1932

Abstract

Focusing on the discovery and characterization of the disease resistance protein RPS5 and its guardee PBS1, this review discusses work done in the Innes laboratory from the initial identification of the gene in 1995 to the recent deployment of the PBS1 decoy system in crops. This is done through discussion of the structure, function, and signaling environment of RPS5 and PBS1, highlighting collaborations and influential ideas along the way. RPS5, a nucleotide-binding leucine-rich repeat (NLR) protein, is activated by the proteolytic cleavage of PBS1. We have shown that the cleavage site within PBS1 can be altered to contain cleavage sites for other proteases, enabling RPS5 activation by these proteases, thereby conferring resistance to different pathogens. This decoy approach has since been translated into crop species using endogenous PBS1 orthologs and holds strong potential for GMO-free development of new genetic resistance against important crop pathogens.

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2020-08-25
2024-06-13
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Literature Cited

  1. 1.
    Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE 1998. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. . Plant Biol 95:1710306–11
    [Google Scholar]
  2. 2.
    Adachi H, Contreras MP, Harant A, Wu C, Derevnina L et al. 2019. An N-terminal motif in NLR immune receptors is functionally conserved across distantly related plant species. eLife 8:e49956
    [Google Scholar]
  3. 3.
    Ade J, DeYoung BJ, Golstein C, Innes RW 2007. Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease. PNAS 104:72531–36
    [Google Scholar]
  4. 4.
    Albers P, Üstün S, Witzel K, Kraner M, Börnke F 2019. A remorin from Nicotiana benthamiana interacts with the Pseudomonas type-III effector protein HopZ1a and is phosphorylated by the immune-related kinase PBS1. Mol. Plant-Microbe Interact. 32:91229–42
    [Google Scholar]
  5. 5.
    Alfano JR, Collmer A. 2004. Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu. Rev. Phytopathol. 42:385–414
    [Google Scholar]
  6. 6.
    Arora S, Steuernagel B, Gaurav K, Chandramohan S, Long Y et al. 2019. Resistance gene cloning from a wild crop relative by sequence capture and association genetics. Nat. Biotechnol. 37:2139–43
    [Google Scholar]
  7. 7.
    Baudin M, Hassan JA, Schreiber KJ, Lewis JD 2017. Analysis of the ZAR1 immune complex reveals determinants for immunity and molecular interactions. Plant Physiol 174:42038–53
    [Google Scholar]
  8. 8.
    Białas A, Zess EK, De La Concepcion JC, Franceschetti M, Pennington HG et al. 2018. Lessons in effector and NLR biology of plant-microbe systems. Mol. Plant-Microbe Interact. 31:134–45
    [Google Scholar]
  9. 9.
    Bisgrove SR, Simonich MT, Smith NM, Sattler A, Innes RW 1994. A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6:7927–33
    [Google Scholar]
  10. 10.
    Boccara M, Sarazin A, Thiébeauld O, Jay F, Voinnet O et al. 2014. The Arabidopsis miR472-RDR6 silencing pathway modulates PAMP- and effector-triggered immunity through the post-transcriptional control of disease resistance genes. PLOS Pathog 10:1e1003883
    [Google Scholar]
  11. 11.
    Boisson B, Giglione C, Meinnel T 2003. Unexpected protein families including cell defense components feature in the N-myristoylome of a higher eukaryote. J. Biol. Chem. 278:4443418–29
    [Google Scholar]
  12. 12.
    Branon TC, Bosch JA, Sanchez AD, Udeshi ND, Svinkina T et al. 2018. Efficient proximity labeling in living cells and organisms with TurboID. Nat. Biotechnol. 36:9880–87
    [Google Scholar]
  13. 13.
    Burdon JJ, Barrett LG, Rebetzke G, Thrall PH 2014. Guiding deployment of resistance in cereals using evolutionary principles. Evol. Appl. 7:6609–24
    [Google Scholar]
  14. 14.
    Caldwell KS, Michelmore RW. 2009. Arabidopsis thaliana genes encoding defense signaling and recognition proteins exhibit contrasting evolutionary dynamics. Genetics 181:2671–84
    [Google Scholar]
  15. 15.
    Caplan J, Padmanabhan M, Dinesh-Kumar SP 2008. Plant NB-LRR immune receptors: from recognition to transcriptional reprogramming. Cell Host Microbe 3:3126–35
    [Google Scholar]
  16. 16.
