稻瘟病菌效应子研究进展

doi:10.16819/j.1001-7216.2025.240611

摘要/Abstract

摘要：

稻瘟病菌引起的稻瘟病是危害最严重的水稻病害之一。在侵染过程中，稻瘟病菌向水稻细胞释放大量效应子，改变水稻的生理状态和代谢，并抑制其免疫反应以促进侵染。深入了解稻瘟病菌效应子的特性及其与水稻之间的作用机制，可为稻瘟病的防治提供重要参考。本文综述了稻瘟病菌效应子分泌进入细胞的机制、效应子对稻瘟病抗性的复杂调控机制，以及效应子的分类等方面的研究进展。同时，讨论了当前稻瘟病菌效应子研究中存在的问题，并对未来的研究方向进行了展望，以期为稻瘟病的防治提供理论依据。

关键词: 水稻, 病害, 病原真菌, 稻瘟病, 效应子

Abstract:

Rice blast, caused by the fungal pathogen Magnaporthe oryzae, is among the most devastating rice diseases worldwide. During infection, M. oryzae deploys an arsenal of effectors into rice cells, altering their physiology and metabolism, and suppressing immune responses to facilitate colonization. A thorough understanding of M. oryzae effectors and their interaction mechanisms with rice holds significant potential to inform strategies for rice blast control. This review summarizes recent advances in elucidating the mechanisms of effector secretion into rice cells, the intricate regulatory mechanisms of effector-mediated rice blast resistance, and the classification of M. oryzae effectors. Additionally, it discusses the current challenges in effector research and outlines future research directions, aiming to provide a reference for the prevention and management of rice blast caused by M. oryzae.

Key words: rice, disease, pathogenic fungi, Magnaporthe oryzae, effector

卢椰子, 邱结华, 蒋楠, 寇艳君, 时焕斌. 稻瘟病菌效应子研究进展[J]. 中国水稻科学, 2025, 39(3): 287-294.

LU Yezi, QIU Jiehua, JIANG Nan, KOU Yanjun, SHI Huanbin. Research Progress in Effectors of Magnaporthe oryzae[J]. Chinese Journal OF Rice Science, 2025, 39(3): 287-294.

