1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Phytopathology
  4. Volume 54, 2016
  5. Article

Annual Review of Phytopathology

Volume 54, 2016

Multiple Disease Resistance in Plants

Abstract

Many plants, both in nature and in agriculture, are resistant to multiple diseases. Although much of the plant innate immunity system provides highly specific resistance, there is emerging evidence to support the hypothesis that some components of plant defense are relatively nonspecific, providing multiple disease resistance (MDR). Understanding MDR is of fundamental and practical interest to plant biologists, pathologists, and breeders. This review takes stock of the available evidence related to the MDR hypothesis. Questions about MDR are considered primarily through the lens of forward genetics, starting at the organismal level and proceeding to the locus level and, finally, to the gene level. At the organismal level, MDR may be controlled by clusters of genes that evolve under diversifying selection, by dispersed, pathogen-specific genes, and/or by individual genes providing MDR. Based on the few MDR loci that are well-understood, MDR is conditioned by diverse mechanisms at the locus and gene levels.

Keyword(s): crop improvement, genome-wide association analysis, linkage analysis, pleiotropy, QTL
Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-080615-100037
2016-08-04
2025-04-22
Loading full text...

Full text loading...

/deliver/fulltext/phyto/54/1/annurev-phyto-080615-100037.html?itemId=/content/journals/10.1146/annurev-phyto-080615-100037&mimeType=html&fmt=ahah

Literature Cited

  1. Ali S, Singh PK, McMullen MP, Mergoum M, Adhikari TB. 1.  2008. Resistance to multiple leaf spot diseases in wheat. Euphytica 159:167–79 [Google Scholar]
  2. Almasia NI, Bazzini AA, Hopp HE, Vazquez-Rovere C. 2.  2008. Overexpression of snakin-1 gene enhances resistance to Rhizoctonia solani and Erwinia carotovora in transgenic potato plants. Mol. Plant Pathol. 9:329–38 [Google Scholar]
  3. Apel K, Hirt H. 3.  2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55:373–99 [Google Scholar]
  4. Atienza SG, Jafary H, Niks RE. 4.  2004. Accumulation of genes for susceptibility to rust fungi for which barley is nearly a nonhost results in two barley lines with extreme multiple susceptibility. Planta 220:71–79 [Google Scholar]
  5. Bakker E, Borm T, Prins P, van der Vossen E, Uenk G. 5.  et al. 2011. A genome-wide genetic map of NB-LRR disease resistance loci in potato. Theor. Appl. Genet. 123:493–508 [Google Scholar]
  6. Balint-Kurti PJ, Yang J, Van Esbroeck G, Jung J, Smith ME. 6.  2010. Use of a maize advanced intercross line for mapping of QTL for northern leaf blight resistance and multiple disease resistance. Crop Sci. 50:458–66 [Google Scholar]
  7. Benson JM, Poland JA, Benson BM, Stromberg EL, Nelson RJ. 7.  2015. Resistance to gray leaf spot of maize: genetic architecture and mechanisms elucidated through nested association mapping and near-isogenic line analysis. PLOS Genet. 11:e1005045 [Google Scholar]
  8. Belcher AR, Zwonitzer JC, Cruz JS, Krakowsky MD, Chung CL. 8.  et al. 2012. Analysis of quantitative disease resistance to Southern leaf blight and of multiple disease resistance in maize, using near-isogenic lines. Theor. Appl. Genet. 124:433–45 [Google Scholar]
  9. Boller T, Felix G. 9.  2009. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60:379–406 [Google Scholar]
  10. Bolouri Moghaddam MR, Van den Ende W. 10.  2012. Sugars and plant innate immunity. J. Exp. Bot. 63:3989–98 [Google Scholar]
  11. Bonman JM, Khush GS, Nelson RJ. 11.  1992. Breeding rice for resistance to pests. Annu. Rev. Phytopathol. 30:507–28 [Google Scholar]
  12. Bonnet J, Danan S, Boudet C, Barchi L, Sage-Palloix A-M. 12.  et al. 2007. Are the polygenic architectures of resistance to Phytophthora capsici and P. parasitica independent in pepper?. Theor. Appl. Genet. 115:253–64 [Google Scholar]
  13. Bostock RM. 13.  2005. Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu. Rev. Phytopathol. 43:545–80 [Google Scholar]
  14. Bozkurt TO, Richardson A, Dagdas YF, Mongrand S, Kamoun S, Raffaele S. 14.  2014. The plant membrane–associated REMORIN1.3 accumulates in discrete perihaustorial domains and enhances susceptibility to Phytophthora infestans. Plant Physiol. 165:1005–18 [Google Scholar]
