寄主植物与病原菌免疫反应的分子遗传基础

doi:10.16288/j.yczz.20-015

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Hereditas(Beijing) ›› 2020, Vol. 42 ›› Issue (3): 278-286.doi: 10.16288/j.yczz.20-015

• Review • Previous Articles Next Articles

Molecular genetic mechanisms of interaction between host plants and pathogens

Dewei Yang^1,³, Shengping Li^2,³, Haitao Cui^2,³, Shenghao Zou³, Wei Wang^2,³()

^1. Institute of Rice, Fujian Academy of Agricultural Sciences, Fuzhou 350018, China
^2. College of Agriculture, Fujian Agriculture and Forestry University, Fuzhou 350002, China
^3. Plant Immunity Center, Fujian Agriculture and Forestry University, Fuzhou 350002, China

Received:2020-01-13 Revised:2020-02-19 Online:2020-03-20 Published:2020-03-01
Contact: Wang Wei E-mail:vic_0214@163.com
Supported by:
Supported by the Youth Technology Innovation Team of the Fujian Academy of Agricultural Sciences No(STIT2017-3-3);the Special Fund for Agro-scientific Research in the Public Interest of Fujian Province No(2017R1021-2);Fujian Provincial Natural Science Foundation No(2019J01102);the Free Exploration Project of the Fujian Academy of Agricultural Sciences No(AA2018-21)

Abstract

Abstract:

In recent years, a great number of plant resistance (R) genes and pathogen avirulence (Avr) genes were identified. Exciting breakthroughs were also made on the structural and functional analysis of R proteins and Avr proteins, and the mechanistic interaction between them. Plants have evolved two layers of the immune system to cope with pathogens in the evolutionary processes, which are pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) and effector-triggered immunity (ETI). In PTI responses, conserved PAMPs are recognized by plant plasma membrane-localized pattern recognition receptors (PRRs) and disease resistance is activated. Furthermore, the ETI immune signaling is activated by the recognition of pathogen Avr proteins by the host R proteins, which usually results in hypersensitive responses at the infection site. In this review, we summarize the progresses on PTI and ETI, and discuss the genetic mechanism of the interaction between plant R gene and pathogen Avr gene in detail. We also envision the new challenges and propose the new strategies for the future investigations on plant resistance molecular breeding.

Key words: plant, Resistance gene, Avirulence gene, interaction, breeding utilization research

Dewei Yang, Shengping Li, Haitao Cui, Shenghao Zou, Wei Wang. Molecular genetic mechanisms of interaction between host plants and pathogens[J]. Hereditas(Beijing), 2020, 42(3): 278-286.

Figures/Tables 2

Fig. 1

Supplementary Table 1

Plant disease resistance genes and avirulence genes"

