1932

Abstract

Plant diseases reduce crop yields and threaten global food security, making the selection of disease-resistant cultivars a major goal of crop breeding. Broad-spectrum resistance (BSR) is a desirable trait because it confers resistance against more than one pathogen species or against the majority of races or strains of the same pathogen. Many BSR genes have been cloned in plants and have been found to encode pattern recognition receptors, nucleotide-binding and leucine-rich repeat receptors, and defense-signaling and pathogenesis-related proteins. In addition, the BSR genes that underlie quantitative trait loci, loss of susceptibility and nonhost resistance have been characterized. Here, we comprehensively review the advances made in the identification and characterization of BSR genes in various species and examine their application in crop breeding. We also discuss the challenges and their solutions for the use of BSR genes in the breeding of disease-resistant crops.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-010720-022215
2020-04-29
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/arplant/71/1/annurev-arplant-010720-022215.html?itemId=/content/journals/10.1146/annurev-arplant-010720-022215&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Afroz A, Chaudhry Z, Rashid U, Ali GM, Nazir F et al. 2011. Enhanced resistance against bacterial wilt in transgenic tomato (Lycopersicon esculentum) lines expressing the Xa21 gene. Plant Cell Tissue Organ Cult 104:227–37
    [Google Scholar]
  2. 2. 
    Aktar-Uz-Zaman M, Tuhina-Khatun M, Hanafi MM, Sahebi M 2017. Genetic analysis of rust resistance genes in global wheat cultivars: an overview. Biotechnol. Biotechnol. Equip. 31:431–45
    [Google Scholar]
  3. 3. 
    Al-Bader N, Meier A, Geniza M, Gongora YS, Oard J, Jaiswal P 2019. Loss of premature stop codon in the Wall-Associated Kinase 91 (OsWAK91) gene confers sheath blight disease resistance in rice.. bioRxiv 625509. https://doi.org/10.1101/625509
    [Crossref]
  4. 4. 
    Albert I, Böhm H, Albert M, Feiler CE, Imkampe J et al. 2015. An RLP23-SOBIR1-BAK1 complex mediates NLP-triggered immunity. Nat. Plants 1:15140
    [Google Scholar]
  5. 5. 
    Ali F, Yan J. 2012. Disease resistance in maize and the role of molecular breeding in defending against global threat. J. Integr. Plant Biol. 54:134–51
    [Google Scholar]
  6. 6. 
    Andersen EJ, Ali S, Byamukama E, Yen Y, Nepal MP 2018. Disease resistance mechanisms in plants. Genes 9:339
    [Google Scholar]
  7. 7. 
    Asea G, Vivek BS, Lipps PE, Pratt RC 2012. Genetic gain and cost efficiency of marker-assisted selection of maize for improved resistance to multiple foliar pathogens. Mol. Breed. 29:515–27
    [Google Scholar]
  8. 8. 
    Assaad FF, Qiu J, Youngs H, Ehrhardt D, Zimmerli L et al. 2004. The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol. Biol. Cell 15:5118–29
    [Google Scholar]
  9. 9. 
    Belfanti E, Silfverberg-Dilworth E, Tartarini S, Patocchi A, Barbieri M et al. 2004. The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated variety. PNAS 101:886–90
    [Google Scholar]
  10. 10. 
    Birker D, Heidrich K, Takahara H, Narusaka M, Deslandes L et al. 2009. A locus conferring resistance to Colletotrichum higginsianum is shared by four geographically distinct Arabidopsis accessions. Plant J 60:602–13
    [Google Scholar]
  11. 11. 
    Boni R, Chauhan H, Hensel G, Roulin A, Sucher J et al. 2018. Pathogen-inducible Ta-Lr34res expression in heterologous barley confers disease resistance without negative pleiotropic effects. Plant Biotechnol. J. 16:245–53
    [Google Scholar]
  12. 12. 
    Boschi F, Schvartzman C, Murchio S, Ferreira V, Siri MI et al. 2017. Enhanced bacterial wilt resistance in potato through expression of Arabidopsis EFR and introgression of quantitative resistance from Solanum commersonii. Front. Plant Sci 8:1642
    [Google Scholar]
  13. 13. 
    Boutrot F, Zipfel C. 2017. Function, discovery, and exploitation of plant pattern recognition receptors for broad-spectrum disease resistance. Annu. Rev. Phytopathol. 55:257–86
    [Google Scholar]
  14. 14. 
    Brown JKM. 2015. Durable resistance of crops to disease: a Darwinian perspective. Annu. Rev. Phytopathol. 53:513–39
    [Google Scholar]
  15. 15. 
    Brunner S, Stirnweis D, Diaz Quijano C, Buesing G, Herren G et al. 2012. Transgenic Pm3 multilines of wheat show increased powdery mildew resistance in the field. Plant Biotechnol. J. 10:398–409
    [Google Scholar]
  16. 16. 
    Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G 2010. A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. PNAS 107:9452–57
    [Google Scholar]
  17. 17. 
    Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M et al. 1997. The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695–705
    [Google Scholar]
  18. 18. 
    Cao H, Li X, Dong X 1998. Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. PNAS 95:6531–36
    [Google Scholar]
  19. 19. 
    Cao Y, Ding X, Cai M, Zhao J, Lin Y et al. 2007. The expression pattern of a rice disease resistance gene Xa3/Xa26 is differentially regulated by the genetic backgrounds and developmental stages that influence its function. Genetics 177:523–33
    [Google Scholar]
  20. 20. 
    Chandrasekaran J, Brumin M, Wolf D, Leibman D, Klap C et al. 2016. Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Mol. Plant Pathol. 17:1140–53
    [Google Scholar]
  21. 21. 
    Chapman S, Stevens LJ, Boevink PC, Engelhardt S, Alexander CJ et al. 2014. Detection of the virulent form of AVR3a from Phytophthora infestans following artificial evolution of potato resistance gene R3a. PLOS ONE 9:e110158
    [Google Scholar]
  22. 22. 
    Chen X, Lewandowska D, Armstrong MR, Baker K, Lim T et al. 2018. Identification and rapid mapping of a gene conferring broad-spectrum late blight resistance in the diploid potato species Solanum verrucosum through DNA capture technologies. Theor. Appl. Genet. 131:1287–97
    [Google Scholar]
  23. 23. 
    Chen XK, Zhang JY, Zhang Z, Du XL, Du BB, Qu SC 2012. Overexpressing MhNPR1 in transgenic Fuji apples enhances resistance to apple powdery mildew. Mol. Biol. Rep. 39:8083–89
    [Google Scholar]
  24. 24. 
    Cheng YT, Li X. 2012. Ubiquitination in NB-LRR-mediated immunity. Curr. Opin. Plant Biol. 15:392–99
    [Google Scholar]
  25. 25. 
    Chern MS, Fitzgerald HA, Yadav RC, Canlas PE, Dong X, Ronald PC 2001. Evidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis. Plant J 27:101–13
    [Google Scholar]
  26. 26. 
    Chu Z, Fu B, Yang H, Xu C, Li Z et al. 2006. Targeting xa13, a recessive gene for bacterial blight resistance in rice. Theor. Appl. Genet. 112:455–61
    [Google Scholar]
  27. 27. 
    Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E et al. 2003. SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425:973–77
    [Google Scholar]
  28. 28. 
    Cook DE, Lee TG, Guo X, Melito S, Wang K et al. 2012. Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338:1206–9
    [Google Scholar]
  29. 29. 
    Dakouri A, McCallum BD, Radovanovic N, Cloutier S 2013. Molecular and phenotypic characterization of seedling and adult plant leaf rust resistance in a world wheat collection. Mol. Breed. 32:663–77
    [Google Scholar]
  30. 30. 
    Delteil A, Gobbato E, Cayrol B, Estevan J, Michel-Romiti C et al. 2016. Several wall-associated kinases participate positively and negatively in basal defense against rice blast fungus. BMC Plant Biol 16:17
    [Google Scholar]
  31. 31. 
    Deng Y, Zhai K, Xie Z, Yang D, Zhu X et al. 2017. Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science 355:962–65
    [Google Scholar]
  32. 32. 
    Deng-wei J, Min C, Qing Y 2014. Cloning and characterization of a Solanum torvum NPR1 gene involved in regulating plant resistance to Verticillium dahliae. Acta Physiol. Plant 36:2999–3011
    [Google Scholar]
  33. 33. 
    Ding B, Bellizzi MR, Ning Y, Meyers BC, Wang GL 2012. HDT701, a histone H4 deacetylase, negatively regulates plant innate immunity by modulating histone H4 acetylation of defense-related genes in rice. Plant Cell 24:3783–94
    [Google Scholar]
  34. 34. 
    Du J, Verzaux E, Chaparro-Garcia A, Bijsterbosch G, Keizer LC et al. 2015. Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nat. Plants 1:15034
    [Google Scholar]
  35. 35. 
    Ellis JG, Lagudah ES, Spielmeyer W, Dodds PN 2014. The past, present and future of breeding rust resistant wheat. Front. Plant Sci. 5:641
    [Google Scholar]
  36. 36. 
    Eom J-S, Luo D, Atienza-Grande G, Yang J, Ji C et al. 2019. Diagnostic kit for rice blight resistance. Nat. Biotechnol. 37:1372–79
    [Google Scholar]
  37. 37. 
    Farnham G, Baulcombe DC. 2006. Artificial evolution extends the spectrum of viruses that are targeted by a disease-resistance gene from potato. PNAS 103:18828–33
    [Google Scholar]
  38. 38. 
    Deleted in proof
  39. 39. 
    Figueroa M, Hammond Kosack KE, Solomon PS 2018. A review of wheat diseases—a field perspective. Mol. Plant Pathol. 19:1523–36
    [Google Scholar]
  40. 39a. 
    Forsyth A, Mansfield JW, Grabov N, de Torres M, Sinapidou E, Grant MR 2010. Genetic dissection of basal resistance to Pseudomonas syringae pv. phaseolicola in accessions of Arabidopsis. Mol. Plant Microbe Interact 23:154552
    [Google Scholar]
  41. 40. 
    Fu D, Uauy C, Distelfeld A, Blechl A, Epstein L et al. 2009. A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323:1357–60
    [Google Scholar]
  42. 41. 
    Fu ZQ, Yan S, Saleh A, Wang W, Ruble J et al. 2012. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486:228–32
    [Google Scholar]
  43. 42. 
    Fukuoka S, Saka N, Koga H, Ono K, Shimizu T et al. 2009. Loss of function of a proline-containing protein confers durable disease resistance in rice. Science 325:998–1001
    [Google Scholar]
  44. 43. 
    Fukuoka S, Saka N, Mizukami Y, Koga H, Yamanouchi U et al. 2015. Gene pyramiding enhances durable blast disease resistance in rice. Sci. Rep. 5:7773
    [Google Scholar]
  45. 44. 
    Gao Y, Zhang C, Han X, Wang Z, Ma L et al. 2018. Inhibition of OsSWEET11 function in mesophyll cells improves resistance of rice to sheath blight disease. Mol. Plant Pathol. 19:2149–61
    [Google Scholar]
  46. 45. 
    Gaudelli NM, Komor AC, Rees HA, Packer MS, Badran AH et al. 2017. Programmable base editing of A·T to G·C in genomic DNA without DNA cleavage. Nature 551:464–71
    [Google Scholar]
  47. 46. 
    German SE, Kolmer JA. 1992. Effect of gene Lr34 in the enhancement of resistance to leaf rust of wheat. Theor. Appl. Genet. 84:97–105
    [Google Scholar]
  48. 47. 
    Giannakopoulou A, Steele JFC, Segretin ME, Bozkurt TO, Zhou J et al. 2015. Tomato 12 immune receptor can be engineered to confer partial resistance to the oomycete Phytophthora infestans in addition to the fungus Fusarium oxysporum. Mol. Plant-Microbe Interact 28:1316–29
    [Google Scholar]
  49. 48. 
    Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43:205–27
    [Google Scholar]
  50. 48a. 
    Gu K, Yang B, Tian D, Wu L, Wang Det al. 2005. R gene expression induced by a type-III effector triggers disease resistance in rice. Nature 435:112225
    [Google Scholar]
  51. 49. 
    Harkenrider M, Sharma R, De Vleesschauwer D, Tsao L, Zhang X et al. 2016. Overexpression of rice wall-associated kinase 25 (OsWAK25) alters resistance to bacterial and fungal pathogens. PLOS ONE 11:e0147310
    [Google Scholar]
  52. 50. 
    Harris CJ, Slootweg EJ, Goverse A, Baulcombe DC 2013. Stepwise artificial evolution of a plant disease resistance gene. PNAS 110:21189–94
    [Google Scholar]
  53. 51. 
    Haverkort AJ, Boonekamp PM, Hutten R, Jacobsen E, Lotz LAP et al. 2016. Durable late blight resistance in potato through dynamic varieties obtained by cisgenesis: scientific and societal advances in the DuRPh project. Potato Res 59:35–66
    [Google Scholar]
  54. 52. 
    Heath MC. 2000. Nonhost resistance and nonspecific plant defenses. Curr. Opin. Plant Biol. 3:315–19
    [Google Scholar]
  55. 53. 
    Helliwell EE, Wang Q, Yang Y 2013. Transgenic rice with inducible ethylene production exhibits broad-spectrum disease resistance to the fungal pathogens Magnaporthe oryzae and Rhizoctonia solani. Plant Biotechnol. J 11:33–42
    [Google Scholar]
  56. 54. 
    Herrera-Foessel SA, Singh RP, Lillemo M, Huerta-Espino J, Bhavani S et al. 2014. Lr67/Yr46 confers adult plant resistance to stem rust and powdery mildew in wheat. Theor. Appl. Genet. 127:781–89
    [Google Scholar]
  57. 55. 
    Hittalmani S, Parco A, Mew TV, Zeigler RS, Huang N 2000. Fine mapping and DNA marker-assisted pyramiding of the three major genes for blast resistance in rice. Theor. Appl. Genet. 100:1121–28
    [Google Scholar]
  58. 56. 
    Holton N, Nekrasov V, Ronald PC, Zipfel C 2015. The phylogenetically-related pattern recognition receptors EFR and XA21 recruit similar immune signaling components in monocots and dicots. PLOS Pathog 11:e1004602
    [Google Scholar]
  59. 57. 
