青枯菌Ⅲ型效应蛋白与宿主蛋白相互作用研究进展

doi:10.16178/j.issn.0528-9017.20250344

摘要/Abstract

摘要：

青枯病(bacterial wilt)是由青枯雷尔氏菌(Ralstonia solanacearum)引发的细菌性病害,主要侵染植株的根、茎、叶,且寄主范围、分布范围极广,是一种毁灭性的植物土传病害。研究表明,青枯菌通过Ⅲ型分泌系统(type Ⅲ secretion system,T3SS)将大量的Ⅲ型效应蛋白(type Ⅲ effectors,T3Es)直接运输到宿主细胞内,以此来干扰寄主的免疫反应。T3Es能够靶向寄主免疫相关蛋白来影响植物代谢及激素信号转导通路,在抑制宿主免疫反应的过程中发挥重要作用。本文总结了青枯菌T3Es与宿主蛋白的相互作用及其机制,为探索青枯菌的致病机制及防治青枯病提供了有效参考。

关键词: 青枯病, 青枯雷尔氏菌, 效应蛋白, 宿主蛋白, 蛋白互作

Abstract:

Bacterial wilt, caused by Ralstonia solanacearum, is a destructive soilborne disease affecting roots, stems, and leaves of a broad host range. R. solanacearum employs a type Ⅲ secretion system (T3SS) to deliver numerous type Ⅲ effectors (T3Es) directly into host cells, thereby subverting plant immunity. These T3Es target host immune-related proteins, modulating plant metabolism and hormone signaling pathways, and thereby play a crucial role in suppressing host immune responses. This review summarized the interactions and mechanisms of R. solanacearum T3Es with host proteins, providing a valuable reference for exploring the bacterial pathogenicity mechanisms and control of bacterial wilt disease.

Key words: bacterial wilt, Ralstonia solanacearum, effector proteins, host proteins, protein-protein interactions

中图分类号:

S432.2

王梅芳, 席超越, 朱海生, 陈丽妃. 青枯菌Ⅲ型效应蛋白与宿主蛋白相互作用研究进展[J]. 浙江农业科学, 2025, 66(9): 2200-2207.

WANG Meifang, XI Chaoyue, ZHU Haisheng, CHEN Lifei. Research progress on the interactions of Ralstonia solanacearum type Ⅲ effector proteins and host proteins[J]. Journal of Zhejiang Agricultural Sciences, 2025, 66(9): 2200-2207.

