Synergy in Rice Immunity: Exploring Strategies of Coordinated Disease Defense Through Receptor-Like Kinases and Receptor- Like Cytoplasmic Kinases

doi:10.1016/j.rsci.2024.07.002

Abstract

Abstract:

Receptor-like kinases (RLKs) and receptor-like cytoplasmic kinases (RLCKs) play an indispensable role in the perception and transmission of extracellular signals in plants. In rice, these kinases actively participate in immune responses against a variety of pathogens, including fungi, bacteria, and viruses. However, research on the specific response mechanisms and the spectrum of different kinase activities against various pathogens remains insufficient. This review provides an in-depth and comprehensive overview of the types and functions of RLKs and RLCKs involved in disease resistance, emphasizing the central role of certain RLKs and RLCKs in the plant immune system. These kinases can recognize specific molecular patterns of pathogens and rapidly initiate an immune response in rice. Furthermore, the activity and functional regulation of these key kinases are tightly controlled by various post-translational modifications, such as phosphorylation and ubiquitination. This meticulous regulation ensures that the rice immune system’s response is both precise and timely, effectively balancing the intensity of the immune response and preventing potential issues caused by either hyperactivity or insufficiency. By synthesizing current research findings, this review not only broadens our understanding of the role of RLKs and RLCKs in plant immunity but also provides new perspectives and strategies for future research on disease resistance breeding in rice. Future studies are expected to delve deeper into the signaling networks and regulatory mechanisms of these kinases, exploring their potential in agricultural production to develop rice varieties with enhanced disease resistance.

Key words: receptor-like kinase, receptor-like cytoplasmic kinase, pathogen-associated molecular pattern, genetic breeding

Pei Mengtian, Cao Yingying, Xie Xuze, Cao Ying, Chen Jia, Zhang Xi, Wang Zonghua, Lu Guodong, Zhang Shenghang. Synergy in Rice Immunity: Exploring Strategies of Coordinated Disease Defense Through Receptor-Like Kinases and Receptor- Like Cytoplasmic Kinases[J]. Rice Science, 2024, 31(6): 643-658.

Figures/Tables 6

References 120

[1]	Abdul Fiyaz R, Shivani D, Chaithanya K, Mounika K, Chiranjeevi M, Laha G S, Viraktamath B C, Subba Rao L V, Sundaram R M. 2022. Genetic improvement of rice for bacterial blight resistance: Present status and future prospects. Rice Sci, 29(2): 118-132.
[2]	Akamatsu A, Wong H L, Fujiwara M, Okuda J, Nishide K, Uno K, Imai K, Umemura K, Kawasaki T, Kawano Y, Shimamoto K. 2013. An OsCEBiP/OsCERK1-OsRacGEF1-OsRac1 module is an essential early component of chitin-induced rice immunity. Cell Host Microbe, 13(4): 465-476.
[3]	Al-Bader N, Meier A, Geniza M, Gongora Y S, Oard J, Jaiswal P. 2023. Loss of a premature stop codon in the rice wall-associated kinase 91 (WAK91) gene is a candidate for improving leaf sheath blight disease resistance. Genes, 14(9): 1673.
[4]	An L, Zhang S, Guo P, Song L, Xie C, Guo H, Fang R, Jia Y. 2022. RIR1 represses plant immunity by interacting with mitochondrial complex I subunit in rice. Mol Plant Pathol, 23(1): 92-103.
[5]	Ao Y, Li Z Q, Feng D R, Xiong F, Liu J, Li J F, Wang M L, Wang J F, Liu B, Wang H B. 2014. OsCERK1 and OsRLCK176 play important roles in peptidoglycan and chitin signaling in rice innate immunity. Plant J, 80(6): 1072-1084.
[6]	Bai S W, Yu H, Wang B, Li J Y. 2018. Retrospective and perspective of rice breeding in China. J Genet Genomics, 45(11): 603-612.
[7]	Bentham A R, de la Concepcion J C, Mukhi N, Zdrzałek R, Draeger M, Gorenkin D, Hughes R K, Banfield M J. 2020. A molecular roadmap to the plant immune system. J Biol Chem, 295(44): 14916-14935.
[8]	Bethke G, Unthan T, Uhrig J F, Pöschl Y, Gust A A, Scheel D, Lee J. 2009. Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proc Natl Acad Sci USA, 106(19): 8067-8072.
[9]	Boudsocq M, Willmann M R, McCormack M, Lee H, Shan L B, He P, Bush J, Cheng S H, Sheen J. 2010. Differential innate immune signalling via Ca²⁺ sensor protein kinases. Nature, 464: 418-422.
[10]	Byndloss M X, Rivera-Chávez F, Tsolis R M, Bäumler A J. 2017. How bacterial pathogens use type III and type IV secretion systems to facilitate their transmission. Curr Opin Microbiol, 35: 1-7.
[11]	Cao S X, Wang Y, Gao Y H, Xu R, Ma J N, Xu Z P, Shang-Guan K K, Zhang B C, Zhou Y H. 2023. The RLCK-VND6 module coordinates secondary cell wall formation and adaptive growth in rice. Mol Plant, 16(6): 999-1015.
[12]	Chaparro-Garcia A, Wilkinson R C, Gimenez-Ibanez S, Findlay K, Coffey M D, Zipfel C, Rathjen J P, Kamoun S, Schornack S. 2011. The receptor-like kinase SERK3/BAK1 is required for basal resistance against the late blight pathogen Phytophthora infestans in Nicotiana benthamiana. PLoS One, 6( 1): e16608.
[13]	Chen F, Gao M J, Miao Y S, Yuan Y X, Wang M Y, Li Q, Mao B Z, Jiang L W, He Z H. 2010. Plasma membrane localization and potential endocytosis of constitutively expressed XA21 proteins in transgenic rice. Mol Plant, 3(5): 917-926.