    Hong Y, Liu Q, Cao Y, Zhang Y, Chen D et al. 2019. The OsMPK15 negatively regulates Magnaporthe oryza and Xoo disease resistance via SA and JA signaling pathway in rice. Front. Plant Sci. 10:752
    [Google Scholar]
  60. 58. 
    Hu K, Cao J, Zhang J, Xia F, Ke Y et al. 2017. Improvement of multiple agronomic traits by a disease resistance gene via cell wall reinforcement. Nat. Plants 3:17009
    [Google Scholar]
  61. 59. 
    Hummel AW, Doyle EL, Bogdanove AJ 2012. Addition of transcription activator-like effector binding sites to a pathogen strain-specific rice bacterial blight resistance gene makes it effective against additional strains and against bacterial leaf streak. New Phytol 195:883–93
    [Google Scholar]
  62. 60. 
    Hurni S, Scheuermann D, Krattinger SG, Kessel B, Wicker T et al. 2015. The maize disease resistance gene Htn1 against northern corn leaf blight encodes a wall-associated receptor-like kinase. PNAS 112:8780–85
    [Google Scholar]
  63. 61. 
    Hutin M, Césari S, Chalvon V, Michel C, Tran TT et al. 2016. Ectopic activation of the rice NLR heteropair RGA4/RGA5 confers resistance to bacterial blight and bacterial leaf streak diseases. Plant J 88:43–55
    [Google Scholar]
  64. 62. 
    Hutin M, Sabot F, Ghesquière A, Koebnik R, Szurek B 2015. A knowledge-based molecular screen uncovers a broad-spectrum OsSWEET14 resistance allele to bacterial blight from wild rice. Plant J 84:694–703
    [Google Scholar]
  65. 63. 
    Ishizaki K, Hoshi T, Abe S, Sasaki Y, Kobayashi K et al. 2005. Breeding of blast resistant isogenic lines in rice variety “Koshihikari” and evaluation of their characters. Breed. Sci. 55:371–77
    [Google Scholar]
  66. 64. 
    Jia Z, Gou J, Sun Y, Yuan L, Tang Q et al. 2010. Enhanced resistance to fungal pathogens in transgenic Populus tomentosa Carr. by overexpression of an nsLTP-like antimicrobial protein gene from motherwort (Leonurus japonicus). Tree Physiol 30:1599–605
    [Google Scholar]
  67. 65. 
    Jiang CJ, Shimono M, Maeda S, Inoue H, Mori M et al. 2009. Suppression of the rice fatty-acid desaturase gene OsSSI2 enhances resistance to blast and leaf blight diseases in rice. Mol. Plant-Microbe Interact. 22:820–29
    [Google Scholar]
  68. 66. 
    Jiang GH, Xia ZH, Zhou YL, Wan J, Li DY et al. 2006. Testifying the rice bacterial blight resistance gene xa5 by genetic complementation and further analyzing xa5 (Xa5) in comparison with its homolog TFIIAγ1. Mol. Genet. Genom 275:354–66
    [Google Scholar]
  69. 67. 
    Jiang H, Feng Y, Bao L, Li X, Gao G et al. 2012. Improving blast resistance of Jin 23B and its hybrid rice by marker-assisted gene pyramiding. Mol. Breed. 30:1679–88
    [Google Scholar]
  70. 68. 
    Jiang JF, Yang DB, Ali J, Mou TM 2015. Molecular marker-assisted pyramiding of broad-spectrum disease resistance genes, Pi2 and Xa23, into GZ63-4S, an elite thermo-sensitive genic male-sterile line in rice. Mol. Breed. 35:83
    [Google Scholar]
  71. 69. 
    Jiang M, Zhang CY, Khalid H, Li N, Sun Q et al. 2012. Pyramiding resistance genes to northern leaf blight and head smut in maize. Int. J. Agric. Biol. 14:430–44
    [Google Scholar]
  72. 70. 
    Jiang R, Li J, Tian Z, Du J, Armstrong M et al. 2018. Potato late blight field resistance from QTL dPI09c is conferred by the NB-LRR gene R8. J. Exp. Bot 69:1545–55
    [Google Scholar]
  73. 71. 
    Jones JD, Dangl JL. 2006. The plant immune system. Nature 444:323–29
    [Google Scholar]
  74. 72. 
    Kang L, Li J, Zhao T, Xiao F, Tang X et al. 2003. Interplay of the Arabidopsis nonhost resistance gene oNHO1 with bacterial virulence. PNAS 100:3519–24
    [Google Scholar]
  75. 73. 
    Kawashima CG, Guimaraes GA, Nogueira SR, MacLean D, Cook DR et al. 2016. A pigeonpea gene confers resistance to Asian soybean rust in soybean. Nat. Biotechnol. 34:661–65
    [Google Scholar]
  76. 74. 
    Keller H, Pamboukdjian N, Ponchet M, Poupet A, Delon R et al. 1999. Pathogen-induced elicitin production in transgenic tobacco generates a hypersensitive response and nonspecific disease resistance. Plant Cell 11:223–35
    [Google Scholar]
  77. 75. 
    Kim MC, Panstruga R, Elliott C, Muller J, Devoto A et al. 2002. Calmodulin interacts with MLO protein to regulate defence against mildew in barley. Nature 416:447–51
    [Google Scholar]
  78. 76. 
    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 351:684–87
    [Google Scholar]
  79. 77. 
    Klymiuk V, Yaniv E, Huang L, Raats D, Fatiukha A et al. 2018. Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family. Nat. Commun. 9:3735
    [Google Scholar]
  80. 78. 
    Koizumi S. 2010. Ecological and genetic studies on durable use of blast resistance in rice. J. Gen. Plant Pathol. 76:406–10
    [Google Scholar]
  81. 79. 
    Koller T, Brunner S, Herren G, Hurni S, Keller B 2018. Pyramiding of transgenic Pm3 alleles in wheat results in improved powdery mildew resistance in the field. Theor. Appl. Genet. 131:861–71
    [Google Scholar]
  82. 80. 
    Kou Y, Wang S. 2010. Broad-spectrum and durability: understanding of quantitative disease resistance. Curr. Opin. Plant Biol. 13:181–85
    [Google Scholar]
  83. 81. 
    Kourelis J, van der Hoorn RAL, Sueldo DJ 2016. Decoy engineering: the next step in resistance breeding. Trends Plant Sci 21:371–73
    [Google Scholar]
  84. 82. 
    Krattinger SG, Lagudah ES, Spielmeyer W, Singh R, Huerta-Espino J et al. 2009. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–63
    [Google Scholar]
  85. 83. 
    Krattinger SG, Sucher J, Selter LL, Chauhan H, Zhou B et al. 2016. The wheat durable, multipathogen resistance gene Lr34 confers partial blast resistance in rice. Plant Biotechnol. J. 14:1261–68
    [Google Scholar]
  86. 84. 
    Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G 2004. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16:3496–507
    [Google Scholar]
  87. 85. 
    Kwon SW, Cho YC, Kim YG, Suh JP, Jeung JU et al. 2008. Development of near-isogenic Japonica rice lines with enhanced resistance to Magnaporthe grisea. Mol. Cell 25:407–16
    [Google Scholar]
  88. 86. 
    Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D et al. 2010. Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat. Biotechnol. 28:365–69
    [Google Scholar]
  89. 87. 
    Lagudah ES, Krattinger SG, Herrera-Foessel SA, Singh RP, Huerta-Espino J et al. 2009. Gene-specific markers for the wheat gene Lr34/Yr18/Pm38 which confers resistance to multiple fungal pathogens. Theor. Appl. Genet. 119:889–98
    [Google Scholar]
  90. 88. 
    Leach JE, Cruz CMV, Bai JF, Leung H 2001. Pathogen fitness penalty as a predictor of durability of disease resistance genes. Annu. Rev. Phytopathol. 39:187–224
    [Google Scholar]
  91. 89. 
    Lee SC, Hwang IS, Choi HW, Hwang BK 2008. Involvement of the pepper antimicrobial protein CaAMP1 gene in broad spectrum disease resistance. Plant Physiol 148:1004–20
    [Google Scholar]
  92. 90. 
    Deleted in proof
  93. 91. 
    Li G, Zhou J, Jia H, Gao Z, Fan M et al. 2019. Mutation of a histidine-rich calcium-binding-protein gene in wheat confers resistance to Fusarium head blight. Nat. Genet. 51:1106–12
    [Google Scholar]
  94. 92. 
    Li S, Shen L, Hu P, Liu Q, Zhu X et al. 2019. Developing disease-resistant thermosensitive male sterile rice by multiplex gene editing. J. Integr. Plant Biol. 61:1201–5
    [Google Scholar]
  95. 93. 
    Li W, Zhong S, Li G, Li Q, Mao B et al. 2011. Rice RING protein OsBBI1 with E3 ligase activity confers broad-spectrum resistance against Magnaporthe oryzae by modifying the cell wall defence. Cell Res 21:835–48
    [Google Scholar]
  96. 94. 
    Li W, Zhu Z, Chern M, Yin J, Yang C et al. 2017. A natural allele of a transcription factor in rice confers broad-spectrum blast resistance. Cell 170:114–26
    [Google Scholar]
  97. 95. 
    Li X, Kapos P, Zhang Y 2015. NLRs in plants. Curr. Opin. Immunol. 32:114–21
    [Google Scholar]
  98. 96. 
    Li Z, Ding B, Zhou X, Wang GL 2017. The rice dynamin-related protein OsDRP1E negatively regulates programmed cell death by controlling the release of cytochrome c from mitochondria. PLOS Pathog 13:e1006157
    [Google Scholar]
  99. 97. 
    Liao Y, Bai Q, Xu P, Wu T, Guo D et al. 2018. Mutation in rice Abscisic Acid2 results in cell death, enhanced disease-resistance, altered seed dormancy and development. Front. Plant Sci. 9:405
    [Google Scholar]
  100. 98. 
    Lillemo M, Asalf B, Singh RP, Huerta-Espino J, Chen XM et al. 2008. The adult plant rust resistance loci Lr34/Yr18 and Lr46/Yr29 are important determinants of partial resistance to powdery mildew in bread wheat line Saar. Theor. Appl. Genet. 116:1155–66
    [Google Scholar]
  101. 99. 
    Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M et al. 2005. Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310:1180–83
    [Google Scholar]
  102. 100. 
    Liu B, Li JF, Ao Y, Qu J, Li Z et al. 2012. Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 24:3406–19
    [Google Scholar]
  103. 101. 
    Liu D, Xin M, Zhou X, Wang C, Zhang Y, Qin Z 2017. Expression and functional analysis of the transcription factor-encoding gene CsERF004 in cucumber during Pseudoperonospora cubensis and Corynespora cassiicola infection. BMC Plant Biol 17:96
    [Google Scholar]
  104. 102. 
    Liu J, Chen X, Liang X, Zhou X, Yang F et al. 2016. Alternative splicing of rice WRKY62 and WRKY76 transcription factor genes in pathogen defense. Plant Physiol 171:1427–42
    [Google Scholar]
  105. 103. 
    Liu J, Liu D, Tao W, Li W, Wang S et al. 2000. Molecular marker-facilitated pyramiding of different genes for powdery mildew resistance in wheat. Plant Breed 119:21–24
    [Google Scholar]
  106. 104. 
    Liu J, Park CH, He F, Nagano M, Wang M et al. 2015. The RhoGAP SPIN6 associates with SPL11 and OsRac1 and negatively regulates programmed cell death and innate immunity in rice. PLOS Pathog 11:e1004629
    [Google Scholar]
  107. 105. 
    Liu JZ, Horstman HD, Braun E, Graham MA, Zhang C et al. 2011. Soybean homologs of MPK4 negatively regulate defense responses and positively regulate growth and development. Plant Physiol 157:1363–78
    [Google Scholar]
  108. 106. 
    Liu M, Shi Z, Zhang X, Wang M, Zhang L et al. 2019. Inducible overexpression of Ideal Plant Architecture1 improves both yield and disease resistance in rice. Nat. Plants 5:389–400
    [Google Scholar]
  109. 107. 
    Liu Q, Ning Y, Zhang Y, Yu N, Zhao C et al. 2017. OsCUL3a negatively regulates cell death and immunity by degrading OsNPR1 in rice. Plant Cell 29:345–59
    [Google Scholar]
  110. 108. 
    Liu S, Kandoth PK, Warren SD, Yeckel G, Heinz R et al. 2012. A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature 492:256–60
    [Google Scholar]
  111. 109. 
    Liu W, Liu J, Triplett L, Leach JE, Wang GL 2014. Novel insights into rice innate immunity against bacterial and fungal pathogens. Annu. Rev. Phytopathol. 52:213–41
    [Google Scholar]
  112. 110. 
    Deleted in proof
  113. 111. 
    Loehrer M, Langenbach C, Goellner K, Conrath U, Schaffrath U 2008. Characterization of nonhost resistance of Arabidopsis to the Asian soybean rust. Mol. Plant-Microbe Interact. 21:1421–30
    [Google Scholar]
  114. 112. 
    Lu F, Wang H, Wang S, Jiang W, Shan C et al. 2015. Enhancement of innate immune system in monocot rice by transferring the dicotyledonous elongation factor Tu receptor EFR. J. Integr. Plant Biol. 57:641–52
    [Google Scholar]
  115. 113. 
    Lu M, Tang X, Zhou JM 2001. Arabidopsis NHO1 is required for general resistance against Pseudomonas bacteria. Plant Cell 13:437–47
    [Google Scholar]
  116. 114. 
    Luo Y, Ma T, Zhang AF, Ong K, Luo Z et al. 2017. Marker-assisted breeding of Chinese elite rice cultivar 9311 for disease resistance to rice blast and bacterial blight and tolerance to submergence. Mol. Breed. 37:106
    [Google Scholar]
  117. 115. 
    Maeda S, Hayashi N, Sasaya T, Mori M 2016. Overexpression of BSR1 confers broad-spectrum resistance against two bacterial diseases and two major fungal diseases in rice. Breed. Sci. 66:396–406
    [Google Scholar]
  118. 116. 