图/表 2

参考文献 57

[1]	Takeda T, Takahashi M, Shimizu M, Sugihara Y, Yamashita T, Saitoh H, Fujisaki K, Ishikawa K, Utsushi H, Kanzaki E, Sakamoto Y, Abe A, Terauchi R. Rice apoplastic CBM1-interacting protein counters blast pathogen invasion by binding conserved carbohydrate binding module 1 motif of fungal proteins[J]. PLoS Pathogens, 2022, 18(9): e1010792.
[2]	Hu J, Liu M, Zhang A, Dai Y, Chen W, Chen F, Wang W, Shen D, Telebanco-Yanoria M J, Ren B, Zhang H, Zhou H, Zhou B, Wang P, Zhang Z. Co-evolved plant and blast fungus ascorbate oxidases orchestrate the redox state of host apoplast to modulate rice immunity[J]. Molecular Plant, 2022, 15(8): 1347-1366.
[3]	Giraldo M C, Dagdas Y F, Gupta Y K, Mentlak T A, Yi M, Martinez-Rocha A L, Saitoh H, Terauchi R, Talbot N J, Valent B. Two distinct secretion systems facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae[J]. Nature Communications, 2013, 4: 1996.
[4]	Sha G, Sun P, Kong X, Han X, Sun Q, Fouillen L, Zhao J, Li Y, Yang L, Wang Y, Gong Q, Zhou Y, Zhou W, Jain R, Gao J, Huang R, Chen X, Zheng L, Zhang W, Qin Z, Zhou Q, Zeng Q, Xie K, Xu J, Chiu T Y, Guo L, Mortimer J C, Boutté Y, Li Q, Kang Z, Ronald P C, Li G. Genome editing of a rice CDP-DAG synthase confers multipathogen resistance[J]. Nature, 2023, 618(7967): 1017-1023
[5]	Delic M, Valli M, Graf A B, Pfeffer M, Mattanovich D, Gasser B. The secretory pathway: Exploring yeast diversity[J]. FEMS Microbiology Reviews, 2013, 37(6): 872-914.
[6]	Cohen M J, Chirico W J, Lipke P N. Through the back door: Unconventional protein secretion[J]. The Cell Surface, 2020, 6: 100045.
[7]	Chen X, Pan S, Bai H, Fan J, Batool W, Shabbir A, Han Y, Zheng H, Lu G, Lin L, Tang W, Wang Z. A nonclassically secreted effector of Magnaporthe oryzae targets host nuclei and plays important roles in fungal growth and plant infection[J]. Molecular Plant Pathology, 2023, 24(9): 1093-1106.
[8]	Fernandez J. The Phantom Menace: Latest findings on effector biology in the rice blast fungus[J]. aBIOTECH, 2023, 4(2): 140-154.
[9]	Ribot C, Césari S, Abidi I, Chalvon V, Bournaud C, Vallet J, Lebrun M H, Morel J B, Kroj T. The Magnaporthe oryzae effector AVR1-CO39 is translocated into rice cells independently of a fungal-derived machinery[J]. The Plant Journal, 2013, 74(1): 1-12.
[10]	Xiao G, Laksanavilat N, Cesari S, Lambou K, Baudin M, Jalilian A, Telebanco-Yanoria M J, Chalvon V, Meusnier I, Fournier E, Tharreau D, Zhou B, Wu J, Kroj T. The unconventional resistance protein PTR recognizes the Magnaporthe oryzae effector AVR-Pita in an allele-specific manner[J]. Nature Plants, 2024, 10(6): 994-1004.
[11]	Orbach M J, Farrall L, Sweigard J A, Chumley F G, Valent B. A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta[J]. The Plant Cell, 2000, 12(11): 2019-2032.
[12]	Vergne E, Ballini E, Marques S, Mammar B S, Droc G, Gaillard S, Bourot S, Derose R, Tharreau D, Notteghem J L, Lebrun M H, Morel J B. Early and specific gene expression triggered by rice resistance gene Pi33 in response to infection by ACE1 avirulent blast fungus[J]. New Phytologist, 2007, 174: 159-171.
[13]	Yoshida K, Saitoh H, Fujisawa S, Kanzaki H, Matsumura H, Yoshida K, Tosa Y, Chuma I, Takano Y, Win J, Kamoun S, Terauchi R. Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae[J]. The Plant Cell, 2009, 21(5): 1573-1591.
[14]	Ashikawa I, Hayashi N, Yamane H, Kanamori H, Wu J, Matsumoto T, Ono K, Yano M. Two adjacent nucleotide-binding site-leucine-rich repeat class genes are required to confer Pikm-specific rice blast resistance[J]. Genetics, 2008, 180(4): 2267-2276.
[15]	Yuan B, Zhai C, Wang W, Zeng X, Xu X, Hu H, Lin F, Wang L, Pan Q. The Pik-p resistance to Magnaporthe oryzae in rice is mediated by a pair of closely linked CC-NBS-LRR genes[J]. Theoretical and Applied Genetics, 2011, 122(5): 1017-1028.
[16]	Yang T, Song L, Hu J, Qiao L, Yu Q, Wang Z, Chen X, Lu G D. Magnaporthe oryzae effector AvrPik-D targets a transcription factor WG7 to suppress rice immunity[J]. Rice (N Y), 2024, 17: 14.
[17]	Li W, Wang B, Wu J, Lu G, Hu Y, Zhang X, Zhang Z, Zhao Q, Feng Q, Zhang H, Wang Z, Wang G, Han B, Wang Z, Zhou B. The Magnaporthe oryzae avirulence gene AvrPiz-t encodes a predicted secreted protein that triggers the immunity in rice mediated by the blast resistance gene Piz-t[J]. Molecular Plant-Microbe Interactions, 2009, 22(4): 411-420.
[18]	Wu J, Kou Y, Bao J, Li Y, Tang M, Zhu X, Ponaya A, Xiao G, Li J, Li C, Song M Y, Cumagun C J R, Deng Q, Lu G, Jeon J S, Naqvi N I, Zhou B. Comparative genomics identifies the Magnaporthe oryzae avirulence effector AvrPi9 that triggers Pi9-mediated blast resistance in rice[J]. New Phytologist, 2015, 206(4): 1463-1475.
[19]	Zhang S, Wang L, Wu W, He L, Yang X, Pan Q. Function and evolution of Magnaporthe oryzae avirulence gene AvrPib responding to the rice blast resistance gene Pib[J]. Scientific Reports, 2015, 5: 11642.
[20]	Damchuay K, Longya A, Sriwongchai T, Songkumarn P, Parinthawong N, Darwell K, Talumphai S, Tasanasuwan P, Jantasuriyarat C. High nucleotide sequence variation of avirulent gene, AVR-Pita1, in Thai rice blast fungus population[J]. Journal of Genetics, 2020, 99: 45.