[14]	Chen X W, Shang J J, Chen D X, Lei C L, Zou Y, Zhai W X, Liu G Z, Xu J C, Ling Z Z, Cao G, Ma B T, Wang Y P, Zhao X F, Li S G, Zhu L H. 2006. A B-lectin receptor kinase gene conferring rice blast resistance. Plant J, 46(5): 794-804.
[15]	Chen X W, Zuo S M, Schwessinger B, Chern M, Canlas P E, Ruan D L, Zhou X G, Wang J, Daudi A, Petzold C J, Heazlewood J L, Ronald P C. 2014. An XA21-associated kinase (OsSERK2) regulates immunity mediated by the XA21 and XA3 immune receptors. Mol Plant, 7(5): 874-892.
[16]	Chen Y, Liu Z Q, Meng S, Shen Z N, Shi H B, Qiu J H, Lin F C, Zhang S, Kou Y J. 2022. OsCERK1 contributes to cupric oxide nanoparticles induced phytotoxicity and basal resistance against blast by regulating the anti-oxidant system in rice. J Fungi, 9(1): 36.
[17]	Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G. 2006. The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell, 18(2): 465-476.
[18]	Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones J D G, Felix G, Boller T. 2007. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature, 448: 497-500.
[19]	Cu R M, Mew T W, Cassman K G, Teng P S. 1996. Effect of sheath blight on yield in tropical, intensive rice production system. Plant Dis, 80: 1103-1108.
[20]	Cui H T, Tsuda K, Parker J E. 2015. Effector-triggered immunity: From pathogen perception to robust defense. Annu Rev Plant Biol, 66: 487-511.
[21]	de Jonge R, van Esse H P, Kombrink A, Shinya T, Desaki Y, Bours R, van der Krol S, Shibuya N, Joosten M H A J, Thomma B P H J. 2010. Conserved fungal LysM effector Ecp6 prevents chitin- triggered immunity in plants. Science, 329: 953-955.
[22]	Delteil A, Gobbato E, Cayrol B, Estevan J, Michel-Romiti C, Dievart A, Kroj T, Morel J B. 2016. Several wall-associated kinases participate positively and negatively in basal defense against rice blast fungus. BMC Plant Biol, 16: 17.
[23]	Desaki Y, Kouzai Y, Ninomiya Y, Iwase R, Shimizu Y, Seko K, Molinaro A, Minami E, Shibuya N, Kaku H, Nishizawa Y. 2018. OsCERK1 plays a crucial role in the lipopolysaccharide-induced immune response of rice. New Phytol, 217(3): 1042-1049.
[24]	Dodds P N, Rathjen J P. 2010. Plant immunity: Towards an integrated view of plant-pathogen interactions. Nat Rev Genet, 11(8): 539-548.
[25]	Du D, Liu M, Xing Y, Chen X, Zhang Y, Zhu M, Lu X, Zhang Q, Ling Y, Sang X, Li Y, Zhang C, He G. 2019. Semi-dominant mutation in the cysteine-rich receptor-like kinase gene, ALS1, conducts constitutive defence response in rice. Plant Biol, 21(1): 25-34.
[26]	Fan J B, Bai P F, Ning Y S, Wang J Y, Shi X T, Xiong Y H, Zhang K, He F, Zhang C Y, Wang R Y, Meng X Z, Zhou J G, Wang M, Shirsekar G, Park C H, Bellizzi M, Liu W D, Jeon J S, Xia Y, Shan L B, Wang G L. 2018. The monocot-specific receptor-like kinase SDS2 controls cell death and immunity in rice. Cell Host Microbe, 23(4): 498-510.e5.
[27]	Gao M H, Wang X, Wang D M, Xu F, Ding X J, Zhang Z B, Bi D L, Cheng Y T, Chen S, Li X, Zhang Y L. 2009. Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host Microbe, 6(1): 34-44.
[28]	Guo L J, Guo C M, Li M, Wang W J, Luo C K, Zhang Y X, 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.
[29]	Harkenrider M, Sharma R, de Vleesschauwer D, Tsao L, Zhang X T, Chern M, Canlas P, Zuo S M, Ronald P C. 2016. Overexpression of rice wall-associated kinase 25 (OsWAK25) alters resistance to bacterial and fungal pathogens. PLoS One, 11(1): e0147310.
[30]	Heese A, Hann D R, Gimenez-Ibanez S, Jones A M E, He K, Li J, Schroeder J I, Peck S C, Rathjen J P. 2007. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA, 104(29): 12217-12222.
[31]	Hohmann U, Lau K, Hothorn M. 2017. The structural basis of ligand perception and signal activation by receptor kinases. Annu Rev Plant Biol, 68: 109-137.
[32]	Hu H H, Xiong L, Yang Y N. 2005. Rice SERK1 gene positively regulates somatic embryogenesis of cultured cell and host defense response against fungal infection. Planta, 222(1): 107-117.
[33]	Hu H T, Wang J, Shi C, Yuan C, Peng C F, Yin J J, Li W T, He M, Wang J C, Ma B T, Wang Y P, Li S G, Chen X W. 2015. A receptor like kinase gene with expressional responsiveness on Xanthomonas oryzae pv. oryzae is essential for Xa21-mediated disease resistance. Rice, 8(1): 34.
[34]	Jalilian A, Bagheri A, Chalvon V, Meusnier I, Kroj T, Kakhki A M. 2023. The RLCK subfamily VII-4 controls pattern-triggered immunity and basal resistance to bacterial and fungal pathogens in rice. Plant J, 115(5): 1345-1356.