  15. Broekaert WF, Delauré SL, De Bolle MFC, Cammue BPA. 15.  2006. The role of ethylene in host-pathogen interactions. Annu. Rev. Phytopathol. 44:393–416 [Google Scholar]
  16. Brown JK. 16.  2002. Yield penalties of disease resistance in crops. Curr. Opin. Plant Biol. 5:339–44 [Google Scholar]
  17. Browse J. 17.  2009. Jasmonate passes muster: a receptor and targets for the defense hormone. Annu. Rev. Plant Biol. 60:183–205 [Google Scholar]
  18. Buerstmayr M, Matiasch L, Mascher F, Vida G, Ittu M. 18.  et al. 2014. Mapping of quantitative adult plant field resistance to leaf rust and stripe rust in two European winter wheat populations reveals co-location of three QTL conferring resistance to both rust pathogens. Theor. Appl. Genet. 127:2011–28 [Google Scholar]
  19. Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M. 19.  et al. 1997. The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695–705 [Google Scholar]
  20. Cao H, Li X, Dong X. 20.  1998. Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. PNAS 95:6531–36 [Google Scholar]
  21. Cartwright HN, Humphries JA, Smith LG. 21.  2009. PAN1: a receptor-like protein that promotes polarization of an asymmetric cell division in maize. Science 323:649–51 [Google Scholar]
  22. Chakrabarti A, Ganapathi TR, Mukherjee PK, Bapat VA. 22.  2003. MSI-99, a magainin analogue, imparts enhanced disease resistance in transgenic tobacco and banana. Planta 216:587–96 [Google Scholar]
  23. Chen SC, Liu AR, Wang FH, Ahammed GJ. 23.  2009. Combined overexpression of chitinase and defensin genes in transgenic tomato enhances resistance to Botrytis cinerea. Afr. J. Biotechnol. 8:5182–88 [Google Scholar]
  24. Chung C-L, Longfellow JM, Walsh EK, Kerdieh Z, Van Esbroeck G. 24.  et al. 2010. Resistance loci affecting distinct stages of fungal pathogenesis: use of introgression lines for QTL mapping and characterization in the maize-Setosphaeria turcica pathosystem. BMC Plant Biol. 10:103 [Google Scholar]
  25. Cooley MB, Pathirana S, Wu HJ, Kachroo P, Klessig DF. 25.  2000. Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens. Plant Cell 12:663–76 [Google Scholar]
  26. Cox TS, Raupp WJ, Wilson DL, Gill BS, Bockus WW, Browder LE. 26.  1992. Resistance to foliar diseases in a collection of Triticum tauschii germ plasm. Plant Dis 76:1061–64 [Google Scholar]
  27. Coyne CJ, Pilet-Nayel M-L, McGee RJ, Porter LD, Smýkal P, Grünwald NJ. 27.  2015. Identification of QTL controlling high levels of partial resistance to Fusarium solani f. sp. pisi in pea. Plant Breed. 134:446–53 [Google Scholar]
  28. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR. 28.  2010. Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant Biol. 61:651–79 [Google Scholar]
  29. Dangl JL, Jones JDG. 29.  2001. Plant pathogens and integrated defence responses to infection. Nature 411:826–33 [Google Scholar]
  30. de Carvalho A, Gomes VM. 30.  2009. Plant defensins—prospects for the biological functions and biotechnological properties. Peptides 30:1007–20 [Google Scholar]
  31. Dixon AGO, Ogbe FO, Okechukwu RU. 31.  2010. Cassava mosaic disease in sub-Saharan Africa: a feasible solution for an unsolved problem. Outlook Agric. 39:89–94 [Google Scholar]
  32. Dong X. 32.  2004. NPR1, all things considered. Curr. Opin. Plant Biol. 7:547–52 [Google Scholar]
  33. Eibach R, Zyprian E, Welter L, Töpfer R. 33.  2007. The use of molecular markers for pyramiding resistance genes in grapevine breeding. Vitis 46:120–24 [Google Scholar]
  34. Elgin JH, Hill RR, Zeiders KE. 34.  1970. Comparison of four methods of multiple trait selection for five traits in alfalfa. Crop Sci. 10:190–93 [Google Scholar]
  35. Faris JD, Li WL, Liu DJ, Chen PD, Gill BS. 35.  1999. Candidate gene analysis of quantitative disease resistance in wheat. Theor. Appl. Genet. 98:219–25 [Google Scholar]
  36. Ferrari S. 36.  2013. Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development. Front. Plant Sci. 4:1–9 [Google Scholar]
  37. Fetch TG, Steffenson BJ, Nevo E. 37.  2003. Diversity and sources of multiple disease resistance in Hordeum spontaneum. Plant Dis. 87:1439–48 [Google Scholar]