    Makandar R, Essig JS, Schapaugh MA, Trick HN, Shah J 2006. Genetically engineered resistance to fusarium head blight in wheat by expression of Arabidopsis NPR1. Mol. Plant-Microbe Interact 19:123–29
    [Google Scholar]
  119. 117. 
    Malnoy M, Borejsza-Wysocka MM, Aldwinckle HS, Jin QL, He SY 2006. Transgenic apple lines over-expressing the apple gene MpNPR1 have increased resistance to fire blight. Acta Hortic 704:521–26
    [Google Scholar]
  120. 118. 
    Malnoy M, Jin Q, Borejsza-Wysocka EE, He SY, Aldwinckle HS 2007. Overexpression of the apple MpNPR1 gene confers increased disease resistance in Malus. × domestica. Mol. Plant-Microbe Interact. 20:1568–80
    [Google Scholar]
  121. 119. 
    Matthews BF, Beard H, Brewer E, Kabir S, MacDonald MH, Youssef RM 2014. Arabidopsis genes, AtNPR1, AtTGA2 and AtPR-5, confer partial resistance to soybean cyst nematode (Heterodera glycines) when overexpressed in transgenic soybean roots. BMC Plant Biol 14:96
    [Google Scholar]
  122. 120. 
    Mazier M, Flamain F, Nicolaï M, Sarnette V, Caranta C 2011. Knock-down of both eIF4E1 and eIF4E2 genes confers broad-spectrum resistance against potyviruses in tomato. PLOS ONE 6:e2959
    [Google Scholar]
  123. 121. 
    McDonald BA, Linde C. 2002. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40:349–79
    [Google Scholar]
  124. 122. 
    Meksem K, Pantazopoulos P, Njiti VN, Hyten LD, Arelli PR, Lightfoot DA 2001. ‘Forrest’ resistance to the soybean cyst nematode is bigenic: saturation mapping of the Rhg1 and Rhg4 loci. Theor. Appl. Genet. 103:710–17
    [Google Scholar]
  125. 123. 
    Mendes BMJ, Cardoso SC, Boscariol-Camargo RL, Cruz RB, Mourão-Filho FAA, Bergamin Filho A 2010. Reduction in susceptibility to Xanthomonas axonopodis pv. citri in transgenic Citrus sinensis expressing the rice Xa21 gene. Plant Pathol 59:68–75
    [Google Scholar]
  126. 123a. 
    Moore JW, Herrera-Foessel S, Lan C, Schnippenkoetter W, Ayliffe Met al. 2015. A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat. Genet 47:149498
    [Google Scholar]
  127. 124. 
    Morbitzer R, Römer P, Boch J, Lahaye T 2010. Regulation of selected genome loci using de novo-engineered transcription activator-like effector (TALE)-type transcription factors. PNAS 107:21617–22
    [Google Scholar]
  128. 125. 
    Mundt CC. 2002. Use of multiline cultivars and cultivar mixtures for disease management. Annu. Rev. Phytopathol. 40:381–410
    [Google Scholar]
  129. 126. 
    Mundt CC. 2014. Durable resistance: a key to sustainable management of pathogens and pests. Infect. Genet. Evol. 27:446–55
    [Google Scholar]
  130. 127. 
    Mundt CC. 2018. Pyramiding for resistance durability: theory and practice. Phytopathology 108:792–802
    [Google Scholar]
  131. 128. 
    Mysore KS, Ryu CM. 2004. Nonhost resistance: How much do we know. Trends Plant Sci 9:97–104
    [Google Scholar]
  132. 129. 
    Narusaka M, Shirasu K, Noutoshi Y, Kubo Y, Shiraishi T et al. 2009. RRS1 and RPS4 provide a dual Resistance-gene system against fungal and bacterial pathogens. Plant J 60:218–26
    [Google Scholar]
  133. 130. 
    Nekrasov V, Wang CM, Win J, Lanz C, Weigel D, Kamoun S 2017. Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Sci. Rep. 7:6
    [Google Scholar]
  134. 131. 
    Nelson R, Wiesner-Hanks T, Wisser R, Balint-Kurti P 2018. Navigating complexity to breed disease-resistant crops. Nat. Rev. Genet. 19:21–33
    [Google Scholar]
  135. 132. 
    Ni DH, Song FS, Ni JL, Zhang AF, Wang CL et al. 2015. Marker-assisted selection of two-line hybrid rice for disease resistance to rice blast and bacterial blight. Field Crop. Res. 184:1–8
    [Google Scholar]
  136. 133. 
    Ni X, Tian Z, Liu J, Song B, Xie C 2010. Cloning and molecular characterization of the potato RING finger protein gene StRFP1 and its function in potato broad-spectrum resistance against Phytophthora infestans. J. Plant Physiol. 167:488–96
    [Google Scholar]
  137. 134. 
    Ning Y, Liu W, Wang GL 2017. Balancing immunity and yield in crop plants. Trends Plant Sci 22:1069–79
    [Google Scholar]
  138. 135. 
    O'Connell RJ, Panstruga R. 2006. Tête à tête inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol 171:699–718
    [Google Scholar]
  139. 136. 
    Oliva R, Ji C, Atienza-Grande G, Huguet-Tapia JC, Perez-Quintero A et al. 2019. Broad-spectrum resistance to bacterial blight in rice using genome editing. Nat. Biotechnol. 37:1344–50
    [Google Scholar]
  140. 137. 
    Omar AA, Murata MM, El-Shamy HA, Graham JH, Grosser JW 2018. Enhanced resistance to citrus canker in transgenic mandarin expressing Xa21 from rice. Transgenic Res 27:179–91
    [Google Scholar]
  141. 138. 
    Parisi K, Shafee TMA, Quimbar P, van der Weerden NL, Bleackley MR, Anderson MA 2019. The evolution, function and mechanisms of action for plant defensins. Semin. Cell Dev. Biol. 88:107–18
    [Google Scholar]
  142. 139. 
    Peng H, Zhang Q, Li Y, Lei C, Zhai Y et al. 2009. A putative leucine-rich repeat receptor kinase, OsBRR1, is involved in rice blast resistance. Planta 230:377–85
    [Google Scholar]
  143. 140. 
    Peng X, Hu Y, Tang X, Zhou P, Deng X et al. 2012. Constitutive expression of rice WRKY30 gene increases the endogenous jasmonic acid accumulation, PR gene expression and resistance to fungal pathogens in rice. Planta 236:1485–98
    [Google Scholar]
  144. 141. 
    Pfeilmeier S, George J, Morel A, Roy S, Smoker M et al. 2019. Expression of the Arabidopsis thaliana immune receptor EFR in Medicago truncatula reduces infection by a root pathogenic bacterium, but not nitrogen-fixing rhizobial symbiosis. Plant Biotechnol. J. 17:569–79
    [Google Scholar]
  145. 142. 
    Piffanelli P, Zhou F, Casais C, Orme J, Jarosch B et al. 2002. The barley MLO modulator of defense and cell death is responsive to biotic and abiotic stress stimuli. Plant Physiol 129:1076–85
    [Google Scholar]
  146. 143. 
    Pink DAC. 2002. Strategies using genes for non-durable disease resistance. Euphytica 124:227–36
    [Google Scholar]
  147. 144. 