[35]	Jiang B, Wang Z Y, Xu C X, Liu W J, Jiang D H. 2019. Screening and identification of Aspergillus activity against Xanthomonas oryzae pv. oryzae and analysis of antimicrobial components. J Microbiol, 57(7): 597-605.
[36]	Jones J D G, Dangl J L. 2006. The plant immune system. Nature, 444: 323-329.
[37]	Jones J D G, Vance R E, Dangl J L. 2016. Intracellular innate immune surveillance devices in plants and animals. Science, 354: aaf6395.
[38]	Kanda Y, Yokotani N, Maeda S, Nishizawa Y, Kamakura T, Mori M. 2017. The receptor-like cytoplasmic kinase BSR1 mediates chitin- induced defense signaling in rice cells. Biosci Biotechnol Biochem, 81(8): 1497-1502.
[39]	Kanda Y, Nishizawa Y, Kamakura T, Mori M. 2020. Overexpressed BSR1-mediated enhancement of disease resistance depends on the MAMP-recognition system. Int J Mol Sci, 21(15): 5397.
[40]	Khush G S. 2005. What it will take to feed 5.0 billion rice consumers in 2030. Plant Mol Biol, 59(1): 1-6.
[41]	Kouzai Y, Kaku H, Shibuya N, Minami E, Nishizawa Y. 2013. Expression of the chimeric receptor between the chitin elicitor receptor CEBiP and the receptor-like protein kinase Pi-d2 leads to enhanced responses to the chitin elicitor and disease resistance against Magnaporthe oryzae in rice. Plant Mol Biol, 81(3): 287-295.
[42]	Lal N K, Nagalakshmi U, Hurlburt N K, Flores R, Bak A, Sone P, Ma X Y, Song G Y, Walley J, Shan L B, He P, Casteel C, Fisher A J, Dinesh-Kumar S P. 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.e5.
[43]	Li H, Zhou S Y, Zhao W S, Su S C, Peng Y L. 2009. A novel wall- associated receptor-like protein kinase gene, OsWAK1, plays important roles in rice blast disease resistance. Plant Mol Biol, 69(3): 337-346.
[44]	Li S P, Xiang X Q, Diao Z J, Xia N, Lu L, Zhang J, Chen Z W, Tang D Z. 2024. The OsBSK1-2-MAPK module regulates blast resistance in rice. Crop J, 12(1): 110-120.
[45]	Li W T, Liu Y, Wang J, He M, Zhou X G, Yang C, Yuan C, Wang J C, Chern M, Yin J J, Chen W L, Ma B T, Wang Y P, Qin P, Li S G, Ronald P, Chen X W. 2016. The durably resistant rice cultivar Digu activates defence gene expression before the full maturation of Magnaporthe oryzae appressorium. Mol Plant Pathol, 17(3): 354-368.
[46]	Li Z Q, Ao Y, Feng D R, Liu J, Wang J F, Wang H B, Liu B. 2017. OsRLCK 57, OsRLCK107 and OsRLCK118 positively regulate chitin- and PGN-induced immunity in rice. Rice, 10(1): 6.
[47]	Liang J H, Lu L, Zhou H L, Fang J B, Zhao Y F, Hou H N, Chen L Z, Cao C, Yang D W, Diao Z J, Tang D Z, Li S P. 2024. Receptor-like kinases OsRLK902-1 and OsRLK902-2 form immune complexes with OsRLCK185 to regulate rice blast resistance. J Exp Bot, 75(5): 1565-1579.
[48]	Liang X X, Zhou J M. 2018. Receptor-like cytoplasmic kinases: Central players in plant receptor kinase-mediated signaling. Annu Rev Plant Biol, 69: 267-299.
[49]	Lin S D, Yao Y, Li J Y, Li X B, Ma J, Weng H Y, Cheng Z X, Ye D P. 2023. Application of UAV-based imaging and deep learning in assessment of rice blast resistance. Rice Sci, 30(6): 652-660.
[50]	Liu F R, Zhang W G, Schwessinger B, Wei T, Ruan D L, Ronald P. 2020. The rice Xa3 gene confers resistance to Xanthomonas oryzae pv. oryzae in the model rice Kitaake genetic background. Front Plant Sci, 11: 49.
[51]	Liu W D, Liu J L, Triplett L, Leach J E, Wang G L. 2014. Novel insights into rice innate immunity against bacterial and fungal pathogens. Annu Rev Phytopathol, 52: 213-241.
[52]	Liu W D, Wang G L. 2016. Plant innate immunity in rice: A defense against pathogen infection. Natl Sci Rev, 3(3): 295-308.
[53]	Liu Y N, Huang X C, Li M, He P, Zhang Y L. 2016. Loss-of- function of Arabidopsis receptor-like kinase BIR1 activates cell death and defense responses mediated by BAK1 and SOBIR1. New Phytol, 212(3): 637-645.
[54]	Liu Z Q, Zhu Y J, Shi H B, Qiu J H, Ding X H, Kou Y J. 2021. Recent progress in rice broad-spectrum disease resistance. Int J Mol Sci, 22(21): 11658.
[55]	Lu D P, Wu S J, Gao X Q, Zhang Y L, Shan L B, He P. 2010. A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc Natl Acad Sci USA, 107(1): 496-501.
[56]	Luu D D, Joe A, Chen Y, Parys K, Bahar O, Pruitt R, Chan L J G, Petzold C J, Long K, Adamchak C, Stewart V, Belkhadir Y, Ronald P C. 2019. Biosynthesis and secretion of the microbial sulfated peptide Ra_xX and binding to the rice XA21 immune receptor. Proc Natl Acad Sci USA, 116(17): 8525-8534.