  38. Flemmig EL. 38.  2012. Molecular markers to deploy and characterize stem rust resistance in wheat MS Thesis, N. C. State. Univ., Raleigh [Google Scholar]
  39. Flint-Garcia SA, Thuillet A-C, Yu J, Pressoir G, Romero SM. 39.  et al. 2005. Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J. 44:1054–64 [Google Scholar]
  40. Fokunang CN, Ikotun T, Dixon AGO, Akem CN. 40.  2000. Field reaction of cassava genotypes to anthracnose, bacterial blight, cassava mosaic disease, and their effects on yield. Afr. Crop Sci. J. 8:179–86 [Google Scholar]
  41. Fotopoulos V, Gilbert MJ, Pittman JK, Marvier AC, Buchanan AJ. 41.  et al. 2003. The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atβfruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol. 132:821–29 [Google Scholar]
  42. Fu J, Liu H, Li Y, Yu H, Li X. 42.  et al. 2011. Manipulating broad-spectrum disease resistance by suppressing pathogen-induced auxin accumulation in rice. Plant Physiol. 155:589–602 [Google Scholar]
  43. Gassmann W, Hinsch ME, Staskawicz BJ. 43.  1999. The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes. Plant J. 20:265–77 [Google Scholar]
  44. Gómez-Ariza J, Campo S, Rufat M, Estopà M, Messeguer J. 44.  et al. 2007. Sucrose-mediated priming of plant defense responses and broad-spectrum disease resistance by overexpression of the maize pathogenesis-related PRms protein in rice plants. Mol. Plant-Microbe Interact. 20:832–42 [Google Scholar]
  45. Govrin EM, Levine A. 45.  2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 10:751–57 [Google Scholar]
  46. Grant M, Godiard L, Straube E, Ashfield T, Lewald J. 46.  et al. 1995. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269:843–46 [Google Scholar]
  47. Greenberg JT, Ausubel FM. 47.  1993. Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging. Plant J. 4:327–41 [Google Scholar]
  48. Gurung S, Bonman JM, Ali S, Patel J, Myrfield M. 48.  et al. 2009. New and diverse sources of multiple disease resistance in wheat. Crop Sci. 49:1655–66 [Google Scholar]
  49. Gurung S, Hansen JM, Bonman JM, Gironella AIN, Adhikari TB. 49.  2012. Multiple disease resistance to four leaf spot diseases in winter wheat accessions from the USDA national small grains collection. Crop Sci. 52:1640–50 [Google Scholar]
  50. Gurung S, Mamidi S, Bonman JM, Xiong M, Brown-Guedira G, Adhikari TB. 50.  2014. Genome-wide association study reveals novel quantitative trait loci associated with resistance to multiple leaf spot diseases of spring wheat. PLOS ONE 9:e108179 [Google Scholar]
  51. Hann DR, Rathjen JP. 51.  2007. Early events in the pathogenicity of Pseudomonas syringae on Nicotiana benthamiana. Plant J. 49:607–18 [Google Scholar]
  52. Heese A, Hann DR, Gimenez-Ibanez S, Jones AME, He K. 52.  et al. 2007. The receptor-like kinase SER3/BAK1 is a central regulator of innate immunity in plants. PNAS 104:12217–22 [Google Scholar]
  53. Hill RR, Leath KT. 53.  1975. Genotypic and phenotypic correlations for reaction to five foliar pathogens in alfalfa. Theor. Appl. Genet. 258:254–58 [Google Scholar]
  54. Hulbert SH, Webb CA, Smith SM, Sun Q. 54.  2001. Resistance gene complexes: evolution and utilization. Annu. Rev. Phytopathol. 39:285–312 [Google Scholar]
  55. Hysing S-C, Hsam SLK, Singh RP, Huerta-Espino J, Boyd LA. 55.  et al. 2007. Agronomic performance and multiple disease resistance in T2BS.2RL wheat-rye translocation lines. Crop Sci. 47:254 [Google Scholar]
  56. Infantino A, Kharrat M, Riccioni L, Coyne CJ, McPhee KE, Grünwald NJ. 56.  2006. Screening techniques and sources of resistance to root diseases in cool season food legumes. Euphytica 147:201–21 [Google Scholar]
  57. Jafary H, Szabo LJ, Niks RE. 57.  2006. Innate nonhost immunity in barley to different heterologous rust fungi is controlled by sets of resistance genes with different and overlapping specificities. Mol. Plant-Microbe Interact. 19:1270–79 [Google Scholar]
  58. Jamann TM, Luo X, Morales L, Kolkman JM, Chung C-L, Nelson RJ. 58.  A remorin gene is implicated in quantitative disease resistance in maize. Theor. Appl. Genet. 129:591–602 [Google Scholar]
  59. Jamann TM, Poland JA, Kolkman JM, Smith LG, Nelson RJ. 59.  2014. Unraveling genomic complexity at a quantitative disease resistance locus in maize. Genetics 198:333–44 [Google Scholar]