图/表 2

参考文献 70

[1]	MANSFIELD J, GENIN S, MAGORI S, et al. Top 10 plant pathogenic bacteria in molecular plant pathology[J]. Molecular Plant Pathology, 2012, 13(6): 614-629.
[2]	VASSE J. Microscopic studies of intercellular infection and protoxylem invasion of tomato roots by Pseudomonas solanacearum[J]. Molecular Plant-Microbe Interactions, 1995, 8(2): 241.
[3]	JIANG G F, WEI Z, XU J, et al. Bacterial wilt in China: history, current status, and future perspectives[J]. Frontiers in Plant Science, 2017, 8: 1549.
[4]	GALÁN J E, LARA-TEJERO M, MARLOVITS T C, et al. Bacterial type Ⅲ secretion systems: specialized nanomachines for protein delivery into target cells[J]. Annual Review of Microbiology, 2014, 68: 415-438.
[5]	HAYWARD A C. Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum[J]. Annual Review of Phytopathology, 1991, 29: 65-87.
[6]	JONES J D G, VANCE R E, DANGL J L. Intracellular innate immune surveillance devices in plants and animals[J]. Science, 2016, 354(6316): aaf6395.
[7]	DESLANDES L, GENIN S. Opening the Ralstonia solanacearum type Ⅲ effector tool box: insights into host cell subversion mechanisms[J]. Current Opinion in Plant Biology, 2014, 20: 110-117.
[8]	MILETIC S, FAHRENKAMP D, GOESSWEINER-MOHR N, et al. Substrate-engaged type Ⅲ secretion system structures reveal gating mechanism for unfolded protein translocation[J]. Nature Communications, 2021, 12(1): 1546.
[9]	WICKER E, LEFEUVRE P, DE CAMBIAIRE J C, et al. Contrasting recombination patterns and demographic histories of the plant pathogen Ralstonia solanacearum inferred from MLSA[J]. The ISME Journal, 2012, 6(5): 961-974.
[10]	GENIN S, DENNY T P. Pathogenomics of the Ralstonia solanacearum species complex[J]. Annual Review of Phytopathology, 2012, 50: 67-89.
[11]	LANDRY D, GONZÁLEZ-FUENTE M, DESLANDES L, et al. The large, diverse, and robust arsenal of Ralstonia solanacearum type Ⅲ effectors and their in planta functions[J]. Molecular Plant Pathology, 2020, 21(10): 1377-1388.
[12]	PEETERS N, CARRÈRE S, ANISIMOVA M, et al. Repertoire, unified nomenclature and evolution of the Type Ⅲ effector gene set in the Ralstonia solanacearum species complex[J]. BMC Genomics, 2013, 14: 85.
[13]	KOBE B, KAJAVA A V. The leucine-rich repeat as a protein recognition motif[J]. Current Opinion in Structural Biology, 2001, 11(6): 725-732.
[14]	YU G, XIAN L, XUE H, et al. A bacterial effector protein prevents MAPK-mediated phosphorylation of SGT1 to suppress plant immunity[J]. PLoS Pathogens, 2020, 16(9): e1008933.
[15]	SHIRASU K. The HSP90-SGT1 chaperone complex for NLR immune sensors[J]. Annual Review of Plant Biology, 2009, 60: 139-164.
[16]	BOTËR M, AMIGUES B, PEART J, et al. Structural and functional analysis of SGT1 reveals that its interaction with HSP90 is required for the accumulation of Rx, an R protein involved in plant immunity[J]. The Plant Cell, 2007, 19(11): 3791-3804.
[17]	CUI H T, TSUDA K, PARKER J E. Effector-triggered immunity: from pathogen perception to robust defense[J]. Annual Review of Plant Biology, 2015, 66: 487-511.
[18]	HOLT B F 3rd, BELKHADIR Y, DANGL J L. Antagonistic control of disease resistance protein stability in the plant immune system[J]. Science, 2005, 309(5736): 929-932.
[19]	AZEVEDO C, BETSUYAKU S, PEART J, et al. Role of SGT1 in resistance protein accumulation in plant immunity[J]. EMBO Journal, 2006, 25(9): 2007-2016.
[20]	NAKANO M, ICHINOSE Y, MUKAIHARA T. Ralstonia solanacearum type Ⅲ effector RipAC targets SGT1 to suppress effector-triggered immunity[J]. Plant & Cell Physiology, 2021, 61(12): 2067-2076.
[21]	NOËL L D, CAGNA G, STUTTMANN J, et al. Interaction between SGT1 and cytosolic/nuclear HSC70 chaperones regulates Arabidopsis immune responses[J]. The Plant Cell, 2007, 19(12): 4061-4076.
[22]	NOCTOR G, MHAMDI A, CHAOUCH S, et al. Glutathione in plants: an integrated overview[J]. Plant, Cell & Environment, 2012, 35(2): 454-484.
[23]	FRENDO P, BALDACCI-CRESP F, BENYAMINA S M, et al. Glutathione and plant response to the biotic environment[J]. Free Radical Biology and Medicine, 2013, 65: 724-730.
[24]	GHANTA S, CHATTOPADHYAY S. Glutathione as a signaling molecule: another challenge to pathogens[J]. Plant Signaling & Behavior, 2011, 6(6): 783-788.
[25]	SANG Y Y, WANG Y R, NI H, et al. The Ralstonia solanacearum type Ⅲ effector RipAY targets plant redox regulators to suppress immune responses[J]. Molecular Plant Pathology, 2018, 19(1): 129-142.
[26]	MUKAIHARA T, HATANAKA T, NAKANO M, et al. Ralstonia solanacearum type Ⅲ effector RipAY is a glutathione-degrading enzyme that is activated by plant cytosolic thioredoxins and suppresses plant immunity[J]. mBio, 2016, 7(2): e00359-16.
[27]	SAITOH M, NISHITOH H, FUJII M, et al. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1[J]. EMBO Journal, 1998, 17(9): 2596-2606.
[28]	WANG B S, HE T J, ZHENG X A, et al. Proteomic analysis of potato responding to the invasion of Ralstonia solanacearum UW551 and its type Ⅲ secretion system mutant[J]. Molecular Plant-Microbe Interactions^®, 2021, 34(4): 337-350.
[29]	BRADAI M, MAHJOUBI H, CHINI A, et al. Genome wide identification of wheat and Brachypodium type one protein phosphatases and functional characterization of durum wheat TdPP1a[J]. PLoS One, 2018, 13(1): e0191272.
[30]	BHERI M, MAHIWAL S, SANYAL S K, et al. Plant protein phosphatases: What do we know about their mechanism of action?[J]. The FEBS Journal, 2021, 288(3): 756-785.
[31]	MOORHEAD G B G, DE WEVER V, TEMPLETON G, et al. Evolution of protein phosphatases in plants and animals[J]. Biochemical Journal, 2009, 417(2): 401-409.
[32]	CEULEMANS H, BOLLEN M. Functional diversity of protein phosphatase-1, a cellular economizer and reset button[J]. Physiological Reviews, 2004, 84(1): 1-39.
[33]	HOU Y J, ZHU Y F, WANG P C, et al. Type one protein phosphatase 1 and its regulatory protein inhibitor 2 negatively regulate ABA signaling[J]. PLoS Genetics, 2016, 12(3): e1005835.
[34]	WANG B S, HE W F, HUANG M S, et al. Ralstonia solanacearum type Ⅲ effector RipAS associates with potato type one protein phosphatase StTOPP6 to promote bacterial wilt[J]. Horticulture Research, 2023, 10(6): uhad087.
[35]	BOLLEN M, PETI W, RAGUSA M J, et al. The extended PP1 toolkit: designed to create specificity[J]. Trends in Biochemical Sciences, 2010, 35(8): 450-458.
[36]	PETI W, NAIRN A C, PAGE R. Structural basis for protein phosphatase 1 regulation and specificity[J]. The FEBS Journal, 2013, 280(2): 596-611.
[37]	COHEN P T W. Protein phosphatase 1: targeted in many directions[J]. Journal of Cell Science, 2002, 115(Pt 2): 241-256.