[57]	Ma W, Smigel A, Tsai Y C, Braam J, Berkowitz G A. 2008. Innate immunity signaling: Cytosolic Ca²⁺ elevation is linked to downstream nitric oxide generation through the action of calmodulin or a calmodulin-like protein. Plant Physiol, 148(2): 818-828.
[58]	Macho A P, Zipfel C. 2015. Targeting of plant pattern recognition receptor-triggered immunity by bacterial type-III secretion system effectors. Curr Opin Microbiol, 23: 14-22.
[59]	Madala N E, Molinaro A, Dubery I A. 2012. Distinct carbohydrate and lipid-based molecular patterns within lipopolysaccharides from Burkholderia cepacia contribute to defense-associated differential gene expression in Arabidopsis thaliana. Innate Immun, 18(1): 140-154.
[60]	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. Breed Sci, 66(3): 396-406.
[61]	Malukani K K, Ranjan A, Hota S J, Patel H K, Sonti R V. 2020. Dual activities of receptor-like kinase OsWAKL21.2 induce immune responses. Plant Physiol, 183(3): 1345-1363.
[62]	Mei Q, Fu Y W, Li T M, Xuan Y H. 2022. Ac/Ds-induced receptor- like kinase genes deletion provides broad-spectrum resistance to bacterial blight in rice. Int J Mol Sci, 23(9): 4561.
[63]	Monaghan J, Zipfel C. 2012. Plant pattern recognition receptor complexes at the plasma membrane. Curr Opin Plant Biol, 15(4): 349-357.
[64]	Moon H, Jeong A R, Park C J. 2024. Rice NLR protein XinN1, induced by a pattern recognition receptor XA21, confers enhanced resistance to bacterial blight. Plant Cell Rep, 43(3): 72.
[65]	Mou B H, Zhao G S, Wang J Y, Wang S Z, He F, Ning Y S, Li D Y, Zheng X H, Cui F H, Xue F, Zhang S Y, Sun W X. 2024. The OsCPK17-OsPUB12-OsRLCK176 module regulates immune homeostasis in rice. Plant Cell, 36(4): 987-1006.
[66]	Naito K, Taguchi F, Suzuki T, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y. 2008. Amino acid sequence of bacterial microbe- associated molecular pattern flg22 is required for virulence. Mol Plant Microbe Interact, 21(9): 1165-1174.
[67]	Nicaise V, Roux M, Zipfel C. 2009. Recent advances in PAMP- triggered immunity against bacteria: Pattern recognition receptors watch over and raise the alarm. Plant Physiol, 150(4): 1638-1647.
[68]	Nikko, Ramdan E P, Risnawati, Sugeru H. 2023. Suppression of Xanthomonas oryzae pv. oryzae infection in rice seeds: Investigating the optimal temperature and packaging conditions for enhanced pathogen control and seed quality. J Ilm Pertan, 20(2): 109-117.
[69]	Oliva R, Ji C H, Atienza-Grande G, Huguet-Tapia J C, Perez- Quintero A, Li T, Eom J S, Li C H, Nguyen H, Liu B, Auguy F, Sciallano C, Luu V T, Dossa G S, Cunnac S, Schmidt S M, Slamet-Loedin I H, Cruz C V, Szurek B, Frommer W B, White F F, Yang B. 2019. Broad-spectrum resistance to bacterial blight in rice using genome editing. Nat Biotechnol, 37(11): 1344-1350.
[70]	Park C J, Song M Y, Kim C Y, Jeon J S, Ronald P C. 2014. Rice BiP3 regulates immunity mediated by the PRRs XA3 and XA21 but not immunity mediated by the NB-LRR protein, Pi5. Biochem Biophys Res Commun, 448( 1): 70-75.
[71]	Peng H, Zhang Q, Li Y D, Lei C L, Zhai Y, Sun X H, Sun D Y, Sun Y, Lu T G. 2009. A putative leucine-rich repeat receptor kinase, OsBRR1, is involved in rice blast resistance. Planta, 230(2): 377-385.
[72]	Peng H C, Kaloshian I. 2014. The tomato leucine-rich repeat receptor- like kinases SlSERK3A and SlSERK3B have overlapping functions in bacterial and nematode innate immunity. PLoS One, 9(3): e93302.
[73]	Petutschnig E K, Jones A M E, Serazetdinova L, Lipka U, Lipka V. 2010. The lysin motif receptor-like kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J Biol Chem, 285(37): 28902-28911.
[74]	Qian Q, Huang L, Yi R, Wang S Z, Ding Y. 2014. Enhanced resistance to blast fungus in rice (Oryza sativa L.) by expressing the ribosome-inactivating protein α-momorcharin. Plant Sci, 217/218: 1-7.
[75]	Rao T B, Chopperla R, Prathi N B, Balakrishnan M, Prakasam V, Laha G S, Balachandran S M, Mangrauthia S K. 2020. A comprehensive gene expression profile of pectin degradation enzymes reveals the molecular events during cell wall degradation and pathogenesis of rice sheath blight pathogen Rhizoctonia solani AG1-IA. J Fungi, 6(2): 71.
[76]	Rao Y C, Jiao R, Wang S, Wu X M, Ye H F, Pan C Y, Li S F, Xin D D, Zhou W Y, Dai G X, Hu J, Ren D Y, Wang Y X. 2021. SPL36 encodes a receptor-like protein kinase that regulates programmed cell death and defense responses in rice. Rice, 14(1): 34.
[77]	Rüter C, Schmidt M A. 2017. Cell-penetrating bacterial effector proteins: Better tools than targets. Trends Biotechnol, 35(2): 109-120.