  60. Jansky SH, Rouse DI. 60.  2003. Multiple disease resistance in interspecific hybrids of potato. Plant Dis. 87:266–72 [Google Scholar]
  61. Jarosch B, Kogel K-H, Schaffrath U. 61.  1999. The ambivalence of the barley Mlo locus: mutations conferring resistance against powdery mildew (Blumeria graminis f. sp. hordei) enhance susceptibility to the rice blast fungus Magnaporthe grisea. Mol. Plant-Microbe Interact. 508:508–14 [Google Scholar]
  62. Jellis GJ. 62.  1992. Multiple resistance to diseases and pests in potatoes. Euphytica 63:51–58 [Google Scholar]
  63. Jha S, Chattoo BB. 63.  2010. Expression of a plant defensin in rice confers resistance to fungal phytopathogens. Transgenic Res. 19:373–84 [Google Scholar]
  64. Jo Y-K, Barker R, Pfender W, Warnke S, Sim S-C, Jung G. 64.  2008. Comparative analysis of multiple disease resistance in ryegrass and cereal crops. Theor. Appl. Genet. 117:531–43 [Google Scholar]
  65. Johnson R. 65.  1981. Durable resistance: definition of, genetic control, and attainment in plant breeding. Phytopathology 71:567 [Google Scholar]
  66. Jones JDG, Dangl JL. 66.  2006. The plant immune system. Nature 444:323–29 [Google Scholar]
  67. Kemmerling B, Schwedt A, Rodriguez P, Mazzotta S, Frank M. 67.  et al. 2007. The BRI1-associated kinase 1, BAK1, has a brassinolide-independent role in plant cell-death control. Curr. Biol. 17:1116–22 [Google Scholar]
  68. Khan MA, Shah MD, Saini RG. 68.  2012. Multiple disease resistance of an Australian bread wheat cultivar Cook. Australas. Plant Pathol. 41:131–37 [Google Scholar]
  69. Kim YJ, Lin N-C, Martin GB. 69.  2002. Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109:589–98 [Google Scholar]
  70. Koornneef A, Pieterse CMJ. 70.  2008. Cross talk in defense signaling. Plant Physiol. 146:839–44 [Google Scholar]
  71. Kou Y, Wang S. 71.  2012. Toward an understanding of the molecular basis of quantitative disease resistance in rice. J. Biotechnol. 159:283–90 [Google Scholar]
  72. Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J. 72.  et al. 2009. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–63 [Google Scholar]
  73. Krijger J-J, Thon MR, Deising HB, Wirsel SG. 73.  2014. Compositions of fungal secretomes indicate a greater impact of phylogenetic history than lifestyle adaptation. BMC Genom. 15:722 [Google Scholar]
  74. Kuang H, Woo S-S, Meyers BC, Nevo E, Michelmore RW. 74.  2004. Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell 16:2870–94 [Google Scholar]
  75. Kump KL, Bradbury PJ, Wisser RJ, Buckler ES, Belcher AR. 75.  et al. 2011. Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population. Nat. Genet. 43:163–68 [Google Scholar]
  76. Lagudah ES, McFadden H, Singh RP, Huerta-Espino J, Bariana HS, Spielmeyer W. 76.  2006. Molecular genetic characterization of the Lr34/Yr18 slow rusting resistance gene region in wheat. Theor. Appl. Genet. 114:21–30 [Google Scholar]
  77. Lander ES, Botstein D. 77.  1989. Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–99 [Google Scholar]
  78. Lebedev VG, Dolgov SV, Lavrova N, Lunin VG, Naroditski BS. 78.  2002. Plant-defensin genes introduction for improvement of pear phytopathogen resistance. Acta. Hortic. 596:167–172 [Google Scholar]
  79. Lee J, Hong J-H, Do JW, Yoon JB. 79.  2010. Identification of QTLs for resistance to anthracnose to two Colletotrichum species in pepper. J. Crop Sci. Biotechnol. 13:227–33 [Google Scholar]
  80. Lemonnier P, Gaillard C, Veillet F, Verbeke J, Lemoine R. 80.  et al. 2014. Expression of Arabidopsis sugar transport protein STP13 differentially affects glucose transport activity and basal resistance to Botrytis cinerea. Plant Mol. Biol. 85:473–84 [Google Scholar]
  81. Li Q, Lawrence CB, Xing HY, Babbitt RA, Bass WT. 81.  et al. 2001. Enhanced disease resistance conferred by expression of an antimicrobial magainin analog in transgenic tobacco. Planta 212:635–39 [Google Scholar]
  82. Li Z, Zhou M, Zhang Z, Ren L, Du L. 82.  et al. 2011. Expression of a radish defensin in transgenic wheat confers increased resistance to Fusarium graminearum and Rhizoctonia cerealis. Funct. Integr. Genom 11:63–70 [Google Scholar]