[21]	Ray S, Singh P K, Gupta D K, Mahato A K, Sarkar C, Rathour R, Singh N K, Sharma T R. Analysis of Magnaporthe oryzae genome reveals a fungal effector, which is able to induce resistance response in transgenic rice line containing resistance gene, Pi54[J]. Frontiers in Plant Science, 2016, 7: 1140.
[22]	Chuma I, Isobe C, Hotta Y, Ibaragi K, Futamata N, Kusaba M, Yoshida K, Terauchi R, Fujita Y, Nakayashiki H, Valent B, Tosa Y. Multiple translocation of the AVR-Pita effector gene among chromosomes of the rice blast fungus Magnaporthe oryzae and related species[J]. PLoS Pathogens, 2011, 7(7): e1002147
[23]	Fujisaki K, Abe Y, Ito A, Saitoh H, Yoshida K, Kanzaki H, Kanzaki E, Utsushi H, Yamashita T, Kamoun S, Terauchi R. Rice Exo70 interacts with a fungal effector, AVR-Pii, and is required for AVR-Pii-triggered immunity[J]. The Plant Journal, 2015, 83(5): 875-887.
[24]	Han J, Wang X, Wang F, Zhao Z, Li G, Zhu X, Su J, Chen L. The fungal effector avr-pita suppresses innate immunity by increasing COX activity in rice mitochondria[J]. Rice, 2021, 14(1): 12.
[25]	Park C H, Chen S, Shirsekar G, Zhou B, Khang C H, Songkumarn P, Afzal A J, Ning Y, Wang R, Bellizzi M, Valent B, Wang G L. The Magnaporthe oryzae effector AvrPiz-t targets the RING E3 ubiquitin ligase APIP6 to suppress pathogen-associated molecular pattern-triggered immunity in rice[J]. The Plant Cell, 2012, 24(11): 4748-4762.
[26]	Singh R, Dangol S, Chen Y, Choi J, Cho Y S, Lee J E, Choi M O, Jwa N S. Magnaporthe oryzae effector AVR-pii helps to establish compatibility by inhibition of the rice NADP-malic enzyme resulting in disruption of oxidative burst and host innate immunity[J]. Molecules and Cells, 2016, 39(5): 426-438.
[27]	Zhang C, Fang H, Shi X, He F, Wang R, Fan J, Bai P, Wang J, Park C H, Bellizzi M, Zhou X, Wang G L, Ning Y. A fungal effector and a rice NLR protein have antagonistic effects on a Bowman-Birk trypsin inhibitor[J]. Plant Biotechnology Journal, 2020, 18(11): 2354-2363.
[28]	Zhang F, Fang H, Wang M, He F, Tao H, Wang R, Long J, Wang J, Wang G L, Ning Y. APIP5 functions as a transcription factor and an RNA-binding protein to modulate cell death and immunity in rice[J]. Nucleic Acids Research, 2022, 50(9): 5064-5079.
[29]	Park C H, Shirsekar G, Bellizzi M, Chen S, Songkumarn P, Xie X, Shi X, Ning Y, Zhou B, Suttiviriya P, Wang M, Umemura K, Wang G L. The E3 ligase APIP10 connects the effector AvrPiz-t to the NLR receptor piz-t in rice[J]. PLoS Pathogens, 2016, 12(3): e1005529.
[30]	Tang M, Ning Y, Shu X, Dong B, Zhang H, Wu D, Wang H, Wang G L, Zhou B. The Nup98 homolog APIP12 targeted by the effector AvrPiz-t is involved in rice basal resistance against Magnaporthe oryzae[J]. Rice, 2017, 10(1): 5.
[31]	Shi X, Long Y, He F, Zhang C, Wang R, Zhang T, Wu W, Hao Z, Wang Y, Wang G L, Ning Y. The fungal pathogen Magnaporthe oryzae suppresses innate immunity by modulating a host potassium channel[J]. PLoS Pathogens, 2018, 14(1): e1006878.
[32]	Gao M, He Y, Yin X, Zhong X, Yan B, Wu Y, Chen J, Li X, Zhai K, Huang Y, Gong X, Chang H, Xie S, Liu J, Yue J, Xu J, Zhang G, Deng Y, Wang E, Tharreau D, Wang G L, Yang W, He Z. Ca²⁺ sensor-mediated ROS scavenging suppresses rice immunity and is exploited by a fungal effector[J]. Cell, 2021, 184(21): 5391-5404.e17.
[33]	Zhai K, Liang D, Li H, Jiao F, Yan B, Liu J, Lei Z, Huang L, Gong X, Wang X, Miao J, Wang Y, Liu J Y, Zhang L, Wang E, Deng Y, Wen C K, Guo H, Han B, He Z. NLRs guard metabolism to coordinate pattern- and effector-triggered immunity[J]. Nature, 2022, 601(7892): 245-251.
[34]	de la Concepcion J C, Langner T, Fujisaki K, Yan X, Were V, Lam A H C, Saado I, Brabham H J, Win J, Yoshida K, Talbot N J, Terauchi R, Kamoun S, Banfield M J. Zinc-finger (ZiF) fold secreted effectors form a functionally diverse family across lineages of the blast fungus Magnaporthe oryzae[J]. PLoS Pathogens, 2024, 20(6): e1012277.
[35]	Liu Z, Qiu J, Shen Z, Wang C, Jiang N, Shi H, Kou Y. The E3 ubiquitin ligase OsRGLG5 targeted by the Magnaporthe oryzae effector AvrPi9 confers basal resistance against rice blast[J]. Plant Communications, 2023, 4(5): 100626.
[36]	Shi X, Xiong Y, Zhang K, Zhang Y, Zhang J, Zhang L, Xiao Y, Wang G L, Liu W. The ANIP1-OsWRKY62 module regulates both basal defense and Pi9-mediated immunity against Magnaporthe oryzae in rice[J]. Molecular Plant, 2023, 16(4): 739-755.
[37]	Liu M, Wang F, He B, Hu J, Dai Y, Chen W, Yi M, Zhang H, Ye Y, Cui Z, Zheng X, Wang P, Xing W, Zhang Z. Targeting Magnaporthe oryzae effector MoErs1 and host papain-like protease OsRD21 interaction to combat rice blast[J]. Nature Plants, 2024, 10(4): 618-632.
[38]	Mosquera G, Giraldo M C, Khang C H, Coughlan S, Valent B. Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1-4 as Biotrophy-associated secreted proteins in rice blast disease[J]. The Plant Cell, 2009, 21(4): 1273-1290.
[39]	Lee S, Völz R, Lim Y J, Harris W, Kim S, Lee Y H. The nuclear effector MoHTR3 of Magnaporthe oryzae modulates host defence signalling in the biotrophic stage of rice infection[J]. Molecular Plant Pathology, 2023, 24(6): 602-615.