[78]	Sasaki A, Ashikari M, Ueguchi-Tanaka M, Itoh H, Nishimura A, Swapan D, Ishiyama K, Saito T, Kobayashi M, Khush G S, Kitano H, Matsuoka M. 2002. Green revolution: A mutant gibberellin- synthesis gene in rice. Nature, 416: 701-702.
[79]	Sathe A P, Su X N, Chen Z, Chen T, Wei X J, Tang S Q, Zhang X B, Wu J L. 2019. Identification and characterization of a spotted- leaf mutant spl40 with enhanced bacterial blight resistance in rice. Rice, 12(1): 68.
[80]	Shang H H, Li P P, Zhang X B, Xu X, Gong J Y, Yang S H, He Y Q, Wu J L. 2022. The gain-of-function mutation, OsSpl26, positively regulates plant immunity in rice. Int J Mol Sci, 23(22): 14168.
[81]	Shi X J, Qin T Z, Liu H, Wu M, Li J J, Shi Y S, Gao Y B, Ren A Z. 2020. Endophytic fungi activated similar defense strategies of Achnatherum sibiricum host to different trophic types of pathogens. Front Microbiol, 11: 1607.
[82]	Shiu S H, Bleecker A B. 2001. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA, 98(19): 10763-10768.
[83]	Shiu S H, Karlowski W M, Pan R S, Tzeng Y H, Mayer K F X, Li W H. 2004. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell, 16(5): 1220-1234.
[84]	Singh R, Sunder S, Kumar P. 2016. Sheath blight of rice: Current status and perspectives. Indian Phytopathol, 69(4): 340-351.
[85]	Song D H, Li G J, Song F M, Zheng Z. 2008. Molecular characterization and expression analysis of OsBISERK1, a gene encoding a leucine- rich repeat receptor-like kinase, during disease resistance responses in rice. Mol Biol Rep, 35(2): 275-283.
[86]	Sun W X, Fan J, Fang A F, Li Y J, Tariqjaveed M, Li D Y, Hu D W, Wang W M. 2020. Ustilaginoidea virens: Insights into an emerging rice pathogen. Annu Rev Phytopathol, 58: 363-385.
[87]	Sun X L, Cao Y L, Yang Z F, Xu C G, Li X H, Wang S P, Zhang Q F. 2004. Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. Plant J, 37(4): 517-527.
[88]	Tan J Y, Zhang X B, Shang H H, Li P P, Wang Z H, Liao X W, Xu X, Yang S H, Gong J Y, Wu J L. 2023. ORYZA SATIVA SPOTTED- LEAF 41 (OsSPL41) negatively regulates plant immunity in rice. Rice Sci, 30(5): 426-436.
[89]	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. Plant Cell, 18(1): 257-273.
[90]	Versteeg G A, Rajsbaum R, Sánchez-Aparicio M T, Maestre A M, Valdiviezo J, Shi M, Inn K S, Fernandez-Sesma A, Jung J, García-Sastre A. 2013. The E3-ligase TRIM family of proteins regulates signaling pathways triggered by innate immune pattern- recognition receptors. Immunity, 38(2): 384-398.
[91]	Vij S, Giri J, Dansana P K, Kapoor S, Tyagi A K. 2008. The receptor-like cytoplasmic kinase (OsRLCK) gene family in rice: Organization, phylogenetic relationship, and expression during development and stress. Mol Plant, 1(5): 732-750.
[92]	Wan J R, Zhang X C, Neece D, Ramonell K M, Clough S, Kim S Y, Stacey M G, Stacey G. 2008. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell, 20(2): 471-481.
[93]	Wang A J, Shu X Y, Jing X, Jiao C Z, Chen L, Zhang J F, Ma L, Jiang Y Q, Yamamoto N, Li S C, Deng Q M, Wang S Q, Zhu J, Liang Y Y, Zou T, Liu H N, Wang L X, Huang Y B, Li P, Zheng A P. 2021. Identification of rice (Oryza sativa L.) genes involved in sheath blight resistance via a genome-wide association study. Plant Biotechnol J, 19(8): 1553-1566.
[94]	Wang C, Wang G, Zhang C, Zhu P K, Dai H L, Yu N, He Z H, Xu L, Wang E T. 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.
[95]	Wang J, Qu B Y, Dou S J, Li L Y, Yin D D, Pang Z Q, Zhou Z Z, Tian M M, Liu G Z, Xie Q, Tang D Z, Chen X W, Zhu L H. 2015. The E3 ligase OsPUB15 interacts with the receptor-like kinase PID2 and regulates plant cell death and innate immunity. BMC Plant Biol, 15: 49.
[96]	Wang K, Li S, Yang Z Y, Chen C, Fu Y H, Du H T, Sun H Z, Li J Z, Zhao Q Z, Du C Q. 2023. L-type lectin receptor-like kinase OsCORK1 as an important negative regulator confers copper stress tolerance in rice. J Hazard Mater, 459: 132214.
[97]	Wang L L, Ma Z B, Kang H X, Gu S, Mukhina Z, Wang C H, Wang H, Bai Y J, Sui G M, Zheng W J, Ma D R. 2022. Cloning and functional analysis of the novel rice blast resistance gene Pi65 in japonica rice. Theor Appl Genet, 135(1): 173-183.
[98]	Wang L L, Xu G J, Li L H, Ruan M Y, Bennion A, Wang G L, Li R, Qu S H. 2023. The OsBDR1-MPK3 module negatively regulates blast resistance by suppressing the jasmonate signaling and terpenoid biosynthesis pathway. Proc Natl Acad Sci USA, 120(13): e2211102120.