  83. Lin W-C, Lu C-F, Wu J-W, Cheng M-L, Lin Y-M. 83.  et al. 2004. Transgenic tomato plants expressing the Arabidopsis NPR1 gene display enhanced resistance to a spectrum of fungal and bacterial diseases. Transgenic Res. 13:567–81 [Google Scholar]
  84. Mago R, Tabe L, McIntosh RA, Pretorius Z, Kota R. 84.  et al. 2011. A multiple resistance locus on chromosome arm 3BS in wheat confers resistance to stem rust (Sr2), leaf rust (Lr27) and powdery mildew. Theor. Appl. Genet. 123:615–23 [Google Scholar]
  85. Manosalva PM, Davidson RM, Liu B, Zhu X, Hulbert SH. 85.  et al. 2009. A germin-like protein gene family functions as a complex quantitative trait locus conferring broad-spectrum disease resistance in rice. Plant Physiol. 149:286–96 [Google Scholar]
  86. Marrs KA. 86.  1996. The functions and regulation of glutathione S-transferases in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:127–58 [Google Scholar]
  87. McGrann GRD, Stavrinides A, Russell J, Corbitt MM, Booth A. 87.  et al. 2014. A trade off between mlo resistance to powdery mildew and increased susceptibility of barley to a newly important disease, ramularia leaf spot. J. Exp. Bot. 65:1025–37 [Google Scholar]
  88. Meyers BC, Chin DB, Shen KA, Sivaramakrishnan S, Lavelle DO. 88.  et al. 1998. The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell 10:1817–32 [Google Scholar]
  89. Miklas PN, Delorme R, Stone V, Daly MJ, Stavely JR. 89.  et al. 2000. Bacterial, fungal, and viral disease resistance loci mapped in a recombinant inbred common bean population (“Dorado”/XAN 176). J. Am. Soc. Hortic. Sci. 125:476–81 [Google Scholar]
  90. Miller-Garvin JE, Viands DR. 90.  1994. Selection for resistance to Fusarium root rot, and associations among resistances to six diseases in alfalfa. Crop Sci. 34:1461–65 [Google Scholar]
  91. Mitchell-Olds T, James RV, Palmer MJ, Williams PH. 91.  1995. Genetics of Brassica rapa (syn. campestris). 2. Multiple disease resistance to three fungal pathogens: Peronospora parasitica, Albugo candida and Leptosphaeria maculans. Heredity 75:362–69 [Google Scholar]
  92. Mizobuchi R, Hirabayashi H, Kaji R, Nishizawa Y, Yoshimura A. 92.  et al. 2002. Isolation and characterization of rice lesion-mimic mutants with enhanced resistance to rice blast and bacterial blight. Plant Sci. 163:345–53 [Google Scholar]
  93. Monteagudo AB, Rodiño AP, Lema M, De la Fuente M, Santalla M, De Ron AM. 93.  2006. Resistance to infection by fungal, bacterial, and viral pathogens in a common bean core collection from the Iberian Peninsula. HortScience 41:319–22 [Google Scholar]
  94. Moore JW, Herrera-Foessel S, Lan C, Schnippenkoetter W, Ayliffe M. 94.  et al. 2015. A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat. Genet. 47:1494–98 [Google Scholar]
  95. Mukhtar MS, Carvunis A-R, Dreze M, Epple P, Steinbrenner J. 95.  et al. 2011. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333:596–601 [Google Scholar]
  96. Narusaka M, Shirasu K, Noutoshi Y, Kubo Y, Shiraishi T. 96.  et al. 2009. RRS1 and RPS4 provide a dual resistance gene system against fungal and bacterial pathogens. Plant J. 60:218–26 [Google Scholar]
  97. Narusaka Y, Narusaka M, Park P, Kubo Y, Hirayama T. 97.  et al. 2004. RCH1, a locus in Arabidopsis that confers resistance to the hemibiotrophic fungal pathogen Colletotrichum higginsianum. Mol. Plant-Microbe. Interact. 17:749–62 [Google Scholar]
  98. Nene YL. 98.  1988. Multiple-disease resistance in grain legumes. Annu. Rev. Phytopathol. 26:203–17 [Google Scholar]
  99. Neuffer MG, Calvert OH. 99.  1975. Dominant disease lesion mimics in maize. J. Hered. 66:265–70 [Google Scholar]
  100. Ng TB. 100.  2004. Antifungal proteins and peptides of leguminous and non-leguminous origins. Peptides 25:1215–22 [Google Scholar]
  101. Niks RE, Qi X, Marcel TC. 101.  2015. Quantitative resistance to biotrophic filamentous plant pathogens: concepts, misconceptions, and mechanisms. Annu. Rev. Phytopathol. 53:445–70 [Google Scholar]
  102. Nothnagel EA, McNeil M, Albersheim P, Dell A. 102.  1983. Host-pathogen interactions. Plant Physiol. 71:916–26 [Google Scholar]
  103. Orton WA. 103.  1902. The wilt diseases of the cowpea and its control. US Dep. Agric. Bur. Plant Ind. Bull. 17:9–20 [Google Scholar]