[40]	Zhu Z, Xiong J, Shi H, Liu Y, Yin J, He K, Zhou T, Xu L, Zhu X, Lu X, Tang Y, Song L, Hou Q, Xiong Q, Wang L, Ye D, Qi T, Zou L, Li G, Sun C, Wu Z, Li P, Liu J, Bi Y, Yang Y, Jiang C, Fan J, Gong G, He M, Wang J, Chen X, Li W. Magnaporthe oryzae effector MoSPAB1 directly activates rice Bsr-d1 expression to facilitate pathogenesis[J]. Nature Communications, 2023, 14(1): 8399.
[41]	Shi X, Xie X, Guo Y, Zhang J, Gong Z, Zhang K, Mei J, Xia X, Xia H, Ning N, Xiao Y, Yang Q, Wang G L, Liu W. A fungal core effector exploits the OsPUX8B. 2-OsCDC48-6 module to suppress plant immunity[J]. Nature Communications, 2024, 15(1): 2559.
[42]	Oliveira-Garcia E, Tamang T M, Park J, Dalby M, Martin-Urdiroz M, Rodriguez Herrero C, Vu A H, Park S, Talbot N J, Valent B. Clathrin-mediated endocytosis facilitates the internalization of Magnaporthe oryzae effectors into rice cells[J]. The Plant Cell, 2023, 35(7): 2527-2551.
[43]	Khang C H, Berruyer R, Giraldo M C, Kankanala P, Park S Y, Czymmek K, Kang S, Valent B. Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement[J]. The Plant Cell, 2010, 22(4) :1388-1403.
[44]	Kim S, Kim C Y, Park S Y, Kim K T, Jeon J, Chung H, Choi G, Kwon S, Choi J, Jeon J, Jeon J S, Khang C H, Kang S, Lee Y H. Two nuclear effectors of the rice blast fungus modulate host immunity via transcriptional reprogramming[J]. Nature Communications, 2020, 11: 5845.
[45]	Liu X, Gao Y, Guo Z, Wang N, Wegner A, Wang J, Zou X, Hu J, Liu M, Zhang H, Zheng X, Wang P, Schaffrath U, Zhang Z. MoIug4 is a novel secreted effector promoting rice blast by counteracting host OsAHL1-regulated ethylene gene transcription[J]. New Phytologist, 2022, 235(3): 1163-1178.
[46]	Ning N, Xie X, Yu H, Mei J, Li Q, Zuo S, Wu H, Liu W, Li Z. Plant peroxisome-targeting effector MoPtep1 is required for the virulence of Magnaporthe oryzae[J]. International Journal of Molecular Sciences, 2022, 23(5): 2515.
[47]	Xu G, Zhong X, Shi Y, Liu Z, Jiang N, Liu J, Ding B, Li Z, Kang H, Ning Y, Liu W, Guo Z, Wang G L, Wang X. A fungal effector targets a heat shock-dynamin protein complex to modulate mitochondrial dynamics and reduce plant immunity[J]. Science Advances, 2020, 6(48): eabb7719.
[48]	Dong Y, Li Y, Zhao M, Jing M, Liu X, Liu M, Guo X, Zhang X, Chen Y, Liu Y, Liu Y, Ye W, Zhang H, Wang Y, Zheng X, Wang P, Zhang Z. Global genome and transcriptome analyses of Magnaporthe oryzae epidemic isolate 98-06 uncover novel effectors and pathogenicity -related genes, revealing gene gain and lose dynamics in genome evolution[J]. Plos Pathogens, 2015, 11(4): e1004801.
[49]	Yang C, Liu R, Pang J, Ren B, Zhou H, Wang G, Wang E, Liu J. Poaceae-specific cell wall-derived oligosaccharides activate plant immunity via OsCERK1 during Magnaporthe oryzae infection in rice[J]. Nature Communications, 2021, 12(1): 2178.
[50]	Yang C, Yu Y, Huang J, Meng F, Pang J, Zhao Q, Islam M A, Xu N, Tian Y, Liu J. Binding of the Magnaporthe oryzae chitinase MoChia1 by a rice tetratricopeptide repeat protein allows free chitin to trigger immune responses[J]. The Plant Cell, 2019, 31(1): 172-188.
[51]	Han Y, Song L, Peng C, Liu X, Liu L, Zhang Y, Wang W, Zhou J, Wang S, Ebbole D, Wang Z, Lu G D. A Magnaporthe oryzae chitinase interacts with a rice jacalin-related lectin to promote host colonization[J]. Plant Physiology, 2019, 179(4): 1416-1430.
[52]	Liu H, Lu X, Li M, Lun Z, Yan X, Yin C, Yuan G, Wang X, Liu N, Liu D, Wu M, Luo Z, Zhang Y, Bhadauria V, Yang J, Talbot N J, Peng Y L. Plant immunity suppression by an exo-β-1,3-glucanase and an elongation factor 1a of the rice blast fungus[J]. Nature Communications, 2023, 14(1): 5491.
[53]	Yang J, Liu L, Wang Y, Wang C, Yan J, Liu Y, Wang C, Li C. Overexpression of BAS1 in rice blast fungus can promote blast fungus growth, sporulation and virulence in planta[J]. Saudi Journal of Biological Sciences, 2017, 24(8): 1884-1893.
[54]	Kang S C, Sweigard J A, Valent B. The PWL host specificity gene family in the blast fungus Magnaporthe grisea[J]. Molecular Plant-Microbe Interactions, 1995, 8(6): 939-948.
[55]	Brabham H J, Gomez De La Cruz D, Were V, Shimizu M, Saitoh H, Hernandez-Pinzon I, Green P, Lorang J, Fujisaki K, Sato K, Molnar I, Simkova H, Dolezel J, Russell J, Taylor J, Smoker M, Gupta Y K, Wolpert T, Talbot N J, Terauchi R, Moscou M J. Barley MLA3 recognizes the host-specificity effector Pwl2 from Magnaporthe oryzae[J]. The Plant Cell, 2024, 36(2): 447-470.
[56]	Mentlak T A, Kombrink A, Shinya T, Ryder L S, Otomo I, Saitoh H, Terauchi R, Nishizawa Y, Shibuya N, Thomma B P H J, Talbot N J. Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease[J]. The Plant Cell, 2012, 24(1): 322-335.
[57]	Li Y, Liu X, Liu M, Wang Y, Zou Y, You Y, Yang L, Hu J, Zhang H, Zheng X, Wang P, Zhang Z. Magnaporthe oryzae auxiliary activity protein MoAa91 functions as chitin-binding protein to induce appressorium formation on artificial inductive surfaces and suppress plant immunity[J]. mBio, 2020, 11(2): e03304-19.