[99]	Wang Z Y, Zhou L, Lan Y, Li X J, Wang J, Dong J F, Guo W, Jing D D, Liu Q, Zhang S H, Liu Z Y, Shi W J, Yang W, Yang T F, Sun F, Du L L, Fu H, Ma Y M, Shao Y D, Chen L, Li J T, Li S, Fan Y J, Wang Y Y, Leung H, Liu B, Zhou Y J, Zhao J L, Zhou T. 2022. An aspartic protease 47 causes quantitative recessive resistance to rice black-streaked dwarf virus disease and southern rice black- streaked dwarf virus disease. New Phytol, 233(6): 2520-2533.
[100]	Wei T, Chern M, Liu F R, Ronald P C. 2016. Suppression of bacterial infection in rice by treatment with a sulfated peptide. Mol Plant Pathol, 17(9): 1493-1498.
[101]	Xiao X R, Wang R, Guo W Y, Khaskhali S, Fan R C, Zhao R, Li C X, He C Z, Niu X L, Chen Y H. 2022. The receptor-like cytoplasmic kinase OsRLCK118 regulates plant development and basal immunity in rice (Oryza sativa L.). Tropical Plants, 1: 4.
[102]	Xu J M, Wang C L, Wang F J, Liu Y P, Li M, Wang H J, Zheng Y H, Zhao K J, Ji Z Y. 2023. PWL1, a G-type lectin receptor-like kinase, positively regulates leaf senescence and heat tolerance but negatively regulates resistance to Xanthomonas oryzae in rice. Plant Biotechnol J, 21(12): 2525-2545.
[103]	Xu Y, Fu S, Tao X R, Zhou X P. 2021. Rice stripe virus: Exploring molecular weapons in the arsenal of a negative-sense RNA virus. Annu Rev Phytopathol, 59: 351-371.
[104]	Yang L Y. 2024. Posttranslational modifications of OsRLCK176 as a molecular switch to balance growth and immunity in rice. Plant Cell, 36(4): 801-802.
[105]	Yang X R, Yan S Y, Li Y J, Li G S, Sun S Q, Li J L, Cui Z Q, Huo J F, Sun Y, Wang X J, Liu F Z. 2023. Comparison of transcriptome between tolerant and susceptible rice cultivar reveals positive and negative regulators of response to Rhizoctonia solani in rice. Int J Mol Sci, 24(18): 14310.
[106]	Yin Z Y, Liu J D, Dou D L. 2024. RLKdb: A comprehensively curated database of plant receptor-like kinase families. Mol Plant, 17(4): 513-515.
[107]	Yoo Y, Park J C, Cho M H, Yang J, Kim C Y, Jung K H, Jeon J S, An G, Lee S W. 2018. Lack of a cytoplasmic RLK, required for ROS homeostasis, induces strong resistance to bacterial leaf blight in rice. Front Plant Sci, 9: 577.
[108]	Yuan M H, Jiang Z Y, Bi G Z, Nomura K, Liu M H, Wang Y P, Cai B Y, Zhou J M, He S Y, Xin X F. 2021. Pattern-recognition receptors are required for NLR-mediated plant immunity. Nature, 592: 105-109.
[109]	Zhai K R, Liang D, Li H L, Jiao F Y, Yan B X, Liu J, Lei Z Y, Huang L, Gong X Y, Wang X, Miao J S, Wang Y C, Liu J Y, Zhang L, Wang E T, Deng Y W, Wen C K, Guo H W, Han B, He Z H. 2022. NLRs guard metabolism to coordinate pattern- and effector-triggered immunity. Nature, 601: 245-251.
[110]	Zhang F M, Cao Z Z, Zheng X, He Y T, Chen M X, Lin X Y. 2024. Interaction between Ustilaginoidea virens and rice and its sustainable control. Rice Sci, 31(3): 269-284.
[111]	Zhang H H, Chen C H, Li L L, Tan X X, Wei Z Y, Li Y J, Li J M, Yan F, Chen J P, Sun Z T. 2021. A rice LRR receptor-like protein associates with its adaptor kinase OsSOBIR1 to mediate plant immunity against viral infection. Plant Biotechnol J, 19(11): 2319-2332.
[112]	Zhang N, Dong X O, Jain R, Ruan D L, de Araujo Junior A T, Li Y, Lipzen A, Martin J, Barry K, Ronald P C. 2024. XA21-mediated resistance to Xanthomonas oryzae pv. oryzae is dose dependent. PeerJ, 12: e17323.
[113]	Zhang X W, Dong W T, Sun J, Feng F, Deng Y W, He Z H, Oldroyd G E D, Wang E T. 2015. The receptor kinase CERK1 has dual functions in symbiosis and immunity signalling. Plant J, 81(2): 258-267.
[114]	Zhang Y, Liu Q N, Zhang Y X, Chen Y Y, Yu N, Cao Y R, Zhan X D, Cheng S H, Cao L Y. 2019. LMM24 encodes receptor-like cytoplasmic kinase 109, which regulates cell death and defense responses in rice. Int J Mol Sci, 20(13): 3243.
[115]	Zhao J, Fu J, Li X H, Xu C G, Wang S P. 2009. Dissection of the factors affecting development-controlled and race-specific disease resistance conferred by leucine-rich repeat receptor kinase-type R genes in rice. Theor Appl Genet, 119(2): 231-239.
[116]	Zhao Q Q, Bao J L, Li H L, Hu W, Kong Y Q, Zhong Y F, Fu Q, Xu G L, Liu F M, Jiao X, Jin J, Ming Z H. 2024. Structural and biochemical basis of FLS2-mediated signal activation and transduction in rice. Plant Commun, 5(3): 100785.
[117]	Zhou X G, Wang J, Peng C F, Zhu X B, Yin J J, Li W T, He M, Wang J C, Chern M, Yuan C, Wu W G, Ma W W, Qin P, Ma B T, Wu X J, Li S G, Ronald P, Chen X W. 2016. Four receptor-like cytoplasmic kinases regulate development and immunity in rice. Plant Cell Environ, 39(6): 1381-1392.