  104. Osusky M, Zhou G, Osuska L, Hancock RE, Kay WW, Misra S. 104.  2000. Transgenic plants expressing cationic peptide chimeras exhibit broad-spectrum resistance to phytopathogens. Nat. Biotechnol. 18:1162–66 [Google Scholar]
  105. Pajerowska-Mukhtar KM, Mukhtar MS, Guex N, Halim VA, Rosahl S. 105.  et al. 2008. Natural variation of potato allene oxide synthase 2 causes differential levels of jasmonates and pathogen resistance in Arabidopsis. Planta 228:293–306 [Google Scholar]
  106. Pan RS, More TA. 106.  1996. Screening of melon (Cucumis melo L.) germplasm for multiple disease resistance. Euphytica 88:125–28 [Google Scholar]
  107. Pataky J, Williams MM. 107.  2010. Reactions of sweet corn hybrids to prevalent diseases Bull. Univ. Ill. Urbana, IL: [Google Scholar]
  108. Piffanelli P, Zhou F, Casais C, Orme J, Jarosch B. 108.  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]
  109. Poland J. 109.  2010. The Genetic Architecture of Quantitative Resistance in Maize. PhD Thesis, Cornell Univ. Ithaca, NY: [Google Scholar]
  110. Poland JA, Bradbury PJ, Buckler ES, Nelson RJ. 110.  2011. Genome-wide nested association mapping of quantitative resistance to northern leaf blight in maize. PNAS 108:6893–98 [Google Scholar]
  111. Portieles R, Ayra C, Gonzalez E, Gallo A, Rodriguez R. 111.  et al. 2010. Nmdef02, a novel antimicrobial gene isolated from Nicotiana megalosiphon confers high-level pathogen resistance under greenhouse and field conditions. Plant Biotechnol. J. 8:678–90 [Google Scholar]
  112. Pritchard JK, Stephens M, Rosenberg NA, Donnelly P. 112.  2000. Association mapping in structured populations. Am. J. Hum. Genet. 67:170–81 [Google Scholar]
  113. Raffaele S, Bayer E, Lafarge D, Cluzet S, German Retana S. 113.  et al. 2009. Remorin, a Solanaceae protein resident in membrane rafts and plasmodesmata, impairs Potato virus X movement. Plant Cell Online 21:1541–55 [Google Scholar]
  114. Ramalingam J, Vera Cruz CM, Kukreja K, Chittoor JM, Wu J. 114.  et al. 2003. Candidate defense genes from rice, barley, and maize and their association with qualitative and quantitative resistance in rice. Mol. Plant-Microbe Interact. 16:14–24 [Google Scholar]
  115. Risterucci AM, Paulin D, Ducamp M, N’Goran JAK, Lanaud C. 115.  2003. Identification of QTLs related to cocoa resistance to three species of Phytophthora. Theor. Appl. Genet. 108:168–74 [Google Scholar]
  116. Robert-Seilaniantz A, Grant M, Jones JDG. 116.  2011. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu. Rev. Phytopathol. 49:317–43 [Google Scholar]
  117. Rustagi A, Kumar D, Shekhar S, Yusuf MA, Misra S, Sarin NB. 117.  2014. Transgenic Brassica juncea plants expressing MsrA1, a synthetic cationic antimicrobial peptide, exhibit resistance to fungal phytopathogens. Mol. Biotechnol. 56:535–45 [Google Scholar]
  118. Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P. 118.  et al. 2013. Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. Plant Cell Rep. 32:1085–98 [Google Scholar]
  119. Schweizer P, Stein N. 119.  2011. Large-scale data integration reveals colocalization of gene functional groups with meta-QTL for multiple disease resistance in barley. Mol. Plant-Microbe Interact. 24:1492–1501 [Google Scholar]
  120. Silva KJP, Brunings A, Peres NA, Mou Z, Folta KM. 120.  2015. The Arabidopsis NPR1 gene confers broad-spectrum disease resistance in strawberry. Transgenic Res. 24:693–704 [Google Scholar]
  121. Singh A, Singh VK, Singh SP, Pandian RTP, Ellur RK. 121.  et al. 2012. Molecular breeding for the development of multiple disease resistance in Basmati rice. AoB Plants 4:pls029 [Google Scholar]
  122. Smedegaard-Petersen V, Tolstrup K. 122.  1985. The limiting effect of disease resistance on yield. Annu. Rev. Phytopathol. 23:475–90 [Google Scholar]
  123. Spielmeyer W, McIntosh RA, Kolmer J, Lagudah ES. 123.  2005. Powdery mildew resistance and Lr34/Yr18 genes for durable resistance to leaf and stripe rust cosegregate at a locus on the short arm of chromosome 7D of wheat. Theor. Appl. Genet. 111:731–35 [Google Scholar]
  124. St. Clair DA. 124.  2010. Quantitative disease resistance and quantitative resistance loci in breeding. Annu. Rev. Phytopathol. 48:247–68 [Google Scholar]
  125. Sun L, Yang DL, Kong Y, Chen Y, Li XZ. 125.  et al. 2014. Sugar homeostasis mediated by cell wall invertase GRAIN INCOMPLETE FILLING 1 (GIF1) plays a role in pre-existing and induced defence in rice. Mol. Plant Pathol. 15:161–73 [Google Scholar]