无毒基因 Avirulence gene	对应R基因 Corresponding R gene	蛋白结构域 Protein domain	编码分泌蛋白 Encoding secretory proteins	参考文献 Reference
Avr-CO39	CO39	未鉴定出已知结构域 No known domains detected	是Yes	[9]
Avr-Pita	Ptr	含金属蛋白酶结构域，作用于宿主细胞质Harbors a metalloprotease domain acting on the host cell cytoplasm	是Yes	[10,11]
ACE1	Pi-33	编码一个非核糖体多聚乙酰合酶 Encodes a nonribosomal polyketide synthase	否 No	[12]
Avr-Pia	Pia	未鉴定出已知结构域 No known domains detected	是Yes	[13]
Avr-Pii	Pii	未鉴定出已知结构域 No known domains detected	是Yes	[13]
Avr-Pik	Pik	未鉴定出已知结构域 No known domains detected	是Yes	[13]
Avr-Pikm	Pikm	未鉴定出已知结构域 No known domains detected	是Yes	[14]
Avr-Pikp	Pikp	未鉴定出已知结构域 No known domains detected	是Yes	[15]
AvrPik-D	Pik-h	未鉴定出已知结构域 No known domains detected	是Yes	[16]
Avr-Piz-t	Piz-t	未鉴定出已知结构域 No known domains detected	是Yes	[17]
Avr-Pi9	Pi9	未鉴定出已知结构域 No known domains detected	是Yes	[18]
Avr-Pib	Pib	未鉴定出已知结构域 No known domains detected	是Yes	[19]
Avr-Pita1	Pita1	未鉴定出已知结构域 No known domains detected	是Yes	[20]
Avr-Pi54	Pi54	未鉴定出已知结构域 No known domains detected	是Yes	[21]