无毒基因	病原菌	寄主	抗性基因	参考文献链接
P3	Soybean mosaic virus	Glycine max	3gG2	http://www.ncbi.nlm.nih.gov/pubmed/23051173
Avr9	Cladosporium fulvum (Syn. Passalora fulva)	Solanum lycopersicum	9DC1	http://www.ncbi.nlm.nih.gov/pubmed/15579714
Avr9	Cladosporium fulvum (Syn. Passalora fulva)	Solanum lycopersicum	9DC2(Syn. 9DC)	https://www.ncbi.nlm.nih.gov/pubmed/11517316/
Avr9	Cladosporium fulvum (Syn. Passalora fulva)	Solanum lycopersicum	9DC3	http://www.ncbi.nlm.nih.gov/pubmed/15579714
Sphinganine-analog mycotoxins	Alternaria alternata	Solanum lycopersicum	Asc-1	http://onlinelibrary.wiley.com/doi/10.1046/j.1365-313X.2002.01444.x/abstract
Not identification	Pseudoperonospora cubensis	Cucumis melo L.	At1	http://www.plantcell.org/content/16/1/172.long
Not identification	Pseudoperonospora cubensis	Cucumis melo L.	At2	http://www.plantcell.org/content/16/1/172.long
Not identification	Clover yellow vein virus	Phaseolus vulgaris	bc-3	http://www.ncbi.nlm.nih.gov/pubmed/23933781
Not identification	Turnip mosaic virus (TuMV)	Brasica pekinensis Rupr	BcTuR3	http://link.springer.com/article/10.1007%2Fs11105-010-0183-3
Not identification	Nilaparvata lugens	Oryza sativa L.	Bph1/9-1 (Syn. Bph1/ Bph10/Bph18/Bph21)	https://www.ncbi.nlm.nih.gov/pubmed/27791169
Not identification	Nilaparvata lugens	Oryza sativa L.	Bph1/9-2 (Syn. Bph2/Bph26)	https://www.ncbi.nlm.nih.gov/pubmed/25076167/
Not identification	Nilaparvata lugens	Oryza sativa L.	Bph1/9-7 (Syn. Bph7;Syn. Bph9)	https://www.ncbi.nlm.nih.gov/pubmed/27791169
Not identification	Nilaparvata lugens	Oryza sativa L.	Bph14	https://www.ncbi.nlm.nih.gov/pubmed/20018701/
AvrBs2	Xanthomonas axonopodis	Solanum lycopersicum	Bs2	http://www.pnas.org/content/96/24/14153.long
AvrHah1	Xanthomonas gardneri	Piper nigrum L.	Bs3	http://www.ncbi.nlm.nih.gov/pubmed/19086184
Hax4	Xanthomonas campestris	Solanum lycopersicum	Bs4	http://apsjournals.apsnet.org/doi/abs/10.1094/MPMI-18-0838
AvrBs4	Xanthomonas campestris	Piper nigrum L.	Bs4C-R	http://www.pnas.org/content/109/47/19480.long
Putative PGN	Pseudomonas syringae	Solanum lycopersicum	Bti9	http://onlinelibrary.wiley.com/doi/10.1111/j.1365-313X.2011.04773.x/full
Not identification	Ralstonia solanacearum	Nicotiana L.	CaLRR51	https://www.ncbi.nlm.nih.gov/pubmed/27438958
Not identification	Meloidogyne incognita	Piper nigrum L.	CaMi	http://www.ncbi.nlm.nih.gov/pubmed/17310335
Not identification	Phakopsora pachyrhizi	Glycine?max	CcRpp1	https://www.ncbi.nlm.nih.gov/pubmed/27111723
Avr4	Cladosporium fulvum (Syn. Passalora fulva)	Solanum lycopersicum	Cf-4 (Syn. Hcr9-4D)	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC157069/
Avr5	Cladosporium fulvum (Syn. Passalora fulva)	Solanum lycopersicum	Cf-5 (Syn. Hcr2-5C)	http://www.ncbi.nlm.nih.gov/pubmed/24678832
Avr9	Cladosporium fulvum (Syn. Passalora fulva)	Solanum lycopersicum	Cf-9 (Syn. Hcr9-9C)	https://www.ncbi.nlm.nih.gov/pubmed/7973631
Not identification	-	Nicotiana benthamiana	Cf-9B (Hcr9-9B)	http://www.ncbi.nlm.nih.gov/pubmed/19737095
Avr9B	Cladosporium fulvum (Syn. Passalora fulva)	Solanum lycopersicum	Cf-9B (Syn. Hcr9-9B)	https://www.ncbi.nlm.nih.gov/pubmed/12423015
Not identification	Heterodera avenae	Triticum aestivum	Cre1	http://apsjournals.apsnet.org/doi/abs/10.1094/MPMI.2003.16.12.1129
Not identification	Heterodera avenae	Triticum aestivum	Cre3	http://www.ncbi.nlm.nih.gov/pubmed/9352645
Not identification	Clover yellow vein virus	Arabidopsis thaliana	cum1-1	http://www.ncbi.nlm.nih.gov/pubmed/15710407
Not identification	Cuscuta reflexa	Solanum lycopersicum	CuRe1	http://science.sciencemag.org/content/353/6298/478.full
Coat protein	Mungbean Yellow Mosaic India Virus (MYMIV)	Vigna mungo	CYR1	http://www.ncbi.nlm.nih.gov/pubmed/22205242
Not identification	-	Arabidopsis thaliana	Dm1 (Uk-3)	http://www.cell.com/current-biology/fulltext/S0960-9822(17)30287-7?elsca1=etoc&elsca2=email&elsca3=0960-9822_20170424_27_8_&elsca4=Cell%20Press
Not identification	Potato virus Y (PVY)	Solanum tuberosum L.	Eva1	http://www.ncbi.nlm.nih.gov/pubmed/22146867
Not identification	Plantago Asiatica Mosaic Virus (PIAMV)	Arabidopsis thaliana	EXA1	http://onlinelibrary.wiley.com/doi/10.1111/tpj.13265/abstract?campaign=woletoc
AvrFom1	Fusarium oxysporum	Cucumis melo L.	Fom-1 (Syn. RGH9)	http://www.cell.com/molecular-plant/fulltext/S1674-2052(14)60896-0#sec1
AvrFom2	Fusarium oxysporum	Cucumis melo L.	Fom-2	http://onlinelibrary.wiley.com/doi/10.1111/nph.13584/abstract
Not identification	Verticillium dahliae	Gossypium spp	GbVE	http://www.ncbi.nlm.nih.gov/pubmed/21739145?dopt=Abstract&holding=npg