[38]	HENDRICKX A, BEULLENS M, CEULEMANS H, et al. Docking motif-guided mapping of the interactome of protein phosphatase-1[J]. Chemistry & Biology, 2009, 16(4): 365-371.
[39]	WANG Y R, ZHAO A C, MORCILLO R J L, et al. A bacterial effector protein uncovers a plant metabolic pathway involved in tolerance to bacterial wilt disease[J]. Molecular Plant, 2021, 14(8): 1281-1296.
[40]	SUN Y H, LI P, DENG M Y, et al. The Ralstonia solanacearum effector RipAK suppresses plant hypersensitive response by inhibiting the activity of host catalases[J]. Cellular Microbiology, 2017, 19(8): e12736.
[41]	MHAMDI A, NOCTOR G, BAKER A. Plant catalases: peroxisomal redox guardians[J]. Archives of Biochemistry and Biophysics, 2012, 525(2): 181-194.
[42]	INABA J I, KIM B M, SHIMURA H, et al. Virus-induced necrosis is a consequence of direct protein-protein interaction between a viral RNA-silencing suppressor and a host catalase[J]. Plant Physiology, 2011, 156(4): 2026-2036.
[43]	ANGOT A, PEETERS N, LECHNER E, et al. Ralstonia solanacearum requires F-box-like domain-containing type Ⅲ effectors to promote disease on several host plants[J]. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(39): 14620-14625.
[44]	LIU T B, WANG Y N, STUKES S, et al. The F-Box protein Fbp1 regulates sexual reproduction and virulence in Cryptococcus neoformans[J]. Eukaryotic Cell, 2011, 10(6): 791-802.
[45]	SCHULMAN B A, CARRANO A C, JEFFREY P D, et al. Insights into SCF ubiquitin ligases from the structure of the Skp1-Skp2 complex[J]. Nature, 2000, 408(6810): 381-386.
[46]	XU C, LI M F, WU J K, et al. Identification of a canonical SCF(SLF) complex Involved in S-RNase-based self-incompatibility of Pyrus(Rosaceae)[J]. Plant Molecular Biology, 2013, 81(3): 245-257.
[47]	ZHUO T, WANG X, CHEN Z Y, et al. The Ralstonia solanacearum effector RipI induces a defence reaction by interacting with the bHLH93 transcription factor in Nicotiana benthamiana[J]. Molecular Plant Pathology, 2020, 21(7): 999-1004.
[48]	HEIM M A, JAKOBY M, WERBER M, et al. The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity[J]. Molecular Biology and Evolution, 2003, 20(5): 735-747.
[49]	BRUEX A, KAINKARYAM R M, WIECKOWSKI Y, et al. A gene regulatory network for root epidermis cell differentiation in Arabidopsis[J]. PLoS Genetics, 2012, 8(1): e1002446.
[50]	XIAN L, YU G, WEI Y L, et al. A bacterial effector protein hijacks plant metabolism to support pathogen nutrition[J]. Cell Host & Microbe, 2020, 28(4): 548-557.e7.
[51]	YU W J, LI M, WANG W J, et al. A bacterial type Ⅲ effector hijacks plant ubiquitin proteases to evade degradation[J]. PLoS Pathogens, 2025, 21(1): e1012882.
[52]	HUH S U. PopP2 interacts with PAD4 in an acetyltransferase activity-dependent manner and affects plant immunity[J]. Plant Signaling & Behavior, 2021, 16(12): 2017631.
[53]	SUN T Y, WU W, WU H X, et al. Ralstonia solanacearum elicitor RipX induces defense reaction by suppressing the mitochondrial atpA gene in host plant[J]. International Journal of Molecular Sciences, 2020, 21(6): 2000.
[54]	MENG Z, ZHENG X Y, ZHANG J, et al. The Ralstonia solanacearum RipAX family effectors repress the phosphorylation of host MAPKs[J]. Journal of Plant Pathology, 2024, 106(4): 1747-1757.
[55]	HOGENHOUT S A, VAN DER HOORN R A L, TERAUCHI R, et al. Emerging concepts in effector biology of plant-associated organisms[J]. Molecular Plant-Microbe Interactions, 2009, 22(2): 115-122.
[56]	FENG F, ZHOU J M. Plant-bacterial pathogen interactions mediated by type Ⅲ effectors[J]. Current Opinion in Plant Biology, 2012, 15(4): 469-476.
[57]	PETRE B, SAUNDERS D G O, SKLENAR J, et al. Candidate effector proteins of the rust pathogen Melampsora larici-Populina target diverse plant cell compartments[J]. Molecular Plant-Microbe Interactions, 2015, 28(6): 689-700.
[58]	吴幕绵, 陈舒婷, 李涛, 等. 青枯菌Ⅲ型效应蛋白调控植物免疫研究进展[J]. 广东农业科学, 2024, 51(8): 138-150.
[59]	NAKANO M, MUKAIHARA T. Comprehensive identification of PTI suppressors in type Ⅲ effector repertoire reveals that Ralstonia solanacearum activates jasmonate signaling at two different steps[J]. International Journal of Molecular Sciences, 2019, 20(23): 5992.
[60]	POPA C, LI L, GIL S, et al. The effector AWR5 from the plant pathogen Ralstonia solanacearum is an inhibitor of the TOR signalling pathway[J]. Scientific Reports, 2016, 6: 27058.
[61]	CAO P, CHEN J L, WANG R B, et al. A conserved type Ⅲ effector RipB is recognized in tobacco and contributes to Ralstonia solanacearum virulence in susceptible host plants[J]. Biochemical and Biophysical Research Communications, 2022, 631: 18-24.
[62]	JEON H, KIM W, KIM B, et al. Ralstonia solanacearum type Ⅲ effectors with predicted nuclear localization signal localize to various cell compartments and modulate immune responses in Nicotiana spp[J]. Plant Pathology Journal, 2020, 36(1): 43-53.
[63]	SANG Y Y, YU W J, ZHUANG H Y, et al. Intra-strain elicitation and suppression of plant immunity by Ralstonia solanacearum type-Ⅲ effectors in Nicotiana benthamiana[J]. Plant Communications, 2020, 1(4): 100025.
[64]	SUN Y H, LI P, SHEN D, et al. The Ralstonia solanacearum effector RipN suppresses plant PAMP-triggered immunity, localizes to the endoplasmic reticulum and nucleus, and alters the NADH/NAD⁺ratio in Arabidopsis[J]. Molecular Plant Pathology, 2019, 20(4): 533-546.
[65]	CHENG D, ZHOU D, WANG Y Q, et al. The Ralstonia solanacearum effector RipV1 acts as a novel E3 ubiquitin ligase to suppress plant PAMP-triggered immunity responses and promote susceptibility in potato[J]. Plant Pathology, 2024, 73(5): 1276-1288.
[66]	CHENG D, ZHOU D, WANG Y D, et al. Ralstonia solanacearum type Ⅲ effector RipV2 encoding a novel E3 ubiquitin ligase (NEL) is required for full virulence by suppressing plant PAMP-triggered immunity[J]. Biochemical and Biophysical Research Communications, 2021, 550: 120-126.
[67]	MACHO A P, GUIDOT A, BARBERIS P, et al. A competitive index assay identifies several Ralstonia solanacearum type Ⅲ effector mutant strains with reduced fitness in host plants[J]. Molecular Plant-Microbe Interactions, 2010, 23(9): 1197-1205.
[68]	NAKANO M, ODA K, MUKAIHARA T. Ralstonia solanacearum novel E3 ubiquitin ligase (NEL) effectors RipAW and RipAR suppress pattern-triggered immunity in plants[J]. Microbiology, 2017, 163(7): 992-1002.
[69]	WU D S, VON ROEPENACK-LAHAYE E, BUNTRU M, et al. A plant pathogen type Ⅲ effector protein subverts translational regulation to boost host polyamine levels[J]. Cell Host & Microbe, 2019, 26(5): 638-649.e5.
[70]	POUEYMIRO M, CAZALÉ A C, FRANÇOIS J M, et al. A Ralstonia solanacearum type Ⅲ effector directs the production of the plant signal metabolite trehalose-6-phosphate[J]. mBio, 2014, 5(6): e02065-14.