    Pradhan SK, Nayak DK, Mohanty S, Behera L, Barik SR et al. 2015. Pyramiding of three bacterial blight resistance genes for broad-spectrum resistance in deepwater rice variety, Jalmagna. Rice 8:51
    [Google Scholar]
  148. 145. 
    Pyott DE, Sheehan E, Molnar A 2016. Engineering of CRISPR/Cas9-mediated potyvirus resistance in transgene-free Arabidopsis plants. Mol. Plant Pathol. 17:1276–88
    [Google Scholar]
  149. 146. 
    Qi T, Seong K, Thomazella DPT, Kim JR, Pham J et al. 2018. NRG1 functions downstream of EDS1 to regulate TIR-NLR-mediated plant immunity in Nicotiana benthamiana. PNAS 115:10979–87
    [Google Scholar]
  150. 147. 
    Qian C, Cui C, Wang X, Zhou C, Hu P et al. 2017. Molecular characterisation of the broad-spectrum resistance to powdery mildew conferred by the Stpk-V gene from the wild species Haynaldia villosa. Plant Biol 19:875–85
    [Google Scholar]
  151. 148. 
    Qiao Y, Jiang W, Lee J, Park B, Choi MS et al. 2010. SPL28 encodes a clathrin-associated adaptor protein complex 1, medium subunit μ1 (AP1M1) and is responsible for spotted leaf and early senescence in rice (Oryza sativa). New Phytol 185:258–74
    [Google Scholar]
  152. 149. 
    Qie Y, Liu Y, Wang M, Li X, See DR et al. 2019. Development, validation, and re-selection of wheat lines with pyramided genes Yr64 and Yr15 linked on the short arm of chromosome 1B for resistance to stripe rust. Plant Dis 103:51–58
    [Google Scholar]
  153. 150. 
    Quilis J, Peñas G, Messeguer J, Brugidou C, San Segundo B 2008. The Arabidopsis AtNPR1 inversely modulates defense responses against fungal, bacterial, or viral pathogens while conferring hypersensitivity to abiotic stresses in transgenic rice. Mol. Plant-Microbe Interact. 21:1215–31
    [Google Scholar]
  154. 151. 
    Rawat N, Pumphrey MO, Liu S, Zhang X, Tiwari VK et al. 2016. Wheat Fhb1 encodes a chimeric lectin with agglutinin domains and a pore-forming toxin-like domain conferring resistance to Fusarium head blight. Nat. Genet. 48:1576–80
    [Google Scholar]
  155. 152. 
    Robatzek S, Bittel P, Chinchilla D, Köchner P, Felix G et al. 2007. Molecular identification and characterization of the tomato flagellin receptor LeFLS2, an orthologue of Arabidopsis FLS2 exhibiting characteristically different perception specificities. Plant Mol. Biol. 64:539–47
    [Google Scholar]
  156. 152a. 
    Robatzek S, Chinchilla D, Boller T 2006. Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev 20:53742
    [Google Scholar]
  157. 153. 
    Römer P, Strauss T, Hahn S, Scholze H, Morbitzer R et al. 2009. Recognition of AvrBs3-like proteins is mediated by specific binding to promoters of matching pepper Bs3 alleles. Plant Physiol 150:1697–712
    [Google Scholar]
  158. 154. 
    Sánchez-Martín J, Steuernagel B, Ghosh S, Herren G, Hurni S et al. 2016. Rapid gene isolation in barley and wheat by mutant chromosome sequencing. Genome Biol 17:221
    [Google Scholar]
  159. 155. 
    Sanfaçon H. 2015. Plant translation factors and virus resistance. Viruses 7:3392–419
    [Google Scholar]
  160. 156. 
    Sathoff AE, Velivelli S, Shah DM, Samac DA 2019. Plant defensin peptides have antifungal and antibacterial activity against human and plant pathogens. Phytopathology 109:402–8
    [Google Scholar]
  161. 157. 
    Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N, Nelson A 2019. The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol. 3:430–39
    [Google Scholar]
  162. 158. 
    Sawada K, Hasegawa M, Tokuda L, Kameyama J, Kodama O et al. 2004. Enhanced resistance to blast fungus and bacterial blight in transgenic rice constitutively expressing OsSBP, a rice homologue of mammalian selenium-binding proteins. Biosci. Biotechnol. Biochem. 68:873–80
    [Google Scholar]
  163. 159. 
    Schoonbeek HJ, Wang HH, Stefanato FL, Craze M, Bowden S et al. 2015. Arabidopsis EF-Tu receptor enhances bacterial disease resistance in transgenic wheat. New Phytol 206:606–13
    [Google Scholar]
  164. 160. 
    Schultink A, Qi T, Lee A, Steinbrenner AD, Staskawicz B 2017. Roq1 mediates recognition of the Xanthomonas and Pseudomonas effector proteins XopQ and HopQ1. Plant J 92:787–95
    [Google Scholar]
  165. 161. 
    Schwessinger B, Bahar O, Thomas N, Holton N, Nekrasov V et al. 2015. Transgenic expression of the dicotyledonous pattern recognition receptor EFR in rice leads to ligand-dependent activation of defense responses. PLOS Pathog 11:e1004809
    [Google Scholar]
  166. 162. 
    Segretin ME, Pais M, Franceschetti M, Chaparro-Garcia A, Bos JIB et al. 2014. Single amino acid mutations in the potato immune receptor R3a expand response to Phytophthora effectors. Mol. Plant-Microbe Interact. 27:624–37
    [Google Scholar]
  167. 163. 
    Shimono M, Koga H, Akagi A, Hayashi N, Goto S et al. 2012. Rice WRKY45 plays important roles in fungal and bacterial disease resistance. Mol. Plant Pathol. 13:83–94
    [Google Scholar]
  168. 164. 
    Silva KJP, Brunings A, Peres NA, Mou Z, Folta KM 2015. The Arabidopsis NPR1 gene confers broad-spectrum disease resistance in strawberry. Transgenic Res 24:693–704
    [Google Scholar]
  169. 165. 
    Silva KJP, Mahna N, Mou Z, Folta KM 2018. NPR1 as a transgenic crop protection strategy in horticultural species. Hortic Res 5:15
    [Google Scholar]
  170. 166. 
    Singh RP, Hodson DP, Jin Y, Lagudah ES, Ayliffe MA et al. 2015. Emergence and spread of new races of wheat stem rust fungus: continued threat to food security and prospects of genetic control. Phytopathology 105:872–84
    [Google Scholar]
  171. 167. 
    Singh RP, Huerta-Espino J, Bhavani S, Herrera-Foessel SA, Singh D et al. 2011. Race non-specific resistance to rust diseases in CIMMYT spring wheats. Euphytica 179:175–86
    [Google Scholar]
  172. 168. 
    Somers DJ, Thomas J, DePauw R, Fox S, Humphreys G, Fedak G 2005. Assembling complex genotypes to resist Fusarium in wheat (Triticum aestivum L.). Theor. Appl. Genet. 111:1623–31
    [Google Scholar]
  173. 168a. 
    Song W-Y, Wang G-L, Chen L-L, Kim H-S, Pi L-Yet al. 1995. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:18046
    [Google Scholar]
  174. 169. 