    Carter ME, Helm M, Chapman AVE, Wan E, Restrepo Sierra AM et al. 2019. Convergent evolution of effector protease recognition by Arabidopsis and barley. Mol. Plant-Microbe Interact. 32:5550–65
    [Google Scholar]
  17. 17.
    Casey LW, Lavrencic P, Bentham AR, Cesari S, Ericsson DJ et al. 2016. The CC domain structure from the wheat stem rust resistance protein Sr33 challenges paradigms for dimerization in plant NLR proteins. PNAS 113:4512856–61
    [Google Scholar]
  18. 18.
    Chisholm ST, Dahlbeck D, Krishnamurthy N, Day B, Sjolander K, Staskawicz BJ 2005. Molecular characterization of proteolytic cleavage sites of the Pseudomonas syringae effector AvrRpt2. PNAS 102:62087–92
    [Google Scholar]
  19. 19.
    Cotton S, Grangeon R, Thivierge K, Mathieu I, Ide C et al. 2009. Turnip mosaic virus RNA replication complex vesicles are mobile, align with microfilaments, and are each derived from a single viral genome. J. Virol. 83:2010460–71
    [Google Scholar]
  20. 20.
    Cui H, Tsuda K, Parker JE 2015. Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66:487–511
    [Google Scholar]
  21. 21.
    Dangl JL, Jones JD. 2001. Plant pathogens and integrated defence responses to infection. Nature 411:6839826–33
    [Google Scholar]
  22. 22.
    Danot O, Marquenet E, Vidal-Ingigliardi D, Richet E 2009. Wheel of life, wheel of death: a mechanistic insight into signaling by STAND proteins. Structure 17:2172–82
    [Google Scholar]
  23. 23.
    De la Concepcion JC, Franceschetti M, MacLean D, Terauchi R, Kamoun S, Banfield MJ 2019. Protein engineering expands the effector recognition profile of a rice NLR immune receptor. eLife 8:e47713
    [Google Scholar]
  24. 24.
    De la Concepcion JC, Franceschetti M, Maqbool A, Saitoh H, Terauchi R et al. 2018. Polymorphic residues in rice NLRs expand binding and response to effectors of the blast pathogen. Nat. Plants 4:8576–85
    [Google Scholar]
  25. 25.
    DeYoung BJ, Qi D, Kim S-H, Burke TP, Innes RW 2012. Activation of a plant nucleotide binding-leucine rich repeat disease resistance protein by a modified self protein. Cell. Microbiol. 14:71071–84
    [Google Scholar]
  26. 26.
    El Kasmi F, Chung E-H, Anderson RG, Li J, Wan L et al. 2017. Signaling from the plasma-membrane localized plant immune receptor RPM1 requires self-association of the full-length protein. PNAS 114:35E7385–94
    [Google Scholar]
  27. 27.
    El Kasmi F, Nishimura MT 2016. Structural insights into plant NLR immune receptor function. PNAS 113:4512619–21
    [Google Scholar]
  28. 28.
    Engelhardt S, Boevink PC, Armstrong MR, Ramos MB, Hein I, Birch PRJ 2013. Relocalization of late blight resistance protein R3a to endosomal compartments is associated with effector recognition and required for the immune response. Plant Cell 24:125142–58
    [Google Scholar]
  29. 29.
    Ercolano MR, Sanseverino W, Carli P, Ferriello F, Frusciante L 2012. Genetic and genomic approaches for R-gene mediated disease resistance in tomato: retrospects and prospects. Plant Cell Rep 31:6973–85
    [Google Scholar]
  30. 30.
    Flor HH. 1956. The complementary genic systems in flax and flax rust. Adv. Genet. 8:29–54
    [Google Scholar]
  31. 31.
    Flor HH. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275–96
    [Google Scholar]
  32. 32.
    Gao Z, Chung E-H, Eitas TK, Dangl JL 2011. Plant intracellular innate immune receptor Resistance to Pseudomonas syringae pv. maculicola 1 (RPM1) is activated at, and functions on, the plasma membrane. PNAS 108:187619–24
    [Google Scholar]
  33. 33.
    Gardner M, Dhroso A, Johnson N, Davis EL, Baum TJ et al. 2018. Novel global effector mining from the transcriptome of early life stages of the soybean cyst nematode Heterodera glycines. Sci. . Rep 8:12505
    [Google Scholar]
  34. 34.
    Gómez-Gómez L, Boller T. 2000. FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. . Cell 5:61003–11
    [Google Scholar]
  35. 35.
