response of wheat to R. cerealis through modulating ROS signaling in wheat.
Keywords:  common wheat (Triticum aestivum)        H2O2        immune respons       , reactive oxygen species        receptor-like cytoplasmic kinase        Rhizoctonia cerealis   
Received: 18 July 2019   Accepted:
Fund: This study was funded by the Natural Science Foundation of China (31771789), the National Key Project for Research on Transgenic Biology, China (2016ZX08002-001-004), and Young Elite Scientists Sponsorship Program by China Association for Science and Technology (2018QNRC001).
Corresponding Authors:  Correspondence ZHANG Zeng-yan, Tel: +86-10-82108781, E-mail:; XU Gang-biao, E-mail:   

Cite this article: 

WU Tian-ci, ZHU Xiu-liang, LÜ Liang-jie, CHEN Xi-yong, XU Gang-biao, ZHANG Zeng-yan. 2020. The wheat receptor-like cytoplasmic kinase TaRLCK1B is required for host immune response to the necrotrophic pathogen Rhizoctonia cerealis. Journal of Integrative Agriculture, 19(11): 2616-2627.

Ao Y, Li Z, Feng D, Xiong F, Liu J, Li J F, Wang M, Wang J, Liu B, Wang H B. 2014. OsCERK1 and OsRLCK176 play important roles in peptidoglycan and chitin signaling in rice innate immunity. The Plant Journal, 80, 1072–1084.
Apel K, Hirt H. 2004. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology, 55, 373–399.
Bi G, Zhou Z, Wang W, Li L, Rao S, Wu Y, Zhang X, Menke FLH, Chen S, Zhou J M. 2018. Receptor-like cytoplasmic kinases directly link diverse pattern recognition receptors to the activation of mitogen-activated protein kinase cascades in Arabidopsis. The Plant Cell, 30, 1543–1561.
Cai S B, Ren L J, Yan W, Wu J Z, Chen H G, Wu X Y, Zhang X Y. 2006. Germplasm development and mapping of resistance to sharp eyespot (Rhizoctonia cerealis) in wheat. Scientia Agricultura Sinica, 39, 928–934. (in Chinese)
Camejo D, Guzmán-Cedeño Á, Moreno A. 2016. Reactive oxygen species, essential molecules, during plant-pathogen interactions. Plant Physiology and Biochemistry, 103, 10–23.
Chen J, Li G H, Du Z Y, Quan W, Zhang H Y, Che M Z, Wang Z, Zhang Z J. 2013. Mapping of QTL conferring resistance to sharp eyespot (Rhizoctonia cerealis) in bread wheat at the adult plant growth stage. Theoretical and Applied Genetics, 126, 2865–2878.
Chen L, Zhang Z Y, Liang H X, Liu H, Du L P, Xu H J, Xin Z Y. 2008. Overexpression of TiERF1 enhances resistance to sharp eyespot in transgenic wheat. Journal of Experimental Botany, 59, 4195–4204.
Couto D, Zipfel C. 2016. Regulation of pattern recognition receptor signalling in plants. Nature Reviews Immunology, 16, 537–552.
Dong N, Liu X, Lu Y, Du L P, Xu H J, Liu H X, Xin Z Y, Zhang Z Y. 2010. Overexpression of TaPIEP1, a pathogen-induced ERF gene of wheat, confers host-enhanced resistance to fungal pathogen Bipolaris sorokiniana. Functional & Integrative Genomics, 10, 215–226.
Hamada M S, Yin Y, Chen H, Ma Z. 2011. The escalating threat of Rhizoctonia cerealis, the causal agent of sharp eyespot in wheat. Pest Management Science, 67, 1411–1419.
Holzberg S, Brosio P, Gross C S, Pogue G P. 2002. Barley stripe mosaic virus-induced gene silencing in a monocot plant. The Plant Journal, 30, 315–327.
Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S, Ntoukakis V, Jones J D, Shirasu K, Menke F, Jones A, Zipfel C. 2014. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Molecular Cell, 54, 43–55.
Kimura S, Waszczak C, Hunter K, Wrzaczek M. 2017. Bound by fate: Reactive oxygen species in receptor-like kinase signaling. The Plant Cell, 29, 638–654.
Klymiuk V, Yaniv E, Huang L, Raats D, Fatiukha A, Chen S, Feng L, Frenkel Z, Krugman T, Lidzbarsky G, Chang W, Jääskeläinen M J, Schudoma C, Paulin L, Laine P, Bariana H, Sela H, Saleem K, Sørensen C K, Hovmøller M S, et al. 2018. Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family. Nature Communications, 9, 3735.
Kobayashi M, Yoshioka M, Asai S, Nomura H, Kuchimura K, Mori H, Mori H, Doke N, Yoshioka H. 2012. StCDPK5 confers resistance to late blight pathogen but increases susceptibility to early blight pathogen in potato via reactive oxygen species burst. New Phytologist, 196, 223–237.
Kumar S, Sud N, Fonseca F V, Hou Y, Black S M. 2010. Shear stress stimulates nitric oxide signaling in pulmonary arterial endothelial cells via a reduction in catalase activity: Role of protein kinase C delta. American Journal of Physiology-lung Cellular and Molecular Physiology, 298, 105–116. 
Lee B H, Lee H, Xiong L, Zhu J K. 2002. A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. The Plant Cell, 14, 1235–1251.
Li L, Li M, Yu L P, Zhou Z Y, Liang X X, Liu Z X, Cai G H, Gao L Y, Zhang X J, Wang Y C, Chen S, Zhou J M. 2014. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe, 15, 329–338.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25, 402–408.