Not identification	Xanthomonas oryzae	Oryza sativa L.	GH3-2	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3075746/
Not identification	Xanthomonas oryzae	Oryza sativa L.	GH3-8	https://www.ncbi.nlm.nih.gov/pubmed/18192436/
Not identification	Heterodera glycines	Glycine max	GmSNAP18 (Syn. Rhg1-a)	http://www.nature.com/articles/ncomms14822
RBP-1	Globodera pallida	Solanum tuberosum L.	Gpa2	http://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1000564
Not identification	Globodera rostochiensis	Solanum tuberosum L.	Gro1-4	http://www.ncbi.nlm.nih.gov/pubmed/15078331
Not identification	Cercospora zeae-maydis	Zea mays	GST23	https://www.ncbi.nlm.nih.gov/pubmed/21490302
Not identification	Plasmopara halstedii	Sunflower	Ha-NTIR11g	http://jxb.oxfordjournals.org/content/56/412/567.full
Avr4E	Cladosporium fulvum (Syn. Passalora fulva)	Solanum lycopersicum	Hcr9-4E	http://www.ncbi.nlm.nih.gov/pubmed/15469522
Not identification	-	Nicotiana benthamiana	Hcr9-9A	http://www.ncbi.nlm.nih.gov/pubmed/19737095
Not identification	Cladosporium fulvum (Syn. Passalora fulva)	Solanum lycopersicum	Hcr9-9E	https://www.ncbi.nlm.nih.gov/pubmed/9413991
Not identification	Venturia inaequalis	Apple	HcrVf2	http://www.pnas.org/content/101/3/886.abstract?ijkey=f43e5958b2305e9ffda4630133bb94f35f67075d&keytype2=tf_ipsecsha
Not identification	Globodera rostochiensis	Solanum lycopersicum	Hero A	http://www.ncbi.nlm.nih.gov/pubmed/12121443
Ave1	Verticillium dahliae	Arabidopsis thaliana	HLVe1-2A	http://onlinelibrary.wiley.com/doi/10.1111/mpp.12390/full
HC toxin	Cochliobolus carbonum	Zea mays	Hm1	http://science.sciencemag.org/content/258/5084/985.long
Coat protein	Turnip crinckle virus	Arabidopsis thaliana	Hrt1	http://www.sciencedirect.com/science/article/pii/S0042682204007202
Not identification	Heterodera schachtii	Beta vulgaris L.	Hs1(pro-1)	http://www.ncbi.nlm.nih.gov/pubmed/9012350
Not identification	Pseudomonas syringae	Nicotiana L.	Hth	http://onlinelibrary.wiley.com/doi/10.1111/j.1365-313X.1993.tb00165.x/abstract
Not identification	Exserohilum turcicum	Zea mays	Htn1 (Syn. ZmWAK-RLK1)	https://www.ncbi.nlm.nih.gov/pubmed/26124097
HC toxin	Cochliobolus carbonum	Hordeum?vulgare	HvHm1	http://www.pnas.org/content/105/5/1762.full
Avr1 (Syn. Six4)	Fusarium oxysporum	Solanum lycopersicum	I	https://www.ncbi.nlm.nih.gov/pubmed/27995670
Avr2 (Six3)	Fusarium oxysporum	Solanum lycopersicum	I2	https://www.ncbi.nlm.nih.gov/pubmed/19228334
Not identification	Fusarium oxysporum	Solanum lycopersicum	I-7	http://www.ncbi.nlm.nih.gov/pubmed/26177154
Not identification	Diabrotica virgifera	Zea mays	IPD072Aa	http://science.sciencemag.org/content/354/6312/634?utm_campaign=toc_sci-mag_2016-11-03&et_rid=17077626&et_cid=959510
Not identification	Botrytis cinerea	Solanum lycopersicum	IVR	http://apsjournals.apsnet.org/doi/abs/10.1094/PHYTO-100-3-0225
Not identification	Tobacco Etch Virus	Arabidopsis thaliana	JAX1	http://www.ncbi.nlm.nih.gov/pubmed/22307853
Coat protein	Tobamovirus	Piper nigrum L.	L^1a	http://apsjournals.apsnet.org/doi/abs/10.1094/MPMI-06-10-0127
Not identification	Melampsora lini	Linum usitatissimum	L2	http://www.ncbi.nlm.nih.gov/pubmed/10072407?dopt=Abstract
Coat protein	Tobamovirus	Piper nigrum L.	L^2b	http://apsjournals.apsnet.org/doi/abs/10.1094/MPMI-06-10-0127
Not identification	Melampsora lini	Linum usitatissimum	L3	http://www.ncbi.nlm.nih.gov/pubmed/10072407?dopt=Abstract
AvrL567-E	Melampsora lini	Linum usitatissimum	L5	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1482673/
Not identification	Melampsora lini	Linum usitatissimum	L8	http://www.ncbi.nlm.nih.gov/pubmed/10072407?dopt=Abstract
Not identification	Striga	Sorghum	LGS1	http://www.pnas.org/content/114/17/4471
Victorin	Cochliobolus victoriae	Arabidopsis thaliana	LOV1	https://www.ncbi.nlm.nih.gov/pubmed/23087001
AVR1	Puccinia triticina	Triticum aestivum	Lr1	http://link.springer.com/article/10.1007%2Fs11103-007-9201-8
AvrLr21	Puccinia triticina	Triticum aestivum	Lr21	http://www.genetics.org/content/164/2/655.long
AVR1	Puccinia triticina	Triticum aestivum	Lr22a	https://www.ncbi.nlm.nih.gov/pubmed/28504667
Not identification	Puccinia striiformis	Triticum aestivum	Lr34 (syn. Yr18/Pm38/Ltn1)	http://science.sciencemag.org/content/323/5919/1360.long
Not identification	Puccinia striiformis	Triticum aestivum	Lr67 (syn. Pm46/ Sr55/Yr46/Ltn3)	http://www.nature.com/ng/journal/v47/n12/abs/ng.3439.html