无毒基因 Avirulence gene	对应R基因 Corresponding R gene	蛋白结构域 Protein domain	编码分泌蛋白 Encoding secretory proteins	参考文献 Reference
Avr-CO39	CO39	未鉴定出已知结构域 No known domains detected	是Yes	[9]
Avr-Pita	Ptr	含金属蛋白酶结构域，作用于宿主细胞质Harbors a metalloprotease domain acting on the host cell cytoplasm	是Yes	[10,11]
ACE1	Pi-33	编码一个非核糖体多聚乙酰合酶 Encodes a nonribosomal polyketide synthase	否 No	[12]
Avr-Pia	Pia	未鉴定出已知结构域 No known domains detected	是Yes	[13]
Avr-Pii	Pii	未鉴定出已知结构域 No known domains detected	是Yes	[13]
Avr-Pik	Pik	未鉴定出已知结构域 No known domains detected	是Yes	[13]
Avr-Pikm	Pikm	未鉴定出已知结构域 No known domains detected	是Yes	[14]
Avr-Pikp	Pikp	未鉴定出已知结构域 No known domains detected	是Yes	[15]
AvrPik-D	Pik-h	未鉴定出已知结构域 No known domains detected	是Yes	[16]
Avr-Piz-t	Piz-t	未鉴定出已知结构域 No known domains detected	是Yes	[17]
Avr-Pi9	Pi9	未鉴定出已知结构域 No known domains detected	是Yes	[18]
Avr-Pib	Pib	未鉴定出已知结构域 No known domains detected	是Yes	[19]
Avr-Pita1	Pita1	未鉴定出已知结构域 No known domains detected	是Yes	[20]
Avr-Pi54	Pi54	未鉴定出已知结构域 No known domains detected	是Yes	[21]