Maeda S, Hayashi N, Sasaya T, Mori M. 2016. Overexpression of BSR1 confers broad-spectrum resistance against two bacterial diseases and two major fungal diseases in rice. Breeding Science, 66, 396–406.
Mhamdi A, Queval G, Chaouch S, Vanderauwera S, Van Breusegem F, Noctor G. 2010. Catalase function in plants: A focus on Arabidopsis mutants as stress-mimic models. Journal of Experimental Botany, 61, 4197–4220.
Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti V B, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F. 2011. ROS signaling: The new wave? Trends in Plant Science, 16, 300–309.
Monaghan J. 2018. Conserved degradation of orthologous RLCKs regulates immune homeostasis. Trends in Plant Science, 23, 554–557.
Monaghan J, Zipfel C. 2012. Plant pattern recognition receptor complexes at the plasma membrane. Current Opinion in Plant Biology, 15, 349–357.
Nowara D, Gay A, Lacomme C, Lacomme C, ShawJ, Ridout C, Douchkov D, Hensel G, Kumlehn J, Schweizer P. 2010. HIGS: host-induced gene silencing in theobligate biotrophic fungal pathogen Blumeria graminis. The Plant Cell, 22, 3130–3141.
Schmidt R, Mieulet D, Hubberten H M, Obata T, Hoefgen R, Fernie A R, Fisahn J, San Segundo B, Guiderdoni E, Schippers J H, Muellerroeber B. 2013. Salt-responsive ERF1 regulates reactive oxygen species-dependent signaling during the initial response to salt stress in rice. The Plant Cell, 25, 2115–2131.
Schwessinger B, Ronald P C. 2012. Plant innate immunity: perception of conserved microbial signatures. Annual Review of Plant Biology, 63, 451–482.
Scofield S R, Huang L, Brandt A S, Gill B S. 2005. Development of a virus-induced gene-silencing system for hexaploid wheat and its use in functional analysis of the Lr21-mediated leaf rust resistance pathway. Plant Physiology, 138, 2165–2173.
Sharma N, Rahman M H, Strelkov S E, Thiagarajah M R, Bansal V K, Kav N N. 2007. Proteome-level changes in two Brassica napus lines exhibiting differential responses to the fungal pathogen Alternaria brassicae. Plant Science, 172, 95–110.
Shewry P R, Hey S J. 2015. The contribution of wheat to human diet and health. Food and Energy Security, 4, 178–202.
Sugano S, Maeda S, Hayashi N, Kajiwara H, Inoue H, Jiang C J, Takatsuji H, Mori M. 2018. Tyrosine phosphorylation of a receptor-like cytoplasmic kinase, BSR1, plays a crucial role in resistance to multiple pathogens in rice. The Plant Journal, 96, 1137–1147
Veronese P, Nakagami H, Bluhm B, Abuqamar S, Chen X, Salmeron J, Dietrich R A, Hirt H, Mengiste T. 2006. The membrane-anchored BOTRYTIS-INDUCED KINASE1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens. The Plant Cell, 18, 257–273.
Wang C, Wang G, Zhang C, Zhu P K, Dai H L, Yu N, He Z H, 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. Molecular Plant, 10, 619–633.
Wu X J, Cheng K, Zhao R H, Zang S J, Bie T, Jiang Z N, Wu R L, Gao D R, Zhang B Q. 2017. Quantitative trait loci responsible for sharp eyespot resistance in common wheat CI12633. Scientific Reports, 7, 11799.
Xu J, Duan X, Yang J, Beeching J R, Zhang P. 2013. Enhanced reactive oxygen species scavenging by overproduction of superoxide dismutase and catalase delays postharvest physiological deterioration of cassava storage roots. Plant Physiology, 161, 1517–1528.
Yoshioka H, Numata N, Nakajima K, Katou S, Kawakita K, Rowland O, Jones J D, Doke N. 2003. Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans. The Plant Cell, 15, 706–718.
Zhang Z Y, Yao W L, Dong N, Liang H X, Liu H X, Huang R F. 2007. A novel ERF transcription activator in wheat and its induction kinetics after pathogen and hormone treatments. Journal of Experimental Botany, 58, 2993–3003.
Zhou X G, Wang J, Peng C F, Zhu X B, Yin J J, Li W T, He M, Wang J H, Chern M S, Yuan C, Wu W G, Ma W W, Qin P, Ma B T, Wu X J, Li S G, Ronald P C, Chen X W. 2016. Four receptor-like cytoplasmic kinases regulate development and immunity in rice. Plant Cell and Environment, 39, 1381–1392.
Zhou Y B, Liu C, Tang D Y, Yan L, Wang D, Yang Y Z, Gui J S, Zhao X Y, Li L G, Tang X D, Yu F, Li J L, Liu L L, Zhu Y H, Lin J Z, Liu X M. 2018. The receptor-like cytoplasmic kinase STRK1 phosphorylates and activates CatC, thereby regulating H2O2 homeostasis and improving salt tolerance in rice. The Plant Cell, 30, 1100–1118.
Zhu X L, Lu C, Du L P, Ye X G, Liu X, Coules A, Zhang Z Y, 2017. The wheat NB-LRR gene TaRCR1 is required for host defence response to the necrotrophic fungal pathogen Rhizoctonia cerealis. Plant Biotechnology Journal, 15, 674–687.
Zhu X L, Yang K, Wei X N, Zhang Q F, Rong W, Du L P, Ye X G, Qi L, Zhang Z Y. 2015. The wheat AGC kinase TaAGC1 is a positive contributor to host resistance to the necrotrophic pathogen Rhizoctonia cerealis. Journal of Experimental Botany, 66, 6591–6603.
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