  126. Swathi Anuradha T, Divya K, Jami SK, Kirti PB. 126.  2008. Transgenic tobacco and peanut plants expressing a mustard defensin show resistance to fungal pathogens. Plant Cell Rep. 27:1777–86 [Google Scholar]
  127. Takahashi H, Miller J, Nozaki Y, Takeda M, Shar J. 127.  et al. 2002. RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. Plant J. 32:655–67 [Google Scholar]
  128. Tang X, Xie M, Kim YJ, Zhou J, Klessig DF, Martin GF. 128.  1999. Overexpression of Pto activates defense responses and confers broad resistance. Plant Cell 11:15–29 [Google Scholar]
  129. Terán H, Jara C, Mahuku G, Beebe S, Singh SP. 129.  2013. Simultaneous selection for resistance to five bacterial, fungal, and viral diseases in three Andean × Middle American inter-gene pool common bean populations. Euphytica 189:283–92 [Google Scholar]
  130. Terras F. 130.  1995. Small cysteine-rich antifungal proteins from radish: their role in host defense. Plant Cell 7:573–88 [Google Scholar]
  131. Thomma B, Cammue B, Thevissen K. 131.  2002. Plant defensins. Planta 216:193–202 [Google Scholar]
  132. Tian D, Traw M, Chen J, Kreitman M, Bergelson J. 132.  2003. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74–77 [Google Scholar]
  133. Timmerman-Vaughan GM, Frew TJ, Russell AC, Khan T, Butler R. 133.  et al. 2002. QTL mapping of partial resistance to field epidemics of Ascochyta blight of pea. Crop Sci. 42:2100 [Google Scholar]
  134. Todesco M, Balasubramanian S, Hu TT, Traw MB, Horton M. 134.  et al. 2010. Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature 465:632–36 [Google Scholar]
  135. Torres MA, Jones JDG, Dangl JL. 135.  2006. Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141:373–78 [Google Scholar]
  136. Van Der Vossen EAG, Van Der Voort JNAM, Kanyuka K, Bendahmane A, Sandbrink H. 136.  et al. 2000. Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: a virus and a nematode. Plant J. 23:567–76 [Google Scholar]
  137. van Eeuwijk FA, Mesterhazy A, Kling CI, Ruckenbauer P, Saur L. 137.  et al. 1995. Assessing non-specificity of resistance in wheat to head blight caused by inoculation with European strains of Fusarium culmorum, F. graminearum and F. nivale using a multiplicative model for interaction. Theor. Appl. Genet. 90:221–28 [Google Scholar]
  138. Villegas-Fernández AM, Sillero JC, Emeran AA, Flores F, Rubiales D. 138.  2011. Multiple-disease resistance in Vicia faba: multi-environment field testing for identification of combined resistance to rust and chocolate spot. Field Crop. Res. 124:59–65 [Google Scholar]
  139. Vivas M, Silveira SF, Pio-Viana A, Amaral-Júnior AT, Ferreguetti GA, Pereira MG. 139.  2015. Resistance to multiple foliar diseases in papaya genotypes in Brazil. Crop Prot. 71:138–43 [Google Scholar]
  140. Vlot AC, Dempsey DA, Klessig DF. 140.  2009. Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol. 47:177–206 [Google Scholar]
  141. Wallace JG, Bradbury PJ, Zhang N, Gibon Y, Stitt M, Buckler ES. 141.  2014. Association mapping across numerous traits reveals patterns of functional variation in maize. PLOS Genet. 10:e1004845 [Google Scholar]
  142. Wally O, Jayaraj J, Punja ZK. 142.  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]
  143. Wally O, Punja ZK. 143.  2010. Enhanced disease resistance in transgenic carrot (Daucus carota L.) plants over-expressing a rice cationic peroxidase. Planta 232:1229–39 [Google Scholar]
  144. Walters D, Heil M. 144.  2007. Costs and trade-offs associated with induced resistance. Physiol. Mol. Plant Pathol. 71:3–17 [Google Scholar]
  145. Wang G-X, Chen Y, Zhao J-R, Li L, Korban SS. 145.  et al. 2007. Mapping of defense response gene homologs and their association with resistance loci in maize. J. Integr. Plant Biol. 49:1580–98 [Google Scholar]
  146. Webber HJ, Orton WA. 146.  1902. A cowpea resistant to root-knot (Heterodera radicicola). US Dep. Agric. Bur. Plant Ind. Bull. 17:23–26 [Google Scholar]
  147. Wisser RJ, Balint-Kurti PJ, Nelson RJ. 147.  2006. The genetic architecture of disease resistance in maize: a synthesis of published studies. Phytopathology 96:120–29 [Google Scholar]