效应蛋白	亚细胞定位	互作宿主蛋白	互作机制	参考文献
RipGs	叶绿体和质膜	SKP1	模拟植物的F-box蛋白功能,劫持植物的SCF复合体,操纵植物的泛素-蛋白酶体系统	[43]
RipE1	—	植物去泛素化酶	与植物去泛素蛋白酶结合,有助于RipE1去泛素化和蛋白质稳定性	[51]
RipI	细胞核	bHLH93、GADs	与bHLH 93转录因子相互作用诱导宿主防御反应;与GADs相互作用,促进GADs被钙调蛋白激活	[47,50]
RipP2(Ppop2)	细胞核	PAD4	通过其乙酰转移酶活性靶向植物免疫调节蛋白PAD4	[52]
RipX	细胞核和质膜	atpA	抑制植物线粒体ATP合酶α亚基基因atpA的表达来诱导植物防御反应	[53]
RipAC	细胞核和细胞质	SGT1	与SGT1结合,抑制NLR介导的SGT1依赖性免疫反应	[14]
RipAK	过氧化物酶体	PDCs、CATs	与PDCs相互作用,抑制其寡聚化和酶活性,促进病原体的毒力;通过抑制CATs活性,靶向植物细胞内的过氧化物酶体,抑制植物的免疫反应	[39-40]
RipAS	核质	StTOPP6	与StTOPP6相互作用,导致StTOPP6在核仁中的积累减少	[34]
RipAX1、RipAX2	细胞质	MAPK	RipAX1及RipAX2能够与MAPK相互作用,RipAX1能够抑制MAPKs的磷酸化	[54]
RipAY	细胞核和细胞质	H型硫氧还蛋白	降解植物中的谷胱甘肽,抑制SA介导的防御	[25-26]