[118]	Zhou Y B, Zhang Z H, Zhao X H, Liu L, Tang Q Y, Fu J, Tang X D, Yang R Q, Lin J Z, Liu X M, Yang Y Z. 2023. Receptor-like cytoplasmic kinase STK confers salt tolerance in rice. Rice, 16(1): 21.
[119]	Zhu Z, Wang T X Z, Lan J P, Ma J J, Xu H Q, Yang Z X, Guo Y L, Chen Y, Zhang J S, Dou S J, Yang M, Li L Y, Liu G Z. 2022. Rice MPK17 plays a negative role in the Xa21-mediated resistance against Xanthomonas oryzae pv. oryzae. Rice, 15(1): 41.
[120]	Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones J D G, Boller T, Felix G. 2006. Perception of the bacterial PAMP EF-tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell, 125(4): 749-760.

Gene name	RLK/RLCK	Function	Reference
OsSERK1	RLK	Enhances the resistance of rice plants to rice blast pathogen	Hu et al, 2005
Pi-d2	RLK	Enhances the resistance of rice plants to rice blast pathogen	Chen et al, 2006; Kouzai et al, 2013
OsBISERK1	RLK	Critical component in rice’s defense against rice blast disease	Song et al, 2008
OsWAK1/14/25/91/92	RLK	Enhances plant resistance during the rice defense against rice blast disease	Li et al, 2009; Delteil et al, 2016; Harkenrider et al, 2016
OsBRR1	RLK	Moderate resistance to rice blast pathogen, susceptibility increased when suppressed	Peng et al, 2009
OsCERK1	RLK	Forms a crucial receptor complex on the plasma membrane, essential for activating the immune response triggered by fungal chitin; Recognizes peptidoglycan and chitin together with other receptor proteins	Akamatsu et al, 2013; Zhang et al, 2015; Wang et al, 2017
OsWAK112d	RLK	Acts as a negative regulator, influencing rice disease resistance	Delteil et al, 2016
LOC_Os08g10300	RLK	Over-expression significantly enhances rice resistance to rice blast disease	Li et al, 2016
SDS2	RLK	Enhances the resistance of rice plants to rice blast pathogen	Fan et al, 2018
Pi65	RLK	Enhances the resistance to rice blast disease when over-expressed	Wang L L et al, 2022
OsBDR1	RLK	Negatively regulates rice resistance to rice blast pathogen by interacting with MPK3, inhibiting jasmonic acid signaling and terpenoid biosynthesis pathways	Wang L L et al, 2023
OsRLK902-1/2	RLK	Positively regulates rice resistance to rice blast by forming an immune complex with OsRLCK185	Liang et al, 2024
OsRLCK57/107/ 118/176/185	RLCK	Enhances the resistance of rice plants to rice blast pathogen	Ao et al, 2014; Li et al, 2017; Wang et al, 2017; Fan et al, 2018; Liang et al, 2024
BSR1	RLCK	Plays a vital intermediary role in immune response, boosting rice resistance against rice blast fungus	Kanda et al, 2017, 2020
RLCK109	RLCK	Plays a key role in regulating cell death and defense responses, enhancing rice resistance to rice blast fungus	Zhang et al, 2019
RLCK188	RLCK	Enhances plant resistance during the rice defense against rice blast disease	Xiao et al, 2022
OsBSK1-2	RLCK	Reduces rice resistance to rice blast fungus	Li et al, 2024

Gene name	RLK/RLCK	Function	Reference
OsSERK1	RLK	Enhances the resistance of rice plants to rice blast pathogen	Hu et al, 2005
Pi-d2	RLK	Enhances the resistance of rice plants to rice blast pathogen	Chen et al, 2006; Kouzai et al, 2013
OsBISERK1	RLK	Critical component in rice’s defense against rice blast disease	Song et al, 2008
OsWAK1/14/25/91/92	RLK	Enhances plant resistance during the rice defense against rice blast disease	Li et al, 2009; Delteil et al, 2016; Harkenrider et al, 2016
OsBRR1	RLK	Moderate resistance to rice blast pathogen, susceptibility increased when suppressed	Peng et al, 2009
OsCERK1	RLK	Forms a crucial receptor complex on the plasma membrane, essential for activating the immune response triggered by fungal chitin; Recognizes peptidoglycan and chitin together with other receptor proteins	Akamatsu et al, 2013; Zhang et al, 2015; Wang et al, 2017
OsWAK112d	RLK	Acts as a negative regulator, influencing rice disease resistance	Delteil et al, 2016
LOC_Os08g10300	RLK	Over-expression significantly enhances rice resistance to rice blast disease	Li et al, 2016
SDS2	RLK	Enhances the resistance of rice plants to rice blast pathogen	Fan et al, 2018
Pi65	RLK	Enhances the resistance to rice blast disease when over-expressed	Wang L L et al, 2022
OsBDR1	RLK	Negatively regulates rice resistance to rice blast pathogen by interacting with MPK3, inhibiting jasmonic acid signaling and terpenoid biosynthesis pathways	Wang L L et al, 2023
OsRLK902-1/2	RLK	Positively regulates rice resistance to rice blast by forming an immune complex with OsRLCK185	Liang et al, 2024
OsRLCK57/107/ 118/176/185	RLCK	Enhances the resistance of rice plants to rice blast pathogen	Ao et al, 2014; Li et al, 2017; Wang et al, 2017; Fan et al, 2018; Liang et al, 2024
BSR1	RLCK	Plays a vital intermediary role in immune response, boosting rice resistance against rice blast fungus	Kanda et al, 2017, 2020
