Research Papers

Response Characteristics of Rice Cysteine-rich Receptor-like Kinases Family Genes to Rhizoctonia solani and Plant Hormones

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  • 1Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding / Key Laboratory of Plant Functional Genomics of Ministry of Education, College of Agriculture, Yangzhou University, Yangzhou 225009, China
    2Jiangsu Collaborative Innovation Center for Modern Industrial Technology of Grain Crops / Jiangsu Key Laboratory of Crop Genetics and Physiology, Yangzhou University, Yangzhou 225009, China

Received date: 2021-03-06

  Revised date: 2021-03-25

  Online published: 2021-09-10

Abstract

【Objective】 Clarifying the response characteristics of rice cysteine-rich receptor-like kinases (CRKs) family genes to Rhizoctonia solani and plant hormones is important preliminary work to analyze the functions of CRKs in rice resistance to R. solani. 【Method】 A phylogenetic tree of 45 CRKs in rice was constructed by bioinformatics. qPCR was used to analyze their response characteristics to R. solani, plant hormones ethylene (ET), jasmonic acid (JA), salicylic acid (SA) and cytokinin (CK), and their expression patterns in different tissues.【Result】 The rice CRKs family can be divided into four groups. Most of the CRKs clustered or closely distributed on chromosomes from the same group or branch. Forty-one CRKs responded to R. solani infection, and 17 of them responded strongly. Combined with their tissue expression patterns, it was found that 10 of the 17 CRKs, including CRK15, CRK23, CRK24, CRK26, CRK27, CRK28, CRK29, CRK30, CRK31 and CRK33, were expressed strongly in leaf sheathes and leaves, suggesting that these genes may be involved in regulating resistance to sheath blight. Most of CRKs from the same branch had similar response characteristics to R. solani, indicating that these CRKs may have functional redundancy in regulating resistance to R. solani. Forty CRKs responded to three or four kinds of plant hormones, and their responses to different hormones varied, indicating that CRKs might be widely involved in these plant hormones-mediated defense pathways. There were 17 CRKs with opposite responses to JA and SA, 21 with similar responses to JA and SA, 21 with similar responses to ET and JA, and 23 with similar responses to ET and SA, respectively. These genes may be involved in the interactions among ET, JA and SA. The results not only reflected the synergistic and antagonistic effects of ET, JA and SA signaling pathways, but also indicated that these genes may participate in the interactions among ET, JA and SA.【Conclusion】 Some rice CRKs involved in the regulation of rice sheath blight resistance have been identified, and they may play roles in the plant hormones-mediated defense pathways, which provides scientific clues for us to further explore the function of CRKs in regulating rice sheath blight resistance.

Cite this article

Zhiming FENG, Guangda WANG, Jianhua ZHAO, Ran JU, Mengchen LI, Peng GAO, Keming HU, Zongxiang CHEN, Shimin ZUO . Response Characteristics of Rice Cysteine-rich Receptor-like Kinases Family Genes to Rhizoctonia solani and Plant Hormones[J]. Chinese Journal OF Rice Science, 2021 , 35(5) : 439 -448 . DOI: 10.16819/j.1001-7216.2021.210305