    Spielmeyer W, Mago R, Wellings C, Ayliffe M 2013. Lr67 and Lr34 rust resistance genes have much in common—they confer broad spectrum resistance to multiple pathogens in wheat. BMC Plant Biol 13:96
    [Google Scholar]
  175. 170. 
    St. Clair DA 2010. Quantitative disease resistance and quantitative resistance loci in breeding. Annu. Rev. Phytopathol. 48:247–68
    [Google Scholar]
  176. 171. 
    Stein M, Dittgen J, Sánchez-Rodríguez C, Hou BH, Molina A et al. 2006. Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18:731–46
    [Google Scholar]
  177. 172. 
    Steuernagel B, Periyannan SK, Hernández-Pinzón I, Witek K, Rouse MN et al. 2016. Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture. Nat. Biotechnol. 34:652–55
    [Google Scholar]
  178. 173. 
    Stirnweis D, Milani SD, Jordan T, Keller B, Brunner S 2014. Substitutions of two amino acids in the nucleotide-binding site domain of a resistance protein enhance the hypersensitive response and enlarge the PM3F resistance spectrum in wheat. Mol. Plant-Microbe Interact. 27:265–76
    [Google Scholar]
  179. 174. 
    Su Z, Bernardo A, Tian B, Chen H, Wang S et al. 2019. A deletion mutation in TaHRC confers Fhb1 resistance to Fusarium head blight in wheat. Nat. Genet. 51:1099–105
    [Google Scholar]
  180. 175. 
    Sucher J, Boni R, Yang P, Rogowsky P, Buchner H et al. 2017. The durable wheat disease resistance gene Lr34 confers common rust and northern corn leaf blight resistance in maize. Plant Biotechnol. J. 15:489–96
    [Google Scholar]
  181. 176. 
    Suh JP, Jeung JU, Noh TH, Cho YC, Park SH et al. 2013. Development of breeding lines with three pyramided resistance genes that confer broad-spectrum bacterial blight resistance and their molecular analysis in rice. Rice 6:5
    [Google Scholar]
  182. 177. 
    Deleted in proof
  183. 178. 
    Swathi G, Rani CVD, Md J, Madhav MS, Vanisree S et al. 2019. Marker-assisted introgression of the major bacterial blight resistance genes, Xa21 and xa13, and blast resistance gene, Pi54, into the popular rice variety, JGL1798. Mol. Breed 39:58
    [Google Scholar]
  184. 179. 
    Tang D, Simonich MT, Innes RW 2007. Mutations in LACS2, a long-chain acyl-coenzyme A synthetase, enhance susceptibility to avirulent Pseudomonas syringae but confer resistance to Botrytis cinerea in Arabidopsis. Plant Physiol 144:1093–103
    [Google Scholar]
  185. 180. 
    Tang X, Xie M, Kim YJ, Zhou J, Klessig DF, Martin GB 1999. Overexpression of Pto activates defense responses and confers broad resistance. Plant Cell 11:15–29
    [Google Scholar]
  186. 181. 
    Tao Z, Liu H, Qiu D, Hou Y, Li X et al. 2009. A pair of allelic WRKY genes play opposite roles in rice-bacteria interactions. Plant Physiol 151:936–48
    [Google Scholar]
  187. 182. 
    Thomma BP, Nurnberger T, Joosten MH 2011. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4–15
    [Google Scholar]
  188. 183. 
    Tripathi JN, Lorenzen J, Bahar O, Ronald P, Tripathi L 2014. Transgenic expression of the rice Xa21 pattern-recognition receptor in banana (Musa sp.) confers resistance to Xanthomonas campestris pv. musacearum. Plant Biotechnol. J. 12:663–73
    [Google Scholar]
  189. 184. 
    Tsilo TJ, Kolmer JA, Anderson JA 2014. Molecular mapping and improvement of leaf rust resistance in wheat breeding lines. Phytopathology 104:865–70
    [Google Scholar]
  190. 185. 
    Van Damme M, Huibers RP, Elberse J, Van den Ackerveken G 2008. Arabidopsis DMR6 encodes a putative 2OG-Fe(II) oxygenase that is defense-associated but required for susceptibility to downy mildew. Plant J 54:785–93
    [Google Scholar]
  191. 186. 
    Vo KTX, Kim CY, Hoang TV, Lee SK, Shirsekar G et al. 2018. OsWRKY67 plays a positive role in basal and XA21-mediated resistance in rice. Front. Plant Sci. 8:2220
    [Google Scholar]
  192. 187. 
    von Arnim AG, Jia Q, Vaughn JN 2014. Regulation of plant translation by upstream open reading frames. Plant Sci 214:1–12
    [Google Scholar]
  193. 188. 
    Wally O, Jayaraj J, Punja ZK 2009. Broad-spectrum disease resistance to necrotrophic and biotrophic pathogens in transgenic carrots (Daucus carota L.) expressing an Arabidopsis NPR1 gene. Planta 231:131–41
    [Google Scholar]
  194. 188a. 
    Wang C, Zhang X, Fan Y, Gao Y, Zhu Qet al. 2015. XA23 is an executor R protein and confers broad-spectrum disease resistance in rice. Mol. Plant 8:290302
    [Google Scholar]
  195. 188b. 
    Wang G-L, Song W-Y, Ruan D-L, Sideris S, Ronald PC 1996. The cloned gene, Xa21, confers resistance to multiple Xanthomonas oryzae pv. oryzae isolates in transgenic plants. Mol. Plant Microbe Interact 9:85055
    [Google Scholar]
  196. 189. 
    Wang J, Qu B, Dou S, Li L, Yin D et al. 2015. The E3 ligase OsPUB15 interacts with the receptor-like kinase PID2 and regulates plant cell death and innate immunity. BMC Plant Biol 15:49
    [Google Scholar]
  197. 190. 
    Wang J, Zhou L, Shi H, Chern M, Yu H et al. 2018. A single transcription factor promotes both yield and immunity in rice. Science 361:1026–28
    [Google Scholar]
  198. 191. 
    Deleted in proof
  199. 192. 
    Wang Y, Tan J, Wu Z, VandenLangenberg K, Wehner TC et al. 2019. STAYGREEN, STAY HEALTHY: A loss-of-susceptibility mutation in the STAYGREEN gene provides durable, broad-spectrum disease resistances for over 50 years of US cucumber production. New Phytol 221:415–30
    [Google Scholar]
  200. 193. 
    Wang YP, Cheng X, Shan QW, Zhang Y, Liu JX et al. 2014. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat. Biotechnol. 32:947–51
    [Google Scholar]
  201. 194. 
    Wang Z, Cheng J, Fan A, Zhao J, Yu Z et al. 2018. LecRK-V, an L-type lectin receptor kinase in Haynaldia villosa, plays positive role in resistance to wheat powdery mildew. Plant Biotechnol. J. 16:50–62
    [Google Scholar]
  202. 195. 
    Wisser RJ, Sun Q, Hulbert SH, Kresovich S, Nelson RJ 2005. Identification and characterization of regions of the rice genome associated with broad-spectrum, quantitative disease resistance. Genetics 169:2277–93
    [Google Scholar]
  203. 196. 