效应蛋白	亚细胞定位	互作宿主蛋白	互作机制	参考文献
RipGs	叶绿体和质膜	SKP1	模拟植物的F-box蛋白功能,劫持植物的SCF复合体,操纵植物的泛素-蛋白酶体系统	[43]
RipE1	—	植物去泛素化酶	与植物去泛素蛋白酶结合,有助于RipE1去泛素化和蛋白质稳定性	[51]
RipI	细胞核	bHLH93、GADs	与bHLH 93转录因子相互作用诱导宿主防御反应;与GADs相互作用,促进GADs被钙调蛋白激活	[47,50]
RipP2(Ppop2)	细胞核	PAD4	通过其乙酰转移酶活性靶向植物免疫调节蛋白PAD4	[52]
RipX	细胞核和质膜	atpA	抑制植物线粒体ATP合酶α亚基基因atpA的表达来诱导植物防御反应	[53]
RipAC	细胞核和细胞质	SGT1	与SGT1结合,抑制NLR介导的SGT1依赖性免疫反应	[14]
RipAK	过氧化物酶体	PDCs、CATs	与PDCs相互作用,抑制其寡聚化和酶活性,促进病原体的毒力;通过抑制CATs活性,靶向植物细胞内的过氧化物酶体,抑制植物的免疫反应	[39-40]
RipAS	核质	StTOPP6	与StTOPP6相互作用,导致StTOPP6在核仁中的积累减少	[34]
RipAX1、RipAX2	细胞质	MAPK	RipAX1及RipAX2能够与MAPK相互作用,RipAX1能够抑制MAPKs的磷酸化	[54]
RipAY	细胞核和细胞质	H型硫氧还蛋白	降解植物中的谷胱甘肽,抑制SA介导的防御	[25-26]