References

[1] Jones J D, Dangl J L. The plant immune system[J]. Nature, 2006, 444(7117): 323-329.
[2] Liang X X, Zhou J M. Receptor-like cytoplasmic kinases: Central players in plant receptor kinase-mediated signaling[J]. Annual Review of Plant Biology, 2018, 69(1): 267-299.
[3] Chen Z A. Superfamily of proteins with novel cysteine- rich repeats[J]. Plant Physiology, 2001, 126(2): 473-476.
[4] Bourdais G, Burdiak P, Gauthier A, Nitsch L, Salojärvi J, Rayapuram C, Idänheimo N, Hunter K, Kimura S, et al. Large-scale phenomics identifies primary and fine-tuning roles for CRKs in responses related to oxidative stress[J]. PLoS Genetics, 2015, 11(7): e1005373.
[5] Sawano Y, Miyakawa T, Yamazaki H, Tanokura M, Hatano K. Purification, characterization, and molecular gene cloning of an antifungal protein from Ginkgo biloba seeds[J]. Biological Chemistry, 2007, 388(3): 273-280.
[6] Chen K, Du L, Chen Z. Sensitization of defense responses and activation of programmed cell death by a pathogen-induced receptor-like protein kinase in Arabidopsis[J]. Plant Molecular Biology, 2003, 53(1): 61-74.
[7] Acharya B R, Raina S, Maqbool S B, Jagadeeswaran G, Mosher S L, Appel H M, Schultz J C. Overexpression of CRK13, an Arabidopsis cysteine-rich receptor-like kinase, results in enhanced resistance to Pseudomonas syringae[J]. Plant Journal, 2007, 50(3): 488-499.
[8] Czernic P, Visser B, Sun W, Savoure A, Deslandes L, Marco Y, van Montagu M, Verbruggen N. Characterization of an Arabidopsis thaliana receptor-like protein kinase gene activated by oxidative stress and pathogen attack[J]. Plant Journal, 1999, 18(3): 321-327.
[9] Chen K, Fan B, Du L, Chen Z. Activation of hypersensitive cell death by pathogen-induced receptor- like protein kinases from Arabidopsis[J]. Plant Molecular Biology, 2004, 56(2): 271-283.
[10] Yeh Y H, Chang Y H, Huang P Y, Huang J B, Zimmerli L. Enhanced Arabidopsis pattern-triggered immunity by overexpression of cysteine-rich receptor-like kinases[J]. Frontiers in Plant Science, 2015, 6(6): 322.
[11] Idänheimo N, Gauthier A, Salojärvi J, Siligato R, Brosché M, Kollist H, Mähönen A P, Kangasjärvi J. The Arabidopsis thaliana cysteine-rich receptor-like kinases CRK6 and CRK7 protect against apoplastic oxidative stress[J]. Biochemical and Biophysical Research Communications, 2014, 445(2): 457-462.
[12] Yang K, Rong W, Qi L, Li J, Wei X, Zhang Z. Isolation and characterization of a novel wheat cysteine-rich receptor-like kinase gene induced by Rhizoctonia cerealis[J]. Scientific Reports, 2013, 3: 3021.
[13] Chern M, Xu Q, Bart R S, Bai W, Ruan D, Sze-To W H, Canlas P E, Jain R, Chen X, Ronald P C. A genetic screen identifies a requirement for cysteine-rich-receptor-like kinases in rice nh1 (osnpr1)-mediated immunity[J]. PLoS Genetics, 2016, 12(5): e1006049.
[14] Li T G, Zhang D D, Zhou L, Kong Z Q, Hussaini A S, Wang D, Li J J, Short D P, Dhar N, Klosterman S J, Wang B L, Yin C M, Subbarao K V, Chen J Y, Dai X F. Genome-wide identification and functional analyses of the CRK gene family in cotton reveals GbCRK18 confers verticillium wilt resistance in Gossypium barbadense[J]. Frontiers in Plant Science, 2018, 9: 1266.
[15] Saintenac C, Cambon F, Aouini L, Verstappen E, Ghaffary S M T, Poucet T, Marande W, Berges H, Xu S, Jaouannet M. A wheat cysteine-rich receptor-like kinase confers broad-spectrum resistance against Septoria tritici blotch[J]. Nature Communications, 2021, 12: 433.
[16] 左示敏, 张亚芳, 陈宗祥, 陈夕军, 潘学彪. 水稻抗纹枯病遗传育种研究进展[J]. 中国科学: 生命科学, 2010, 40(11): 1014-1023.
[16] Zuo S M, Zhang Y F, Chen Z X, Pan X B. Current progress on genetics and breeding in resistance to rice sheath blight[J]. Scientia Sinica Vitae, 2010, 40(11): 1014-1023. (in Chinese with English abstract)
[17] Molla K A, Karmakar S, Molla J, Bajaj P, Varshney R K, Datta S K, Datta K. Understanding sheath blight resistance in rice: The road behind and the road ahead[J]. Plant Biotechnology Journal, 2020, 18(4): 895-915.
[18] Qiao L, Zheng L, Sheng C, Zhao H, Jin H, Niu D. Rice siR109944 suppresses plant immunity to sheath blight and impacts multiple agronomic traits by affecting auxin homeostasis[J]. Plant Journal, 2020, 102(5): 948-964.
[19] Peng X, Hu Y, Tang X, Zhou P, Deng X, Wang H, Guo Z. Constitutive expression of rice WRKY30 gene increases the endogenous jasmonic acid accumulation, PR gene expression and resistance to fungal pathogens in rice[J]. Planta, 2012, 236(5): 1485-1498.
[20] Peng X, Wang H, Jang J C, Xiao T, He H, Jiang D, Tang X. OsWRKY80-OsWRKY4 module as a positive regulatory circuit in rice resistance against Rhizoctonia solani[J]. Rice, 2016, 9: 63.