    Wu Y, Xiao N, Chen Y, Yu L, Pan C et al. 2019. Comprehensive evaluation of resistance effects of pyramiding lines with different broad-spectrum resistance genes against Magnaporthe oryzae in rice (Oryza sativa L.). Rice 12:11
    [Google Scholar]
  204. 197. 
    Xiao N, Wu YY, Pan CH, Yu L, Chen Y et al. 2017. Improving of rice blast resistances in Japonica by pyramiding major R genes. Front. Plant Sci. 7:1918
    [Google Scholar]
  205. 198. 
    Xiong L, Yang Y. 2003. Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid–inducible mitogen-activated protein kinase. Plant Cell 15:745–59
    [Google Scholar]
  206. 199. 
    Xu G, Yuan M, Ai C, Liu L, Zhuang E et al. 2017. uORF-mediated translation allows engineered plant disease resistance without fitness costs. Nature 545:491–94
    [Google Scholar]
  207. 200. 
    Xu HY, Zhang C, Li ZC, Wang ZR, Jiang XX et al. 2018. The MAPK kinase kinase GmMEKK1 regulates cell death and defense responses. Plant Physiol 178:907–22
    [Google Scholar]
  208. 201. 
    Yamaguchi T, Kuroda M, Yamakawa H, Ashizawa T, Hirayae K et al. 2009. Suppression of a phospholipase D gene, OsPLDβ1, activates defense responses and increases disease resistance in rice. Plant Physiol 150:308–19
    [Google Scholar]
  209. 202. 
    Yan C, Liu Y, Mou T 2013. Improvement of rice bacterial blight resistance of hybrid rice Jinyou 207 by molecular marker-assisted selection. Chin. J. Rice Sci. 27:365–72
    [Google Scholar]
  210. 203. 
    Yang Q, Balint-Kurti P, Xu M 2017. Quantitative disease resistance: dissection and adoption in maize. Mol. Plant 10:402–13
    [Google Scholar]
  211. 204. 
    Yang Q, He Y, Kabahuma M, Chaya T, Kelly A et al. 2017. A gene encoding maize caffeoyl-CoA O-methyltransferase confers quantitative resistance to multiple pathogens. Nat. Genet. 49:1364–72
    [Google Scholar]
  212. 204a. 
    Yang X, Li J, Li X, She R, Pei Y 2006. Isolation and characterization of a novel thermostable non-specific lipid transfer protein-like antimicrobial protein from motherwort (Leonurus japonicus Houtt) seeds. Peptides 27:312228
    [Google Scholar]
  213. 205. 
    Yang ZP, Gilbert J, Somers DJ, Fedak G, Procunier JD, McKenzie IH 2003. Marker assisted selection of Fusarium head blight resistance genes in two doubled haploid populations of wheat. Mol. Breed. 12:309–17
    [Google Scholar]
  214. 206. 
    Yasuda N, Mitsunaga T, Hayashi K, Koizumi S, Fujita Y 2015. Effects of pyramiding quantitative resistance genes pi21, Pi34, and Pi35 on rice leaf blast disease. Plant Dis 99:904–9
    [Google Scholar]
  215. 207. 
    You Q, Zhai K, Yang D, Yang W, Wu J et al. 2016. An E3 ubiquitin ligase-BAG protein module controls plant innate immunity and broad-spectrum disease resistance. Cell Host Microbe 20:758–69
    [Google Scholar]
  216. 208. 
    Yu N, Lee TG, Rosa DP, Hudson M, Diers BW 2016. Impact of Rhg1 copy number, type, and interaction with Rhg4 on resistance to Heterodera glycines in soybean. Theor. Appl. Genet. 129:2403–12
    [Google Scholar]
  217. 209. 
    Yuan M, Ke Y, Huang R, Ma L, Yang Z et al. 2016. A host basal transcription factor is a key component for infection of rice by TALE-carrying bacteria. eLife 5:e19605
    [Google Scholar]
  218. 210. 
    Zaidi SS, Mukhtar MS, Mansoor S 2018. Genome editing: targeting susceptibility genes for plant disease resistance. Trends Biotechnol 36:898–906
    [Google Scholar]
  219. 211. 
    Zeilmaker T, Ludwig N, Elberse J, Seidl MF, Berke L et al. 2015. DOWNY MILDEW RESISTANT 6 and DMR6-LIKE OXYGENASE 1 are partially redundant but distinct suppressors of immunity in Arabidopsis. Plant J 81:210–22
    [Google Scholar]
  220. 212. 
    Zeng LR, Qu S, Bordeos A, Yang C, Baraoidan M et al. 2004. Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell 16:2795–808
    [Google Scholar]
  221. 213. 
    Zeng X, Tian D, Gu K, Zhou Z, Yang X et al. 2015. Genetic engineering of the Xa10 promoter for broad-spectrum and durable resistance to Xanthomonas oryzae pv. oryzae. Plant Biotechnol. J. 13:993–1001
    [Google Scholar]
  222. 214. 
    Zhai K, Deng Y, Liang D, Tang J, Liu J et al. 2019. RRM transcription factors interact with NLRs and regulate broad-spectrum blast resistance in rice. Mol. Cell 74:996–1009
    [Google Scholar]
  223. 215. 
    Zhang Y, Cheng YT, Qu N, Zhao Q, Bi D, Li X 2006. Negative regulation of defense responses in Arabidopsis by two NPR1 paralogs. Plant J 48:647–56
    [Google Scholar]
  224. 216. 
    Zhao X, Tan G, Xing Y, Wei L, Chao Q et al. 2012. Marker-assisted introgression of qHSR1 to improve maize resistance to head smut. Mol. Breed. 30:1077–88
    [Google Scholar]
  225. 217. 
    Zheng Z, Appiano M, Pavan S, Bracuto V, Ricciardi L et al. 2016. Genome-wide study of the tomato SlMLO gene family and its functional characterization in response to the powdery mildew fungus Oidium neolycopersici. Front. Plant Sci 7:380
    [Google Scholar]
  226. 218. 
    Zhong C, Ren Y, Qi Y, Yu X, Wu X, Tian Z 2018. PAMP-responsive ATL gene StRFP1 and its orthologue NbATL60 positively regulate Phytophthora infestans resistance in potato and Nicotiana benthamiana. Plant Sci 270:47–57
    [Google Scholar]
  227. 219. 
    Zhou J, Peng Z, Long J, Sosso D, Liu B et al. 2015. Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J 82:632–43
    [Google Scholar]
  228. 220. 
    Zhou X, Liao H, Chern M, Yin J, Chen Y et al. 2018. Loss of function of a rice TPR-domain RNA-binding protein confers broad-spectrum disease resistance. PNAS 115:3174–79
    [Google Scholar]
  229. 221. 
    Zhu S, Li Y, Vossen JH, Visser RG, Jacobsen E 2012. Functional stacking of three resistance genes against Phytophthora infestans in potato. Transgenic Res 21:89–99
    [Google Scholar]
  230. 222. 
    Zhu Y, Chen H, Fan J, Wang Y, Li Y et al. 2000. Genetic diversity and disease control in rice. Nature 406:718–22
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-010720-022215
Loading
/content/journals/10.1146/annurev-arplant-010720-022215
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error