    Grangeon R, Agbeci M, Chen J, Grondin G, Zheng H, Laliberte J-F 2012. Impact on the endoplasmic reticulum and Golgi apparatus of turnip mosaic virus infection. J. Virol. 86:179255–65
    [Google Scholar]
  36. 36.
    Grangeon R, Jiang J, Wan J, Agbeci M, Zheng H, Laliberté J-F 2013. 6K2-induced vesicles can move cell to cell during turnip mosaic virus infection. Front. Microbiol. 4:351
    [Google Scholar]
  37. 37.
    Grant M, Brown I, Adams S, Knight M, Ainslie A, Mansfield J 2000. The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J 23:4441–50
    [Google Scholar]
  38. 38.
    Hao W, Collier SM, Moffett P, Chai J 2013. Structural basis for the interaction between the potato virus X resistance protein (Rx) and its cofactor Ran GTPase-activating protein 2 (RanGAP2). J. Biol. Chem. 288:5035868–76
    [Google Scholar]
  39. 39.
    Helm M, Qi M, Sarkar S, Yu H, Whitham SA, Innes RW 2019. Engineering a decoy substrate in soybean to enable recognition of the soybean mosaic virus NIa protease. Mol. Plant-Microbe Interact. 32:6760–69
    [Google Scholar]
  40. 40.
    Hu Z, Zhou Q, Zhang C, Fan S, Cheng W et al. 2015. Structural and biochemical basis for induced self-propagation of NLRC4. Science 350:6259399–404
    [Google Scholar]
  41. 41.
    Hundleby PAC, Harwood WA. 2019. Impacts of the EU GMO regulatory framework for plant genome editing. Food Energy Secur 8:2e00161
    [Google Scholar]
  42. 42.
    Innes RW, Bisgrove SR, Smith NM, Bent AF, Staskawicz BJ, Liu YC 1993. Identification of a disease resistance locus in Arabidopsis that is functionally homologous to the RPG1 locus of soybean. Plant J 4:5813–20
    [Google Scholar]
  43. 43.
    Jagadeeswaran G, Raina S, Acharya BR, Maqbool SB, Mosher SL et al. 2007. Arabidopsis GH3-LIKE DEFENSE GENE 1 is required for accumulation of salicylic acid, activation of defense responses and resistance to Pseudomonas syringae. . Plant J 51:2234–46
    [Google Scholar]
  44. 44.
    Jenner C, Hitchin E, Mansfield J, Walters K, Betteridge P et al. 1991. Gene-for-gene interactions between Pseudomonas syringae pv. phaseolicola and phaseolus. Mol. Plant-Microbe Interact 4:6553–62
    [Google Scholar]
  45. 45.
    Jin H, Axtell MJ, Dahlbeck D, Ekwenna O, Zhang S et al. 2002. NPK1, and MEKK1-like mitogen-activated protein kinase kinase kinase, regulates innate immunity and development in plants. Dev. Cell 3:2291–97
    [Google Scholar]
  46. 46.
    Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:7117323–29
    [Google Scholar]
  47. 47.
    Jones JDG, Vance RE, Dangl JL 2016. Intracellular innate immune surveillance devices in plants and animals. Science 354:6316aaf6395
    [Google Scholar]
  48. 48.
    Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N et al. 2006. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. PNAS 103:2911086–91
    [Google Scholar]
  49. 49.
    Keen NT, Ersek T, Long M, Bruegger B, Holliday M 1981. Inhibition of the hypersensitive reaction of soybean leaves to incompatible Pseudomonas spp. by blasticidin S, streptomycin or elevated temperature. Physiol. Plant Pathol. 18:3325–37
    [Google Scholar]
  50. 50.
    Khan M, Subramaniam R, Desveaux D 2016. Of guards, decoys, baits and traps: pathogen perception in plants by type III effector sensors. Curr. Opin. Microbiol. 29:49–55
    [Google Scholar]
  51. 51.
    Kim SH, Qi D, Ashfield T, Helm M, Innes RW 2016. Using decoys to expand the recognition specificity of a plant disease resistance protein. Science 351:6274684–87
    [Google Scholar]
  52. 52.
    Klaubauf S, Tharreau D, Fournier E, Groenewald JZ, Crous PW et al. 2014. Resolving the polyphyletic nature of Pyricularia (Pyriculariaceae). Stud. Mycol. 79:185–120
    [Google Scholar]
  53. 53.