Not identification	Turnip mosaic virus (TuMV)	Arabidopsis thaliana	lsp1-1	http://www.ncbi.nlm.nih.gov/pubmed/12123581
AvrM	Melampsora lini	Linum usitatissimum	M	https://www.ncbi.nlm.nih.gov/pubmed/16326930
Not identification	Meloidogyne	Prunus cerasifera Ehrh	Ma	http://www.plantphysiol.org/content/156/2/779.long
Not identification	Meloidogyne	Solanum lycopersicum	Mi-1	http://www.plantcell.org/content/10/8/1307.long
AVRa1	Blumeria graminis	Hordeum?vulgare	Mla1	http://www.plantcell.org/content/13/2/337.abstract?ijkey=c5713604701ee5a09abcf09273b43f0de9e2f8e7&keytype2=tf_ipsecsha
AVRa10	Blumeria graminis	Hordeum?vulgare	Mla10	https://www.ncbi.nlm.nih.gov/pubmed/16905653
AvrMla12	Blumeria graminis	Hordeum?vulgare	Mla12	http://www.plantcell.org/content/15/3/732.abstract?ijkey=0b1e54f48774d56a8dfe0908d8b574baffb11c4b&keytype2=tf_ipsecsha
AVRa13	Blumeria graminis	Hordeum?vulgare	Mla13	http://www.plantphysiol.org/content/131/2/558.abstract?ijkey=1e8d7f4258e07863bdc38fe2c7fe70f96cb093b6&keytype2=tf_ipsecsha
AvrMla6	Blumeria graminis	Hordeum?vulgare	Mla6	http://www.ncbi.nlm.nih.gov/pubmed/11208025
AvrMla7	Blumeria graminis	Hordeum?vulgare	Mla7	http://www.ncbi.nlm.nih.gov/pubmed/15078326
Not identification	Blumeria graminis	Hordeum?vulgare	Mla8	http://apsjournals.apsnet.org/doi/abs/10.1094/MPMI-23-4-0497
Not identification	Blumeria graminis	Hordeum?vulgare	Mla9	http://apsjournals.apsnet.org/doi/abs/10.1094/MPMI-23-4-0497
Not identification	Lettuce Mosaic Virus	Lactuca sativa L. var. ramosa Hort	Mo-1	http://www.ncbi.nlm.nih.gov/pubmed/12857809
Not identification	Diplocarpon rosae	Rosa rugosa Thunb	muRdr1A (Syn. Rdr1)	https://www.ncbi.nlm.nih.gov/pubmed/28779550
AvrPto	Pseudomonas syringae	Nicotiana benthamiana	NbPrf (Niben101Scf00650g02002XLOC)	https://www.ncbi.nlm.nih.gov/pubmed/11874570?dopt=Abstract
FoAve1	Fusarium oxysporum	Nicotiana glutinosa	NgVe1	http://onlinelibrary.wiley.com/doi/10.1111/mpp.12390/full
Not identification	Xanthomonas oryzae	Oryza sativa L.	OsAPX8	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4868969/
Not identification	Magnaporthe oryzae	Oryza sativa L.	OsCul3a	http://www.plantcell.org/content/early/2017/01/18/tpc.16.00650.abstract?papetoc
AvrP	Melampsora lini	Linum usitatissimum	P	http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2767095/
AvrP123	Melampsora lini	Linum usitatissimum	P2	https://www.ncbi.nlm.nih.gov/pubmed/16326930
Not identification	Heterobasidion parviporum	Picea abies	PaLAR3	https://www.ncbi.nlm.nih.gov/pubmed/27317690
Not identification	Pantoea stewartii	Zea mays	pan1	https://www.ncbi.nlm.nih.gov/pubmed/25009146
Not identification	Magnaporthe oryzae	Oryza sativa L.	Pb1	http://www.ncbi.nlm.nih.gov/pubmed/20807214?dopt=Abstract&holding=f1000,f1000m,isrctn
AvrBs3Δ16	Xanthomonas campestris	Piper nigrum L.	pBs3-E	http://science.sciencemag.org/content/318/5850/645.full
Pc-toxin	Periconia circinata	Sorghum bicolor (L.) Moench	Pc	https://www.ncbi.nlm.nih.gov/pubmed/18719093
Not identification	Tomato yellow leaf curl virus	Solanum lycopersicum	Pelo (Syn. Ty-5)	http://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1005538
Not identification	Phytophthora infestans	Solanum lycopersicum	Ph-3	http://link.springer.com/article/10.1007%2Fs00122-014-2303-1
Not identification	Magnaporthe oryzae	Oryza sativa L.	Pi1-5	https://www.ncbi.nlm.nih.gov/pubmed/22643901
Not identification	Magnaporthe oryzae	Oryza sativa L.	Pi2	http://apsjournals.apsnet.org/doi/abs/10.1094/MPMI-19-1216
Not identification	Magnaporthe oryzae	Oryza sativa L.	pi21	http://science.sciencemag.org/content/325/5943/998.long
Not identification	Magnaporthe oryzae	Oryza sativa L.	Pi25	http://www.sciencedirect.com/science/article/pii/S1673852711000567
Not identification	Magnaporthe oryzae	Oryza sativa L.	Pi35	https://www.nature.com/articles/srep04550
Not identification	Magnaporthe oryzae	Oryza sativa L.	Pi36	http://www.genetics.org/content/176/4/2541.long
Not identification	Magnaporthe oryzae	Oryza sativa L.	Pi37	http://www.genetics.org/content/177/3/1871.long
Not identification	Magnaporthe oryzae	Oryza sativa L.	Pi50	https://www.ncbi.nlm.nih.gov/pubmed/26183036
Not identification	Magnaporthe oryzae	Oryza sativa L.	Pi5-2	http://www.ncbi.nlm.nih.gov/pubmed/19153255?dopt=Abstract&holding=f1000,f1000m,isrctn
Not identification	Magnaporthe oryzae	Oryza sativa L.	Pi54 (Syn. Pik-k(h))	https://link.springer.com/article/10.1007%2Fs13562-010-0026-1
Not identification	Magnaporthe oryzae	Oryza sativa L.	Pi55(t)	https://www.ncbi.nlm.nih.gov/pubmed/22415685/