RLCK109	RLCK	Plays a key role in regulating cell death and defense responses, enhancing rice resistance to rice blast fungus	Zhang et al, 2019
RLCK188	RLCK	Enhances plant resistance during the rice defense against rice blast disease	Xiao et al, 2022
OsBSK1-2	RLCK	Reduces rice resistance to rice blast fungus	Li et al, 2024

Gene name	RLK/RLCK	Function	Reference
Xa26	RLK	Provides resistance to bacterial blight at different growth stages	Sun et al, 2004; Zhao et al, 2009
Xa21	RLK	Encodes a receptor kinase conferring broad-spectrum resistance to bacterial blight, and recognizes sulfated peptide RaxX	Chen et al, 2010; Luu et al, 2019; Wei et al, 2016; Moon et al, 2024
OsCERK1	RLK	Recognizes bacterial pathogen-specific molecular pattern peptidoglycan; The immune response triggered by lipopolysaccharides is almost completely suppressed in the absence of OsCERK1	Ao et al, 2014; Desaki et al, 2018
OsSERK2	RLK	Interacts with XA21, positively regulating rice resistance to bacterial blight	Chen et al, 2014
XIK1	RLK	Negatively regulates rice resistance to bacterial leaf blight	Hu et al, 2015
WAK25	RLK	Weakens rice resistance to bacterial leaf blight	Harkenrider et al, 2016
SPL26/36/40/41	RLK	Negatively regulates rice resistance to bacterial leaf blight	Sathe et al, 2019; Rao et al, 2021; Shang et al, 2022; Tan et al, 2023
Xa3	RLK	Similar to Xa26, provides resistance to bacterial blight	Liu et al, 2020
OsWAKL21.2	RLK	Positively regulates rice resistance against bacterial leaf blight	Malukani et al, 2020
RIR1	RLK	Makes plants more susceptible to bacterial leaf blight infection	An et al, 2022
RLK20/21/22	RLK	Positively regulates rice resistance against bacterial leaf blight	Mei et al, 2022
PWL1	RLK	Negatively regulates rice resistance to bacterial leaf blight	Xu et al, 2023
NRRB	RLCK	Lacking NRRB shows robust resistance to bacterial leaf blight	Guo et al, 2014
BSR1	RLCK	Boosts rice resistance to Xoo when over-expressed	Maeda et al, 2016
OsRLCK57/107/ 118/176	RLCK	Positively regulates rice resistance against bacterial leaf blight	Zhou et al, 2016; Xiao et al, 2022
rrsRLK	RLCK	Lacking rrsRLK shows robust resistance to bacterial leaf blight	Yoo et al, 2018

Gene name	RLK/RLCK	Function	Reference
Xa26	RLK	Provides resistance to bacterial blight at different growth stages	Sun et al, 2004; Zhao et al, 2009
Xa21	RLK	Encodes a receptor kinase conferring broad-spectrum resistance to bacterial blight, and recognizes sulfated peptide RaxX	Chen et al, 2010; Luu et al, 2019; Wei et al, 2016; Moon et al, 2024
OsCERK1	RLK	Recognizes bacterial pathogen-specific molecular pattern peptidoglycan; The immune response triggered by lipopolysaccharides is almost completely suppressed in the absence of OsCERK1	Ao et al, 2014; Desaki et al, 2018
OsSERK2	RLK	Interacts with XA21, positively regulating rice resistance to bacterial blight	Chen et al, 2014
XIK1	RLK	Negatively regulates rice resistance to bacterial leaf blight	Hu et al, 2015
WAK25	RLK	Weakens rice resistance to bacterial leaf blight	Harkenrider et al, 2016
SPL26/36/40/41	RLK	Negatively regulates rice resistance to bacterial leaf blight	Sathe et al, 2019; Rao et al, 2021; Shang et al, 2022; Tan et al, 2023
Xa3	RLK	Similar to Xa26, provides resistance to bacterial blight	Liu et al, 2020
OsWAKL21.2	RLK	Positively regulates rice resistance against bacterial leaf blight	Malukani et al, 2020
RIR1	RLK	Makes plants more susceptible to bacterial leaf blight infection	An et al, 2022
RLK20/21/22	RLK	Positively regulates rice resistance against bacterial leaf blight	Mei et al, 2022
PWL1	RLK	Negatively regulates rice resistance to bacterial leaf blight	Xu et al, 2023
NRRB	RLCK	Lacking NRRB shows robust resistance to bacterial leaf blight	Guo et al, 2014
BSR1	RLCK	Boosts rice resistance to Xoo when over-expressed	Maeda et al, 2016
OsRLCK57/107/ 118/176	RLCK	Positively regulates rice resistance against bacterial leaf blight	Zhou et al, 2016; Xiao et al, 2022
rrsRLK	RLCK	Lacking rrsRLK shows robust resistance to bacterial leaf blight	Yoo et al, 2018

Gene name	RLK/RLCK	Function	Reference
WAK25	RLK	Over-expression weakens rice resistance to necrotrophic fungal pathogens like sheath blight, increasing susceptibility	Harkenrider et al, 2016
OsSOBIR1	RLK	Interaction between OsSOBIR1 and the receptor-like protein OsRLP1 enhances rice resistance to rice black-streaked dwarf virus	Zhang et al, 2021
WAK91	RLK	Specific mutations enhance rice resistance to sheath blight, holding potential significance for reducing yield losses	Al-Bader et al, 2023
BSR1	RLCK	Over-expression significantly enhances rice resistance to sheath blight	Maeda et al, 2016
OsRLCK5	RLCK	Interacts with rice glutaredoxin GRX20 and participates in ascorbate-glutathione cycle to enhance rice defense against reactive oxygen species, augmenting resistance to sheath blight	Wang et al, 2021