    Knepper C, Savory EA, Day B 2011. Arabidopsis NDR1 is an integrin-like protein with a role in fluid loss and plasma membrane-cell wall adhesion. Plant Physiol 156:1286–300
    [Google Scholar]
  54. 54.
    Kunkel BN, Bent AF, Dahlbeck D, Innes RW, Staskawicz BJ 2007. RPS2, an Arabidopsis disease resistance locus specifying recognition of Pseudomonas syringae strains expressing the avirulence gene avrRpt2. . Plant Cell 5:8865–75
    [Google Scholar]
  55. 55.
    Leipe DD, Koonin EV, Aravind L 2004. STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer. J. Mol. Biol. 343:11–28
    [Google Scholar]
  56. 56.
    Liang X, Zhou J-M. 2018. Receptor-like cytoplasmic kinases: central players in plant receptor kinase-mediated signaling. Annu. Rev. Plant Biol. 69:267–99
    [Google Scholar]
  57. 57.
    Lim HS, Jang C-Y, Bae H-H, Kim J, Lee CH et al. 2011. Soybean mosaic virus infection and helper component-protease enhance accumulation of Bean pod mottle virus-specific siRNAs. Plant Pathol. J. 27:4315–23
    [Google Scholar]
  58. 58.
    Lo Presti L, Lanver D, Schweizer G, Tanaka S, Liang L et al. 2015. Fungal effectors and plant susceptibility. Annu. Rev. Plant Biol. 66:513–45
    [Google Scholar]
  59. 59.
    Lu M, Tang X, Zhou J-M 2001. Arabidopsis NHO1 is required for general resistance against Pseudomonas bacteria. Plant Cell 13:2437–47
    [Google Scholar]
  60. 60.
    MacLean AM, Orlovskis Z, Kowitwanich K, Zdziarska AM, Angenent GC et al. 2014. Phytoplasma effector SAP54 hijacks plant reproduction by degrading MADS-box proteins and promotes insect colonization in a RAD23-dependent manner. PLOS Biol 12:41001835
    [Google Scholar]
  61. 61.
    Maekawa T, Cheng W, Spiridon LN, Töller A, Lukasik E et al. 2011. Coiled-coil domain-dependent homodimerization of intracellular barley immune receptors defines a minimal functional module for triggering cell death. Cell Host Microbe 9:3187–99
    [Google Scholar]
  62. 62.
    Maqbool A, Saitoh H, Franceschetti M, Stevenson C, Uemura A et al. 2015. Structural basis of pathogen recognition by an integrated HMA domain in a plant NLR immune receptor. eLife 4:e08709
    [Google Scholar]
  63. 63.
    McDowell JM, Simon SA. 2006. Recent insights into R gene evolution. Mol. Plant Pathol. 7:5437–48
    [Google Scholar]
  64. 64.
    Morel JB, Dangl JL. 1997. The hypersensitive response and the induction of cell death in plants. Cell Death Differ 4:8671–83
    [Google Scholar]
  65. 65.
    Mur LAJ, Kenton P, Lloyd AJ, Ougham H, Prats E 2008. The hypersensitive response; the centenary is upon us but how much do we know. J. Exp. Bot. 59:3501–20
    [Google Scholar]
  66. 66.
    Muskett PR. 2002. Arabidopsis RAR1 exerts rate-limiting control of R gene-mediated defenses against multiple pathogens. Plant Cell 14:5979–92
    [Google Scholar]
  67. 67.
    Narusaka M, Kubo Y, Hatakeyama K, Imamura J, Ezura H et al. 2013. Breaking restricted taxonomic functionality by dual resistance genes. Plant Signal. Behav. 8:6e24244
    [Google Scholar]
  68. 68.
    Ng JCK, Perry KL. 2004. Transmission of plant viruses by aphid vectors. Mol. Plant Pathol. 5:5505–11
    [Google Scholar]
  69. 69.
    Nimchuk Z, Marois E, Kjemtrup S, Leister RT, Katagiri F, Dangl JL 2000. Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several type III effector proteins from Pseudomonas syringae. . Cell 101:4353–63
    [Google Scholar]
  70. 70.
    Nolen B, Taylor S, Ghosh G 2004. Regulation of protein kinases: controlling activity through activation segment conformation. Mol. Cell 15:5661–75
    [Google Scholar]
  71. 71.
    Porter K, Shimono M, Tian M, Day B 2012. Arabidopsis actin-depolymerizing factor-4 links pathogen perception, defense activation and transcription to cytoskeletal dynamics. PLOS Pathog 8:11e1003006
    [Google Scholar]
  72. 72.