Not identification	Magnaporthe oryzae	Oryza sativa L.	Pi64	https://www.ncbi.nlm.nih.gov/pubmed/25650828
AvrPi9	Magnaporthe oryzae	Oryza sativa L.	Pi9	http://www.ncbi.nlm.nih.gov/pubmed/25659573
AvrPiB	Magnaporthe oryzae	Oryza sativa L.	Pib	http://www.nature.com/articles/srep11642
Not identification	Magnaporthe oryzae	Oryza sativa L.	Pi-d2	http://www.ncbi.nlm.nih.gov/pubmed/16709195
Not identification	Magnaporthe oryzae	Oryza sativa L.	Pid3	http://www.genetics.org/content/182/4/1303.long
Not identification	Magnaporthe oryzae	Oryza sativa L.	Pid3-A4	https://www.ncbi.nlm.nih.gov/pubmed/23384860/
Not identification	Magnaporthe oryzae	Oryza sativa L.	PigmR (Syn. PigmR6)	https://www.ncbi.nlm.nih.gov/pubmed/28154240
AvrPii	Magnaporthe oryzae	Oryza sativa L.	Pii	http://www.ncbi.nlm.nih.gov/pubmed/26186703
Avr-PikE	Magnaporthe oryzae	Oryza sativa L.	Pik-1	https://www.ncbi.nlm.nih.gov/pubmed/21118257
Avr-PikA	Magnaporthe oryzae	Oryza sativa L.	Pik-h	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2700537/
Avr-PikD	Magnaporthe oryzae	Oryza sativa L.	Pik-p1	https://www.ncbi.nlm.nih.gov/pubmed/21153625
Avr-PikD	Magnaporthe oryzae	Oryza sativa L.	Pik-s	https://www.ncbi.nlm.nih.gov/pubmed/24896089
Not identification	Magnaporthe oryzae	Oryza sativa L.	Pish	http://bmcplantbiol.biomedcentral.com/articles/10.1186/1471-2229-10-175
Not identification	Magnaporthe oryzae	Oryza sativa L.	Pit	http://www.ncbi.nlm.nih.gov/pubmed/18808453
AvrPita2	Magnaporthe oryzae	Oryza sativa L.	Pi-ta	http://www.ncbi.nlm.nih.gov/pubmed/18393625
AvrPiz-t	Magnaporthe oryzae	Oryza sativa L.	Piz-t	http://apsjournals.apsnet.org/doi/abs/10.1094/MPMI-22-4-0411
BgsE-5845	Blumeria graminis	Triticum aestivum	Pm2	http://onlinelibrary.wiley.com/doi/10.1111/nph.14372/full
AvrPm3^a2/f2	Blumeria graminis	Triticum aestivum	Pm3a	http://www.plantcell.org/content/27/10/2991.abstract?etoc
AvrPm3b	Blumeria graminis	Triticum aestivum	Pm3b	http://www.ncbi.nlm.nih.gov/pubmed/14756761
Not identification	Blumeria graminis	Triticum aestivum	Pm3c	https://www.ncbi.nlm.nih.gov/pubmed/16740148
Not identification	Blumeria graminis	Triticum aestivum	Pm3d	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1256003/
Not identification	Blumeria graminis	Triticum aestivum	Pm3e	https://www.ncbi.nlm.nih.gov/pubmed/16740148
AvrPm3^a2/f2	Blumeria graminis	Triticum aestivum	Pm3f	http://www.plantcell.org/content/27/10/2991.abstract?etoc
Not identification	Blumeria graminis	Triticum aestivum	Pm3g	https://www.ncbi.nlm.nih.gov/pubmed/16740148
Not identification	Blumeria graminis	Triticum aestivum	Pm3k	https://www.ncbi.nlm.nih.gov/pubmed/18980638?dopt=Abstract
Not identification	Potato virus Y (PVY)	Solanum lycopersicum	Pot-1	http://www.ncbi.nlm.nih.gov/pubmed/15971038
avrPtoB, AvrPto (B728a)	Pseudomonas syringae	Solanum lycopersicum	Prf	https://www.ncbi.nlm.nih.gov/pubmed/16391110
avrBs3	Xanthomonas citri	Citrus X paradise	ProBs314EBE::avrGf1	http://onlinelibrary.wiley.com/doi/10.1111/mpp.12454/full
Not identification	Papaya ring-spot virus	Cucumis melo L.	Prv1 (Syn. RGH10)	http://www.cell.com/molecular-plant/fulltext/S1674-2052(14)60896-0#sec1
2a	Cucumber mosaic virus (CMV)	Phaseolus vulgaris	PvCMR1 (Syn. RT4-4)	http://www.ncbi.nlm.nih.gov/pubmed/16880399
Not identification	Potato virus Y (PVY)	Piper nigrum L.	Pvr2¹	http://onlinelibrary.wiley.com/doi/10.1046/j.1365-313X.2002.01499.x/abstract
RNA-dependent RNA polymerase (NIb)	Potato virus Y (PVY)	Nicotiana benthamiana	Pvr4	https://www.ncbi.nlm.nih.gov/pubmed/27612097
Not identification	Pepper Veinal Mottle Virus	Piper nigrum L.	pvr6	http://www.ncbi.nlm.nih.gov/pubmed/19641047
BV1	Bean Dwarf Mosaic Virus	Phaseolus vulgaris	PvVTT1	http://www.ncbi.nlm.nih.gov/pubmed/20507487
Not identification	Magnaporthe grisea	Zea mays	qMdr9.02 (Syn. ZmCCoAOMT2)	https://www.ncbi.nlm.nih.gov/pubmed/28740263
Not identification	Fusarium graminearum	Zea mays	qRfg1 (Syn. ZmCCT)	https://www.ncbi.nlm.nih.gov/pubmed/28722229
Avr1	Phytophthora infestans	Solanum tuberosum L.	R1	http://library.wur.nl/WebQuery/wurpubs/369564
Avr2	Phytophthora infestans	Solanum tuberosum L.	R2	http://www.ncbi.nlm.nih.gov/pubmed/22885736
Avr3a KI	Phytophthora infestans	Solanum tuberosum L.	R3a	https://www.ncbi.nlm.nih.gov/pubmed/15807786
Avr3b	Phytophthora infestans	Solanum tuberosum L.	R3b	http://www.ncbi.nlm.nih.gov/pubmed/21649512
Avr8	Phytophthora infestans	Solanum tuberosum L.	R8 (Syn. Rpi-smira2)	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4983296/