[21] Helliwell E E, Wang Q, Yang Y. Transgenic rice with inducible ethylene production exhibits broad-spectrum disease resistance to the fungal pathogens Magnaporthe oryzae and Rhizoctonia solani[J]. Plant Biotechnology Journal, 2013, 11(1): 33-42.
[22] Sadumpati V, Kalambur M, Vudem D R, Kirti P B. Transgenic indica rice lines, expressing Brassica juncea Nonexpressor of pathogenesis-related genes 1 (BjNPR1), exhibit enhanced resistance to major pathogens[J]. Journal of Biotechnology, 2013, 166(3): 114-121.
[23] Kouzai Y, Kimura M, Watanabe M, Kusunoki K, Osaka D, Suzuki T, Matsui H, Yamamoto M, Ichinose Y, et al. Salicylic acid-dependent immunity contributes to resistance against Rhizoctonia solani, a necrotrophic fungal agent of sheath blight, in rice and Brachypodium distachyon[J]. New Phytologist, 2017, 217(2): 771-783.
[24] Xue X, Cao Z X, Zhang X T, Wang Y, Zhang Y F, Chen Z X, Zuo S M. Overexpression of OsOSM1 enhances resistance to rice sheath blight[J]. Plant Disease, 2016, 100(8): 1634-1642.
[25] Zhang F, Zeng D, Zhang C S, Lu J L, Chen T J, Xie J P, Zhou Y L. Genome-wide association analysis of the genetic basis for sheath blight resistance in rice[J]. Rice, 2019, 12: 93.
[26] 薛芗, 冯志明, 曹文磊, 王雨, 陈宗祥, 马玉银, 张亚芳, 潘学彪, 左示敏. 乙烯信号参与调控水稻纹枯病抗性的研究[J]. 植物病理学报, 2020, 50(4): 462-470.
[26] Xue X, Feng Z M, Cao W L, Wang Y, Chen Z X, Ma Y Y, Zhang Y F, Pan X B, Zuo S M. A study on ethylene signaling involving in regulating resistance to rice sheath blight. Acta Phytopathologica Sinica, 2020, 50(4): 462-470. (in Chinese with English abstract)
[27] 左示敏, 薛芗, 张亚芳, 陈宗祥, 潘学彪. 细胞分裂素在调控水稻对纹枯病的抗性中的应用: ZL201610643969.X[P]. 2018.08.07.
[27] Zuo S M, Xue X, Zhang Y F, Chen Z X, Pan X B. Application of cytokinin in regulating rice resistance to sheath blight: ZL201610643969.X[P]. 2018.08.07.
[28] 左示敏, 章慧敏, 冯志明, 陈宗祥, 张亚芳. OsCKX7蛋白质及其编码基因在调控植物纹枯病抗性中的应用: CN201910071781.6[P]. 2019.01.25.
[28] Zuo S M, Zhang H M, Feng Z M, Chen Z X, Zhang Y F. Application of OsCKX7 in regulating rice resistance to sheath blight: CN201910071781.6[P]. 2019.01.25. (in Chinese)
[29] 贺闽, 尹俊杰, 冯志明, 朱孝波, 赵剑华, 左示敏, 陈学伟. 水稻稻瘟病和纹枯病抗性鉴定方法[J]. 植物学报, 2020, 55(5): 48-58.
[29] He M, Yin J J, Feng Z M, Zhu X B, Zhao J H, Zuo S M, Chen X W. Evaluation of rice resistance to blast disease and sheath blight disease[J]. Chinese Bulletin of Botany, 2020, 55(5): 48-58. (in Chinese with English abstract)
[30] De Vleesschauwer D, Yang Y, Cruz C V, Höfte M. Abscisic acid-induced resistance against the brown spot pathogen Cochliobolus miyabeanus in rice involves MAP kinase-mediated repression of ethylene signaling[J]. Plant Physiology, 2010, 152(4): 2036-2052.
[31] Takahashi H, Kanayama Y, Zheng MS, Kusano T, Hase S, Ikegami M, Shah J. Antagonistic interactions between the SA and JA signaling pathways in Arabidopsis modulate expression of defense genes and gene-for-gene resistance to cucumber mosaic virus[J]. Plant and Cell Physiology, 2004, 46(6): 803-809.
[32] Leon-Reyes A, Du Y J, Koomeef A, Proietti S, Körbes A P, Memelink J, Pieterse C M J. Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid[J]. Molecular Plant-Microbe Interactions, 2010, 23(2): 187-197.
[33] Shinshi H. Ethylene-regulated transcription and crosstalk with jasmonic acid[J]. Plant Science, 2008, 175(1): 18.
[34] Yang Y X, Ahammed G J, Wu C. Crosstalk among jasmonate, salicylate and ethylene signaling pathways in plant disease and immune responses[J]. Current Protein & Peptide Science, 2015, 16(5): 450-461.
[35] Tena G, Asai T, Chiu W L, Sheen J. Plant mitogen- activated protein kinase signaling cascades[J]. Current Opinion in Plant Biology, 2001, 4(5): 392-400.
[36] Yang Y X, Ahammed G, Wu C, Fan S Y, Zhou Y H. Crosstalk among jasmonate, salicylate and ethylene signaling pathways in plant disease and immune responses[J]. Current Protein and Peptide Science, 2015, 16(5): 450-461.
[37] Spoel S H, Johnson J S, Dong X. Regulation of tradeoffs between plant defenses against pathogens with different lifestyles[J]. Proceedings of the National Academy of Sciences of the USA, 2007, 104(47): 18842-18847.
[38] Bari R, Jones J D. Role of plant hormones in plant defence responses[J]. Plant Molecular Biology, 2009, 69(4): 473-488.
[39] Jung Y H, Rakwal R. Differential expression of defense/stress-related marker proteins in leaves of a unique rice blast lesion mimic mutant (blm)[J]. Journal of Proteome Research, 2006, 5(10): 2586-2598.
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