    Pottinger SE, Bak A, Margets A, Helm M, Tang Let al. 2020. Optimizing the PBS1 decoy system to confer resistance to potyvirus infection in Arabidopsis and soybean. Mol. Plant-Microbe Int 33:793244
    [Google Scholar]
  73. 73.
    Qi D, DeYoung BJ, Innes RW 2012. Structure-function analysis of the coiled-coil and leucine-rich repeat domains of the RPS5 disease resistance protein. Plant Physiol 158:41819–32
    [Google Scholar]
  74. 74.
    Qi D, Dubiella U, Kim SH, Sloss DI, Dowen RH et al. 2014. Recognition of the protein kinase AVRPPHB SUSCEPTIBLE1 by the disease resistance protein RESISTANCE TO PSEUDOMONAS SYRINGAE5 is dependent on S-acylation and an exposed loop in AVRPPHB SUSCEPTIBLE1. Plant Physiol 164:1340–51
    [Google Scholar]
  75. 75.
    Raffaele S, Win J, Cano LM, Kamoun S 2010. Analysis of genome architecture and gene expression reveal novel candidate virulence factors in the secretome of Phytophthora infestans. . BMC Genom 11:1637
    [Google Scholar]
  76. 76.
    Rao S, Zhou Z, Miao P, Bi G, Hu M et al. 2018. Roles of receptor-like cytoplasmic kinase VII members in pattern-triggered immune signaling. Plant Physiol 177:41679–90
    [Google Scholar]
  77. 77.
    Rekhter D, Lüdke D, Ding Y, Feussner K, Zienkiewicz K et al. 2019. Isochorismate-derived biosynthesis of the plant stress hormone salicylic acid. Science 365:6452498–502
    [Google Scholar]
  78. 78.
    Ritter C, Dangl JL. 1995. The avrRpm1 gene of Pseudomonas syringae pv. maculicola is required for virulence on Arabidopsis. Mol. . Plant-Microbe Interact 8:3444–53
    [Google Scholar]
  79. 79.
    Ruiz MT, Voinnet O, Baulcombe DC 1998. Initiation and maintenance of virus-induced gene silencing. Plant Cell 10:6937–46
    [Google Scholar]
  80. 80.
    Sali A, Blundell T. 1994. Comparative modelling by satisfaction of spatial restraints. J. Mol. Biol. 234:3779–815
    [Google Scholar]
  81. 81.
    Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW 2003. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301:56371230–33
    [Google Scholar]
  82. 82.
    Shao F, Merritt PM, Bao Z, Innes RW, Dixon JE 2002. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109:5575–88
    [Google Scholar]
  83. 83.
    Shinya T, Yamaguchi K, Desaki Y, Yamada K, Narisawa T et al. 2014. Selective regulation of the chitin-induced defense response by the Arabidopsis receptor-like cytoplasmic kinase PBL27. Plant J 79:156–66
    [Google Scholar]
  84. 84.
    Simonich MT, Innes RW. 1995. A disease resistance gene in Arabidopsis with specificity for the avrPph3 gene of Pseudomonas syringae pv. phaseolicola. Mol. Plant-Microbe Interact. 8:4637–40
    [Google Scholar]
  85. 85.
    Sun J, Huang G, Fan F, Wang S, Zhang Y et al. 2017. Comparative study of Arabidopsis PBS1 and a wheat PBS1 homolog helps understand the mechanism of PBS1 functioning in innate immunity. Sci. Rep. 7:15487
    [Google Scholar]
  86. 86.
    Sung YK, Valencia M, Eui SL, Park D, Oh M et al. 2004. Identification of CED-3 substrates by a yeast-based screening method. Appl. Biochem. Biotechnol. 27:11–6
    [Google Scholar]
  87. 87.
    Swiderski MR, Innes RW. 2001. The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. Plant J 26:1101–12
    [Google Scholar]
  88. 88.
    Tai TH, Dahlbeck D, Clark ET, Gajiwala P, Pasion R et al. 1999. Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. PNAS 96:2414153–58
    [Google Scholar]
  89. 89.
    Takemoto D, Rafiqi M, Hurley U, Lawrence GJ, Bernoux M et al. 2012. N-Terminal motifs in some plant disease resistance proteins function in membrane attachment and contribute to disease resistance. Mol. Plant-Microbe Interact. 25:3379–92
    [Google Scholar]
  90. 90.