Not identification	Albugo candida	Arabidopsis thaliana	RAC1	http://apsjournals.apsnet.org/doi/abs/10.1094/MPMI.2004.17.7.711
Avrblb1 (Syn. IPI-O/PexRD)	Phytophthora infestans	Solanum tuberosum L.	Rb (Syn. Rpi-blb1)	https://www.ncbi.nlm.nih.gov/pubmed/18682852
HopBA1	Pseudomonas syringae	Arabidopsis thaliana	RBA1	https://www.ncbi.nlm.nih.gov/pubmed/28137883
Not identification	Glomerella graminicola (Syn. Colletotrichum graminicola)	Zea mays	Rcg1	https://www.google.com/patents/WO2006107931A2?cl=en
Not identification	Colletotrichum trifolii	Lotuscorniculatus L.	RCT1	http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2527883/
Coat protein	Cucumber mosaic virus (CMV)	Arabidopsis thaliana	Rcy1	http://www.ncbi.nlm.nih.gov/pubmed/12472683
Not identification	Pyrenophora graminea	Hordeum vulgare	Rdg2a	http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0012599
Not identification	Turnip mosaic virus (TuMV)	Brassica oleracea L. var.capitata L.	retr01	http://www.ncbi.nlm.nih.gov/pubmed/17947545
Not identification	Fusarium oxysporum	Arabidopsis thaliana	RFO1	http://www.genetics.org/content/171/1/305.long
Not identification	Fusarium oxysporum	Arabidopsis thaliana	RFO3	http://www.ncbi.nlm.nih.gov/pubmed/23790083
AvrLr10	Puccinia triticina	Triticum aestivum	Rga2	http://www.ncbi.nlm.nih.gov/pubmed/19769576
Not identification	-	Triticum aestivum	RGA2a	http://science.sciencemag.org/content/341/6147/786.long
Avr-Pia	Magnaporthe oryzae	Oryza sativa L.	RGA5-A (Syn. Pia-1)	https://www.ncbi.nlm.nih.gov/pubmed/21251109
Avr3	Bremia lactucae	Lactuca sativa L. var. ramosa Hort	RGC2B (Syn. Dm3)	http://www.plantcell.org/content/10/11/1817.full.html
Not identification	Heterodera glycines	Glycine max	Rhg1-b	http://science.sciencemag.org/content/338/6111/1206
Not identification	Leptosphaeria maculans	Arabidopsis thaliana	RLM1A	http://onlinelibrary.wiley.com/doi/10.1111/j.1365-313X.2006.02688.x/abstract
AvrLm2	Leptosphaeria maculans	Brassica campestris L.	RLM2	http://onlinelibrary.wiley.com/doi/10.1111/pbi.12341/abstract
Not identification	Alternaria brassicae	Arabidopsis thaliana	RLM3	http://bmcplantbiol.biomedcentral.com/articles/10.1186/s12870-014-0298-z
XopQ	Xanthomonas campestris	Nicotiana benthamiana	Roq1	https://www.ncbi.nlm.nih.gov/pubmed/28891100
Complex of PGTG_10537.2 and PGTG_16791	Puccinia graminis	Hordeum vulgare	Rpg1	https://www.ncbi.nlm.nih.gov/pubmed/21873196
AvrB	Pseudomonas savastanoi	Glycine max	Rpg1-b	http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0108159
AvrRpm1	Pseudomonas syringae	Glycine max	Rpg1r	http://www.plantphysiol.org/content/166/1/235.long
Not identification	Puccinia graminis	Hordeum vulgare	Rpg5	http://www.ncbi.nlm.nih.gov/pubmed/23216085
AvrLr10	Puccinia sorghi	Zea mays	Rpi1-D	http://www.plantcell.org/content/11/7/1365.long
Avr2	Phytophthora infestans	Solanum tuberosum L.	Rpi-abpt	http://www.ncbi.nlm.nih.gov/pubmed/22885736
Not identification	Phytophthora infestans	Solanum tuberosum L.	Rpi-amr3i	https://www.ncbi.nlm.nih.gov/pubmed/27111721
Avrblb2 (Syn. PexRD39/PexRD40)	Phytophthora infestans	Solanum tuberosum L.	Rpi-blb2	https://www.ncbi.nlm.nih.gov/pubmed/19794118/
Avr2	Phytophthora infestans	Solanum tuberosum L.	Rpi-blb3	http://www.ncbi.nlm.nih.gov/pubmed/22885736
Avrblb1 (Syn. IPI-O/PexRD)	Phytophthora infestans	Solanum tuberosum L.	Rpi-pta1	https://www.ncbi.nlm.nih.gov/pubmed/18682852
Avr2	Phytophthora infestans	Solanum tuberosum L.	Rpi-snk1.1	http://edepot.wur.nl/138175
Avrblb1 (Syn. IPI-O/PexRD)	Phytophthora infestans	Solanum tuberosum L.	Rpi-sto1	https://www.ncbi.nlm.nih.gov/pubmed/18682852
Avrvnt1	Phytophthora infestans	Solanum tuberosum L.	Rpi-vnt1.1	http://apsjournals.apsnet.org/doi/abs/10.1094/MPMI-22-5-0601
AvrRpm1, AvrB	Pseudomonas syringae	Arabidopsis thaliana	RPM1	http://www.ncbi.nlm.nih.gov/pubmed/1477552
ATR13-Emco5	Hyaloperonospora arabidopsidis	Arabidopsis thaliana	RPP13-Nd-1	https://www.ncbi.nlm.nih.gov/pubmed/15591208
Not identification	Hyaloperonospora arabidopsidis	Arabidopsis thaliana	RPP13-Rld-2	https://www.ncbi.nlm.nih.gov/pubmed/10743658
ATR13-Maks9	Hyaloperonospora arabidopsidis	Arabidopsis thaliana	RPP13-UKID34	https://www.ncbi.nlm.nih.gov/pubmed/19523099
ATR13-Emco5	Hyaloperonospora arabidopsidis	Arabidopsis thaliana	RPP13-UKID37	https://www.ncbi.nlm.nih.gov/pubmed/19523099
Atr1Ndwsb	Hyaloperonospora arabidopsidis	Arabidopsis thaliana	RPP1-EstA	https://www.ncbi.nlm.nih.gov/pubmed/26725254
Atr1Ndwsb	Hyaloperonospora arabidopsidis	Arabidopsis thaliana	Rpp1Nda	https://www.ncbi.nlm.nih.gov/pubmed/15894715/