  148. Wisser RJ, Kolkman JM, Patzoldt ME, Holland JB, Yu J. 148.  et al. 2011. Multivariate analysis of maize disease resistances suggests a pleiotropic genetic basis and implicates a GST gene. PNAS 108:7339–44 [Google Scholar]
  149. Wisser RJ, Sun Q, Hulbert S, Kresovich S, Nelson RJ. 149.  2005. Identification and characterization of regions of the rice genome associated with broad-spectrum, quantitative disease resistance. Genetics 169:2277–93 [Google Scholar]
  150. Wright SAL, Azarang M, Falk AB. 150.  2013. Barley lesion mimics, supersusceptible or highly resistant to leaf rust and net blotch. Plant Pathol. 62:982–92 [Google Scholar]
  151. Wroblewski T, Caldwell KS, Piskurewicz U, Cavanaugh KA, Xu H. 151.  et al. 2009. Comparative large-scale analysis of interactions between several crop species and the effector repertoires from multiple pathovars of Pseudomonas and Ralstonia. Plant Physiol. 150:1733–49 [Google Scholar]
  152. Wroblewski T, Piskurewicz U, Tomczak A, Ochoa O, Michelmore RW. 152.  2007. Silencing of the major family of NBS-LRR-encoding genes in lettuce results in the loss of multiple resistance specificities. Plant J. 51:803–18 [Google Scholar]
  153. Wu C, Bordeos A, Madamba MRS, Baraoidan M, Ramos M. 153.  et al. 2008. Rice lesion mimic mutants with enhanced resistance to diseases. Mol. Genet. Genom. 279:605–19 [Google Scholar]
  154. Yin Z, Chen J, Zeng L, Goh M, Leung H. 154.  et al. 2000. Characterizing rice lesion mimic mutants and identifying a mutant with broad-spectrum resistance to rice blast and bacterial blight. Mol. Plant-Microbe Interact. 13:869–76 [Google Scholar]
  155. Yu D, Chen C, Chen Z. 155.  2001. Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. Plant Cell 13:1527–40 [Google Scholar]
  156. Yu J, Holland JB, McMullen MD, Buckler ES. 156.  2008. Genetic design and statistical power of nested association mapping in maize. Genetics 178:539–51 [Google Scholar]
  157. Zasloff M. 157.  2002. Antimicrobial peptides of multicellular organisms. Nature 415:389–95 [Google Scholar]
  158. Zeng ZB. 158.  1994. Precision mapping of quantitative trait loci. Genetics 136:1457–68 [Google Scholar]
  159. Zhang X, Dai Y, Xiong Y, DeFraia C, Li J. 159.  et al. 2007. Overexpression of Arabidopsis MAP kinase kinase 7 leads to activation of plant basal and systemic acquired resistance. Plant J. 52:1066–79 [Google Scholar]
  160. Zhang XY, Nie ZH, Wang WJ, Leung DWM, Xu DG. 160.  et al. 2013. Relationship between disease resistance and rice oxalate oxidases in transgenic rice. PLOS ONE 8:e78348 [Google Scholar]
  161. Zhang Z, Ersoz E, Lai C, Todhunter RJ, Tiwari HK. 161.  et al. 2010. Mixed linear model approach adapted for genome-wide association studies. Nat. Genet. 42:355–60 [Google Scholar]
  162. Zhou J, Zhang H, Yang Z, Li G, Hu L. 162.  et al. 2012. Characterization of a new T2DS.2DL-?R translocation triticale ZH-1 with multiple resistances to diseases. Genet. Resour. Crop Evol. 59:1161–68 [Google Scholar]
  163. Zhou Y-L, Xu J-L, Zhou S-C, Yu J, Xie X-W. 163.  et al. 2009. Pyramiding Xa23 and Rxo1 for resistance to two bacterial diseases into an elite indica rice variety using molecular approaches. Mol. Breed. 23:279–87 [Google Scholar]
  164. Zipfel C. 164.  2008. Pattern-recognition receptors in plant innate immunity. Curr. Opin. Immunol. 20:10–16 [Google Scholar]
  165. Zwart RS, Thompson JP, Milgate AW, Bansal UK, Williamson PM. 165.  et al. 2010. QTL mapping of multiple foliar disease and root-lesion nematode resistances in wheat. Mol. Breed. 26:107–24 [Google Scholar]
  166. Zwonitzer JC, Coles ND, Krakowsky MD, Arellano C, Holland JB. 166.  et al. 2010. Mapping resistance quantitative trait loci for three foliar diseases in a maize recombinant inbred line population: evidence for multiple disease resistance?. Phytopathology 100:72–79 [Google Scholar]
/content/journals/10.1146/annurev-phyto-080615-100037
Loading
Multiple Disease Resistance in Plants
Annual Review of Phytopathology 54, 229 (2016); https://doi.org/10.1146/annurev-phyto-080615-100037
/content/journals/10.1146/annurev-phyto-080615-100037
/content/journals/10.1146/annurev-phyto-080615-100037
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

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