    Tamaki S, Dahlbeck D, Staskawicz B, Keen NT 1988. Characterization and expression of two avirulence genes cloned from Pseudomonas syringae pv. glycinea. J. Bacteriol. 170:104846–54
    [Google Scholar]
  91. 91.
    Tameling WIL, Elzinga SDJ, Darmin PS, Vossen JH, Takken FLW et al. 2002. The tomato R gene products I-2 and MI-1 are functional ATP binding proteins with ATPase activity. Plant Cell 14:112929–39
    [Google Scholar]
  92. 92.
    Tameling WIL, Vossen JH, Albrecht M, Lengauer T, Berden JA et al. 2006. Mutations in the NB-ARC domain of I-2 that impair ATP hydrolysis cause autoactivation. Plant Physiol 140:41233–45
    [Google Scholar]
  93. 93.
    Tian M, Chaudhry F, Ruzicka DR, Meagher RB, Staiger CJ, Day B 2009. Arabidopsis actin-depolymerizing factor AtADF4 mediates defense signal transduction triggered by the Pseudomonas syringae effector AvrPphB. Plant Physiol 150:2815–24
    [Google Scholar]
  94. 94.
    Tornero P, Chao RA, Luthin WN, Goff SA, Dangl JL 2002. Large-scale structure-function analysis of the Arabidopsis RPM1 disease resistance protein. Plant Cell 14:2435–50
    [Google Scholar]
  95. 95.
    Tran DTNN, Chung E-H, Habring-Müller A, Demar M, Schwab R et al. 2017. Activation of a plant NLR complex through heteromeric association with an autoimmune risk variant of another NLR. Curr. Biol. 27:81148–60
    [Google Scholar]
  96. 96.
    USDA 2018. Secretary Perdue issues USDA statement on plant breeding innovation Press Release, March 28. https://www.usda.gov/media/press-releases/2018/03/28/secretary-perdue-issues-usda-statement-plant-breeding-innovation
    [Google Scholar]
  97. 97.
    Van Der Biezen EA, Jones JDG 1998. Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23:12454–56
    [Google Scholar]
  98. 98.
    Wang J, Hu M, Wang J, Qi J, Han Z et al. 2019. Reconstitution and structure of a plant NLR resistosome conferring immunity. Science 364:6435eaav5870
    [Google Scholar]
  99. 99.
    Wang J, Wang J, Hu M, Wu S, Qi J et al. 2019. Ligand-triggered allosteric ADP release primes a plant NLR complex. Science 364:6435eaav5868
    [Google Scholar]
  100. 100.
    Warren RF, Henk A, Mowery P, Holub E, Innes RW 1998. A mutation within the leucine-rich repeat domain of the Arabidopsis disease resistance gene RPS5 partially suppresses multiple bacterial and downy mildew resistance genes. Plant Cell 10:91439–52
    [Google Scholar]
  101. 101.
    Warren RF, Merritt PM, Holub E, Innes RW 1999. Identification of three putative signal transduction genes involved in R gene–specified disease resistance in Arabidopsis. . Genetics 152:401–12
    [Google Scholar]
  102. 102.
    Whalen MC, Innes RW, Bent AF, Staskawicz BJ 1991. Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell 3:149–59
    [Google Scholar]
  103. 103.
    Yang X, Yang F, Wang W, Lin G, Hu Z et al. 2018. Structural basis for specific flagellin recognition by the NLR protein NAIP5. Cell Res 28:135–47
    [Google Scholar]
  104. 104.
    Zhang J, Li W, Xiang T, Liu Z, Laluk K et al. 2010. Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7:4290–301
    [Google Scholar]
  105. 105.
    Zhang L, Chen S, Ruan J, Wu J, Tong AB et al. 2015. Cryo-EM structure of the activated NAIP2-NLRC4 inflammasome reveals nucleated polymerization. Science 350:6259404–9
    [Google Scholar]
  106. 106.
    Zhang Y, Malzahn AA, Sretenovic S, Qi Y 2019. The emerging and uncultivated potential of CRISPR technology in plant science. Nat. Plants 5:8778–94
    [Google Scholar]
  107. 107.
    Zhu M, Shao F, Innes RW, Dixon JE, Xu Z 2004. The crystal structure of Pseudomonas avirulence protein AvrPphB: a papain-like fold with a distinct substrate-binding site. PNAS 101:1302–7
    [Google Scholar]
  108. 108.
    Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG et al. 2006. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:4749–60
    [Google Scholar]
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