效应子类型 Types of effector	效应子 Effector	对应的水稻靶标蛋白 Corresponding rice target protein	作用方式 Mechanism of action	参考文献 Reference
胞质效应子 Cytoplasmic effectors	Avr-Pita	Ptr	水稻抗性蛋白Ptr以等位基因特异性方式检测到AVR-Pita，它的不同等位基因赋予水稻特异的Pi-ta或Pi-ta2稻瘟病抗性	[10]
	Avr-Pita	OsCOX11	Avr-Pita干扰细胞色素c氧化酶组装的关键蛋白OsCOX11，降低ROS水平，进而降低水稻抗性	[24]
	AvrPiz-t	Piz-t	AvrPiz-t被R蛋白Piz-t间接识别，启动Piz-t基因介导的抗病反应	[27]
		APIP4	AvrPiz-t与APIP4相互作用，抑制其胰蛋白酶抑制剂功能，调控水稻对稻瘟病的基础抗性	[28]
		APIP5	AvrPiz-t作用于水稻蛋白APIP5，调节水稻细胞死亡和免疫	[28]
		APIP6	AvrPiz-t作用于RING E3泛素连接酶APIP6，减弱水稻的基础抗性	[25]
		APIP10	AvrPiz-t促使E3连接酶APIP10降解，减弱基础抗性，同时增强Piz-t介导的抗性	[29]
		APIP12	AvrPiz-t影响核孔蛋白APIP12，调控水稻对稻瘟病的基础抗性	[30]
		OsAKT1	AvrPiz-t针对钾通道蛋白OsAKT1，影响钾的流动并降低植物的基础抗性	[31]
	AvrPi9	Pi9	AvrPi9被Pi9识别后，激活Pi9介导的抗性	[18]
		PICI1	AvrPi9靶向去泛素化酶PICI1使其降解，从而减弱水稻的基础抗性	[33]
		OsRGLG5	AvrPi9降低E3泛素连接酶OsRGLG5的稳定性，从而减弱水稻的基础抗性	[35]
		ANIP1-OsWRKY62	AvrPi9与ANIP1-OsWRKY62互作，调控水稻的基础抗性及Pi9介导的抗性	[36]
	Avr-Pii	Pii	Avr-Pii被R蛋白Pii识别后，能激发Pii介导的抗病反应	[38]
		NADP-ME2	Avr-Pii作用于NADP-丙酮酸脱氢酶NADP-ME，减少ROS迸发，进而降低基础抗性	[23]
		OsExo70	进而调控基础抗性	[23]
	MoHTR1-3	-	核效应蛋白MoHTR1-3通过降低防御相关基因的表达，抑制宿主的免疫反应	[39]
	MoIug4	OsAHL1	MoIug4通过干扰转录激活因子OsAHL1，减少乙烯信号通路中关键成员OsEIN2和防御相关基因的表达	[45]
	Bas170	-	Bas170不仅能在BIC的动态囊状膜效应区MEC的点状结构积累，还能进入水稻细胞核，但是其具体功能目前并不清楚	[42]
	MoCDIP4	OsDjA9	MoCDIP4与线粒体相关的OsDjA9结合，干扰OsDRP1E的功能，导致线粒体缩短，降低水稻抗性	[47]
	Bas1	-	在稻瘟病菌中过表达 BAS1可促进稻瘟病菌在植物中的生长、产孢，增强其毒力	[53]
	Bas2	-	Bas2是一种小的富含Cys的分泌蛋白，主要定位于BIC位点	[38]
	Bas3	-	Bas3可能在侵染菌丝穿透水稻细胞壁的过程中发挥一定的作用	[38]
	Bas83	-	Bas83可能参与募集水稻质膜以帮助BIC效应子进入水稻细胞	[42]
	Iug9	-	在水稻中表达Iug6和Iug9导致水稻防御相关基因表达受到抑制	[42]
	Pwl1		Pwl1是Pwl2的同源基因，调控稻瘟病菌寄主专化性，阻止其侵染弯叶画眉草	[54]
	Pwl2		Pwl2是稻瘟病菌寄主决定因子，调控其寄主专化性，可被大麦NLR免疫受体MLA3识别	[55]
	Pwl3		不参与寄主专化性调控
	Pwl4	-	不参与寄主专化性调控
	MoNLE1	OsPUX8B.2	MoNLE1是通过特异性干扰OsPUX8B.2来抑制水稻免疫的核毒力因子	[41]
	MoErs1	OsRD21	MoErs1通过抑制水稻半胱氨酸蛋白酶OsRD21来参与水稻免疫，破坏MoErs1-OsRD21互作能够有效地控制稻瘟病	[37]
质外体效应子 Apoplastic effectors	MoSlp1	-	MoSlp1与几丁质结合蛋白OsCEBiP竞争性结合几丁质寡糖，干扰几丁质触发的免疫反应	[56]
	MoAa91	-	MoAa91与OsCEBiP竞争性结合几丁质，削弱几丁质触发的免疫反应	[57]
	MoChia1	OsTPR1	水稻中的三肽重复蛋白OsTPR1通过与几丁质酶MoChia1进行竞争性结合，导致游离几丁质积累，进而引发植物免疫反应	[50]
	MoCel12A/12B	-	糖苷水解酶家族GH12中的内切酶MoCel12A/12B破坏植物细胞壁来释放损伤相关分子模式，进而激活植物免疫反应	[49]
	MoCel10A	OsRMC	受体激酶OsRMC抑制木聚糖酶MoCel10A对水稻木聚糖的降解，进而干扰稻瘟病菌的侵染	[1]
	MoEbg1	-	Ebg1蛋白抑制β-1,3-葡聚糖激发的免疫反应	[52]
	MoAo1	OsAO3/ OsAO4	MoAo1通过抑制水稻中的抗坏血酸氧化酶OsAO3和OsAO4的活性，进而调控细胞外基质的氧化还原状态，以削弱水稻的免疫反应	[2]
	Bas4	-	Bas4参与水稻稻瘟病菌从活体营养阶段向死体营养阶段的转变，并改变水稻的防御机制。	[38]
	Bas113	-	稻瘟病菌细胞壁与寄主包膜之间的交界面菌丝膜(EIHM)的主要组成部分	[3]