Not identification	Hyaloperonospora arabidopsidis	Arabidopsis thaliana	Rpp1-Wsa	https://www.ncbi.nlm.nih.gov/pubmed/9811793/
Atr1Ndwsb	Hyaloperonospora arabidopsidis	Arabidopsis thaliana	Rpp1-Wsb	https://www.ncbi.nlm.nih.gov/pubmed/15894715/
Not identification	Hyaloperonospora arabidopsidis	Arabidopsis thaliana	Rpp1-Wsc	https://www.ncbi.nlm.nih.gov/pubmed/9811793/
Atr1Ndwsb	Hyaloperonospora arabidopsidis	Arabidopsis thaliana	RPP1-ZdrA	https://www.ncbi.nlm.nih.gov/pubmed/26725254
Not identification	Phakopsora pachyrhizi	Glycine max	Rpp4C4	http://www.plantphysiol.org/content/150/1/295.long
AvrRpt2	Phytophthora sojae	Glycine max	Rps1k-1 and/or Rps1k-2	https://www.ncbi.nlm.nih.gov/pubmed/23530601
AvrRpt2	Pseudomonas syringae	Arabidopsis thaliana	RPS2	http://onlinelibrary.wiley.com/doi/10.1111/j.1365-313X.2008.03716.x/abstract
AvrPphB	Pseudomonas syringae	Arabidopsis thaliana	RPS5	http://science.sciencemag.org/content/351/6274/684.full
HopA1 (hrmA/hopPsyA)	Pseudomonas syringae	Arabidopsis thaliana	RPS6	http://www.plantphysiol.org/content/150/4/1723.long
Not identification	Erysiphe cichoracearum (Syn. Golovinomyces cichoracearum)	Arabidopsis thaliana	Rpw8.1	http://www.plantcell.org/content/25/10/4242.long
Not identification	Erysiphe cichoracearum (Syn. Golovinomyces cichoracearum)	Arabidopsis thaliana	Rpw8.2	https://www.ncbi.nlm.nih.gov/pubmed/11141561
AvrRps4 (Syn. AvrPpiE)	Pseudomonas syringae	Arabidopsis thaliana	RRS1B	http://www.ncbi.nlm.nih.gov/pubmed/25744164?dopt=Abstract
AvrRps4 (Syn. AvrPpiE)	Pseudomonas syringae	Arabidopsis thaliana	RRS1-S	http://www.ncbi.nlm.nih.gov/pubmed/19519800
Not identification	Xanthomonas campestris	Arabidopsis thaliana	RRS1ws-0	http://www.ncbi.nlm.nih.gov/pubmed/26212639
Not identification	Striga gesnerioides	Pisum sativum L.	RSG3-301	https://www.ncbi.nlm.nih.gov/pubmed?cmd=Search&doptcmdl=Citation&defaultField=Title%20Word&term=Li%5Bauthor%5D%20AND%20Gene-for-gene%20resistance%20in%20Striga-cowpea%20associations
Not identification	Tobacco Etch Virus	Arabidopsis thaliana	Rtm3	https://www.ncbi.nlm.nih.gov/pubmed/20584941/
Not identification	Golovinomyces cichoracearum	Arabidopsis thaliana	RTP1	http://onlinelibrary.wiley.com/doi/10.1111/nph.13707/abstract?campaign=wolearlyview
Not identification	Watermelon Mosaic Virus	Arabidopsis thaliana	rwm1	http://www.ncbi.nlm.nih.gov/pubmed/24930633
Coat protein	Potato virus X (PVX)	Solanum tuberosum L.	Rx1	https://www.ncbi.nlm.nih.gov/pubmed/17526750
AvrRxo1-ORF1	Xanthomonas oryzae	Zea mays	Rxo1	http://www.pnas.org/content/102/43/15383
Not identification	Barley yellow mosaic virus	Hordeum vulgare	Rym-4	http://www.ncbi.nlm.nih.gov/pubmed/20565670
Not identification	Beet Necrotic Yellow Vein Virus (BNYVV)	Beta vulgaris L.	Rz2	https://www.ncbi.nlm.nih.gov/pubmed/28585529
Not identification	Bean yellow mosaic virus	Pisum sativum L.	sbm1 (Syn. wlv/cyv2)	http://www.ncbi.nlm.nih.gov/pubmed/17849710
Not identification	Heterodera glycines	Glycine max	SHMT (Syn. Rhg4)	http://www.nature.com/nature/journal/v492/n7428/full/nature11651.html?WT.ec_id=NATURE-20121213
Not identification	Pepper mottle virus	Solanum lycopersicum	SleIF4E1-G1485A	http://www.ncbi.nlm.nih.gov/pubmed/20593023
Putative PGN	Pseudomonas syringae	Solanum lycopersicum	SlLyk13	http://onlinelibrary.wiley.com/doi/10.1111/j.1365-313X.2011.04773.x/full
SnTox1	Stagonospora nodorum	Triticum aestivum	Snn1 (Syn. TaWAK1)	https://www.ncbi.nlm.nih.gov/pubmed/27819043
Not identification	Puccinia graminis	Triticum aestivum	Sr22	https://www.ncbi.nlm.nih.gov/pubmed/27111722
Not identification	Puccinia graminis	Triticum aestivum	Sr33 (Syn. Rga1e)	http://science.sciencemag.org/content/341/6147/786.long
Not identification	Puccinia graminis	Triticum aestivum	Sr35	http://science.sciencemag.org/content/341/6147/783.long
Not identification	Puccinia graminis	Triticum aestivum	Sr45	https://www.ncbi.nlm.nih.gov/pubmed/27111722
Not identification	Puccinia graminis	Triticum aestivum	Sr50 (Syn. ScRGA1-A/SrR)	http://www.nature.com/articles/nplants2015186?WT.ec_id=NPLANTS-201512&spMailingID=50148885&spUserID=OTA4NzM2NzAyNDgS1&spJobID=820156687&spReportId=ODIwMTU2Njg3S0
FoAve1	Fusarium oxysporum	Solanum melongena L.	StoVe1	http://onlinelibrary.wiley.com/doi/10.1111/mpp.12390/full
Not identification	Blumeria graminis	Triticum aestivum	Stpk-V (Pm21)	http://www.pnas.org/content/108/19/7727.long
CbAve1	Cercospora beticola	Solanum tuberosum L.	StuVe1	http://onlinelibrary.wiley.com/doi/10.1111/mpp.12390/full