效应蛋白	亚细胞定位	功能	参考文献
RipA5	细胞质	在酵母和本氏烟草中抑制TOR通路,在拟南芥中对毒力产生负面影响,并在不同种类的烟草中引发细胞死亡	[59-60]
RipB		Roq1介导的青枯病抗性	[61]
RipD	内质网	提高茄子、番茄和豆类中细菌的适应性,以及在本氏烟草中抑制flg22诱导的活性氧自由基产生	[62]
RipE1	—	诱导水杨酸和茉莉酸合成以触发拟南芥和本氏烟草中的免疫应答	[63]
RipM、RipQ、RipS1	—	在本氏烟草中抑制flg22诱导的活性氧自由基产生	[59]
RipN	细胞核和内质网	改变植物NADH/NAD⁺比率并抑制拟南芥中的PAMP触发的免疫防御	[64]
RipV1、RipV2	质膜	PAMP引发的免疫抑制对其E3泛素连接酶活性的影响	[65-66]
RipX	细胞核和质膜	在矮牵牛、烟草和本氏烟草中通过对其atpA基因的转录以及离子传导孔形成的负面效应	[53]
RipAD	细胞质和叶绿体	在本氏烟草中抑制flg22诱导的活性氧自由基产生	[62]
RipAF1	细胞核和细胞质		[62,67]
RipAR、RipAW	细胞质	PAMP引发的免疫抑制对其E3泛素连接酶活性的影响	[68]
RipAU			[59]
RipAY	细胞核和细胞质	在酵母、茄子和拟南芥中耗竭谷胱甘肽,在拟南芥中抑制水杨酸介导的防御,并在本氏烟草中抑制RipE1介导的超敏反应	[63]
RipTAL	细胞核	诱导植物多胺的合成,抑制竞争菌株的增殖	[69]
RipTPS	—	在酵母中合成海藻糖-6-磷酸,并在烟草中诱导酶活性独立的超敏反应	[70]

效应蛋白	亚细胞定位	功能	参考文献
RipA5	细胞质	在酵母和本氏烟草中抑制TOR通路,在拟南芥中对毒力产生负面影响,并在不同种类的烟草中引发细胞死亡	[59-60]
RipB		Roq1介导的青枯病抗性	[61]
RipD	内质网	提高茄子、番茄和豆类中细菌的适应性,以及在本氏烟草中抑制flg22诱导的活性氧自由基产生	[62]
RipE1	—	诱导水杨酸和茉莉酸合成以触发拟南芥和本氏烟草中的免疫应答	[63]
RipM、RipQ、RipS1	—	在本氏烟草中抑制flg22诱导的活性氧自由基产生	[59]
RipN	细胞核和内质网	改变植物NADH/NAD⁺比率并抑制拟南芥中的PAMP触发的免疫防御	[64]
RipV1、RipV2	质膜	PAMP引发的免疫抑制对其E3泛素连接酶活性的影响	[65-66]
RipX	细胞核和质膜	在矮牵牛、烟草和本氏烟草中通过对其atpA基因的转录以及离子传导孔形成的负面效应	[53]
RipAD	细胞质和叶绿体	在本氏烟草中抑制flg22诱导的活性氧自由基产生	[62]
RipAF1	细胞核和细胞质		[62,67]
RipAR、RipAW	细胞质	PAMP引发的免疫抑制对其E3泛素连接酶活性的影响	[68]
RipAU			[59]
RipAY	细胞核和细胞质	在酵母、茄子和拟南芥中耗竭谷胱甘肽,在拟南芥中抑制水杨酸介导的防御,并在本氏烟草中抑制RipE1介导的超敏反应	[63]
RipTAL	细胞核	诱导植物多胺的合成,抑制竞争菌株的增殖	[69]
RipTPS	—	在酵母中合成海藻糖-6-磷酸,并在烟草中诱导酶活性独立的超敏反应	[70]