效应子类型 Types of effector	效应子 Effector	对应的水稻靶标蛋白 Corresponding rice target protein	作用方式 Mechanism of action	参考文献 Reference
胞质效应子 Cytoplasmic effectors	Avr-Pita	Ptr	水稻抗性蛋白Ptr以等位基因特异性方式检测到AVR-Pita，它的不同等位基因赋予水稻特异的Pi-ta或Pi-ta2稻瘟病抗性	[10]
	Avr-Pita	OsCOX11	Avr-Pita干扰细胞色素c氧化酶组装的关键蛋白OsCOX11，降低ROS水平，进而降低水稻抗性	[24]
	AvrPiz-t	Piz-t	AvrPiz-t被R蛋白Piz-t间接识别，启动Piz-t基因介导的抗病反应	[27]
		APIP4	AvrPiz-t与APIP4相互作用，抑制其胰蛋白酶抑制剂功能，调控水稻对稻瘟病的基础抗性	[28]
		APIP5	AvrPiz-t作用于水稻蛋白APIP5，调节水稻细胞死亡和免疫	[28]
		APIP6	AvrPiz-t作用于RING E3泛素连接酶APIP6，减弱水稻的基础抗性	[25]
		APIP10	AvrPiz-t促使E3连接酶APIP10降解，减弱基础抗性，同时增强Piz-t介导的抗性	[29]
		APIP12	AvrPiz-t影响核孔蛋白APIP12，调控水稻对稻瘟病的基础抗性	[30]
		OsAKT1	AvrPiz-t针对钾通道蛋白OsAKT1，影响钾的流动并降低植物的基础抗性	[31]
	AvrPi9	Pi9	AvrPi9被Pi9识别后，激活Pi9介导的抗性	[18]
		PICI1	AvrPi9靶向去泛素化酶PICI1使其降解，从而减弱水稻的基础抗性	[33]
		OsRGLG5	AvrPi9降低E3泛素连接酶OsRGLG5的稳定性，从而减弱水稻的基础抗性	[35]
		ANIP1-OsWRKY62	AvrPi9与ANIP1-OsWRKY62互作，调控水稻的基础抗性及Pi9介导的抗性	[36]
	Avr-Pii	Pii	Avr-Pii被R蛋白Pii识别后，能激发Pii介导的抗病反应	[38]
		NADP-ME2	Avr-Pii作用于NADP-丙酮酸脱氢酶NADP-ME，减少ROS迸发，进而降低基础抗性	[23]
		OsExo70	进而调控基础抗性	[23]
	MoHTR1-3	-	核效应蛋白MoHTR1-3通过降低防御相关基因的表达，抑制宿主的免疫反应	[39]
	MoIug4	OsAHL1	MoIug4通过干扰转录激活因子OsAHL1，减少乙烯信号通路中关键成员OsEIN2和防御相关基因的表达	[45]
	Bas170	-	Bas170不仅能在BIC的动态囊状膜效应区MEC的点状结构积累，还能进入水稻细胞核，但是其具体功能目前并不清楚	[42]
	MoCDIP4	OsDjA9	MoCDIP4与线粒体相关的OsDjA9结合，干扰OsDRP1E的功能，导致线粒体缩短，降低水稻抗性	[47]
	Bas1	-	在稻瘟病菌中过表达 BAS1可促进稻瘟病菌在植物中的生长、产孢，增强其毒力	[53]
	Bas2	-	Bas2是一种小的富含Cys的分泌蛋白，主要定位于BIC位点	[38]
	Bas3	-	Bas3可能在侵染菌丝穿透水稻细胞壁的过程中发挥一定的作用	[38]
	Bas83	-	Bas83可能参与募集水稻质膜以帮助BIC效应子进入水稻细胞	[42]
	Iug9	-	在水稻中表达Iug6和Iug9导致水稻防御相关基因表达受到抑制	[42]
	Pwl1		Pwl1是Pwl2的同源基因，调控稻瘟病菌寄主专化性，阻止其侵染弯叶画眉草	[54]
	Pwl2		Pwl2是稻瘟病菌寄主决定因子，调控其寄主专化性，可被大麦NLR免疫受体MLA3识别	[55]
	Pwl3		不参与寄主专化性调控
	Pwl4	-	不参与寄主专化性调控
	MoNLE1	OsPUX8B.2	MoNLE1是通过特异性干扰OsPUX8B.2来抑制水稻免疫的核毒力因子	[41]
	MoErs1	OsRD21	MoErs1通过抑制水稻半胱氨酸蛋白酶OsRD21来参与水稻免疫，破坏MoErs1-OsRD21互作能够有效地控制稻瘟病	[37]
质外体效应子 Apoplastic effectors	MoSlp1	-	MoSlp1与几丁质结合蛋白OsCEBiP竞争性结合几丁质寡糖，干扰几丁质触发的免疫反应	[56]
	MoAa91	-	MoAa91与OsCEBiP竞争性结合几丁质，削弱几丁质触发的免疫反应	[57]
	MoChia1	OsTPR1	水稻中的三肽重复蛋白OsTPR1通过与几丁质酶MoChia1进行竞争性结合，导致游离几丁质积累，进而引发植物免疫反应	[50]
	MoCel12A/12B	-	糖苷水解酶家族GH12中的内切酶MoCel12A/12B破坏植物细胞壁来释放损伤相关分子模式，进而激活植物免疫反应	[49]
	MoCel10A	OsRMC	受体激酶OsRMC抑制木聚糖酶MoCel10A对水稻木聚糖的降解，进而干扰稻瘟病菌的侵染	[1]
	MoEbg1	-	Ebg1蛋白抑制β-1,3-葡聚糖激发的免疫反应	[52]
	MoAo1	OsAO3/ OsAO4	MoAo1通过抑制水稻中的抗坏血酸氧化酶OsAO3和OsAO4的活性，进而调控细胞外基质的氧化还原状态，以削弱水稻的免疫反应	[2]
	Bas4	-	Bas4参与水稻稻瘟病菌从活体营养阶段向死体营养阶段的转变，并改变水稻的防御机制。	[38]
	Bas113	-	稻瘟病菌细胞壁与寄主包膜之间的交界面菌丝膜(EIHM)的主要组成部分	[3]