Not identification	Rice Stripe Virus	Oryza sativa L.	STV11-R	http://www.ncbi.nlm.nih.gov/pubmed/?term=STV11+encodes+a+sulphotransferase+and+confers+durable+resistance+to+rice+stripe+virus
HopAI1	Pseudomonas syringae	Arabidopsis thaliana	SUMM2	https://www.ncbi.nlm.nih.gov/pubmed/27986791
Nsm	Tomato spotted wilt virus	Solanum lycopersicum	Sw-5b	https://www.ncbi.nlm.nih.gov/pubmed/28814646
Not identification	Blumeria graminis	Triticum aestivum	Taedr1	http://onlinelibrary.wiley.com/doi/10.1111/tpj.13599/abstract?campaign=woletoc
AvrB	Pseudomonas savastanoi	Arabidopsis thaliana	Tao1	http://www.ncbi.nlm.nih.gov/pubmed/18424557
Not identification	Sclerotinia sclerotiorum	Solanum lycopersicum	TcBI-1	http://onlinelibrary.wiley.com/doi/10.1111/mpp.12463/abstract?campaign=woletoc
RNA-dependent RNA polymerase	Tomato Mosaic Virus (ToMV)	Solanum lycopersicum	Tm-1	http://www.ncbi.nlm.nih.gov/pubmed/17699618
Movement protein	Tobacco mosaic virus (TMV)	Solanum lycopersicum	Tm-2	http://www.ncbi.nlm.nih.gov/pubmed/16172136
Not identification	Bemisia tabaci	Gossypium spp.	Tma12	http://www.nature.com/nbt/journal/v34/n10/full/nbt.3665.html
Not identification	Blumeria graminis	Triticum aestivum	TmMLA1	http://onlinelibrary.wiley.com/doi/10.1111/j.1365-313X.2010.04445.x/full
Not identification	Pseudomonas syringae	Arabidopsis thaliana	TN13	https://www.ncbi.nlm.nih.gov/pubmed/28901644
Not identification	-	Arabidopsis thaliana	TN2,TN1,SOC3	http://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1004945
ToxA	Stagonospora nodorum	Triticum aestivum	Tsn1	https://www.ncbi.nlm.nih.gov/pubmed/20624958
NSs	Tomato spotted wilt virus	Nicotiana benthamiana	Tsw	https://www.ncbi.nlm.nih.gov/pubmed/27612097
Not identification	Tomato yellow leaf curl virus	Solanum lycopersicum	Ty-1	http://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1003399
Not identification	Aphis gossypii	Cucumis melo L.	VAT	http://onlinelibrary.wiley.com/doi/10.1111/tpj.12690/abstract
CbAve1	Cercospora beticola	Solanum lycopersicum	Ve1	http://www.pnas.org/content/109/13/5110
Not identification	Callosobruchus chinensis	Leguminosae spp.	VrPGIP2	https://link.springer.com/article/10.1007/s00122-016-2731-1
Not identification	Puccinia striiformis	Triticum aestivum	WCBP1 (Syn. YrL693)	http://bmcplantbiol.biomedcentral.com/articles/10.1186/s12870-015-0612-4
Not identification	Puccinia striiformis	Triticum aestivum	WKS1 (syn. Yr36 )	http://science.sciencemag.org/content/323/5919/1357?ijkey=9152616eb796132f01bc722808278438b2337fdd&keytype2=tf_ipsecsha
Tal3a mutant (containing full C-terminus)	Xanthomonas oryzae	Oryza sativa L.	Xa1	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5097170/
AvrXa10	Xanthomonas oryzae	Oryza sativa L.	Xa10	http://www.plantcell.org/content/26/1/497.long
AvrXa10	Xanthomonas oryzae	Oryza sativa L.	Xa10E5	http://onlinelibrary.wiley.com/doi/10.1111/pbi.12342/full
PthXo1	Xanthomonas oryzae	Oryza sativa L.	xa13	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1472899/
RaxX; RaxX21-sY	Xanthomonas oryzae	Oryza sativa L.	XA21	http://advances.sciencemag.org/content/1/6/e1500245
AvrXa23	Xanthomonas oryzae	Oryza sativa L.	Xa23	http://www.sciencedirect.com/science/article/pii/S1674205214000306
Not identification	Xanthomonas oryzae	Oryza sativa L.	xa25	http://onlinelibrary.wiley.com/doi/10.1111/j.1365-3040.2011.02391.x/abstract
AvrXa27	Xanthomonas oryzae	Oryza sativa L.	Xa27	http://www.nature.com/nature/journal/v435/n7045/full/nature03630.html
Not identification	Xanthomonas oryzae	Oryza sativa L.	Xa4	http://www.nature.com/articles/nplants20179?WT.ec_id=NPLANTS-201703&spMailingID=53544637&spUserID=OTA4NzM2NzAyNDgS1&spJobID=1120508217&spReportId=MTEyMDUwODIxNwS2
Not identification	Xanthomonas oryzae	Oryza sativa L.	xa5	https://www.ncbi.nlm.nih.gov/pubmed/15597740
Not identification	Potato virus Y (PVY)	Solanum tuberosum L.	Y-1	http://www.ncbi.nlm.nih.gov/pubmed/12118888
Not identification	Puccinia striiformis	Triticum aestivum	Yr10	http://www.sciencedirect.com/science/article/pii/S1674205214609795
HopZ1a (Syn. HopPsyH)	Pseudomonas syringae	Arabidopsis thaliana	ZAR1	http://www.pnas.org/content/110/46/18722.abstract
Not identification	Sugarcane Mosaic Virus	Zea mays	ZmTrxh (Syn. Scmv1)	https://www.ncbi.nlm.nih.gov/pubmed/28216424
Not identification	Sphacelotheca reiliana	Zea mays	ZmWAK1 (Syn. qHSR1)	https://www.ncbi.nlm.nih.gov/pubmed/25531751

Supplementary Table 1

References 47

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