Quantitative Resistance to Biotrophic Filamentous Plant Pathogens: Concepts, Misconceptions, and Mechanisms

Annual Review of Phytopathology

Volumn 53, Issue , 2015, Pages 445-470

  Niks, Rients E ^a   Qi, Xiaoquan ^b   Marcel, Thierry C ^c  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b INSTITUTE OF BOTANY   (China)

^c INRA Institut National de la Recherche Agronomique   (France)

Author keywords

Basal resistance; Durability; Effector targets; Mechanisms; Partial resistance

Indexed keywords

ANTIBIOSIS; GENETICS; IMMUNOLOGY; MICROBIOLOGY; PLANT; PLANT DISEASE;

ANTIBIOSIS; PLANT DISEASES; PLANTS;

EID: 84938692800     PISSN: 00664286     EISSN: 15452107     Source Type: Book Series    
DOI: 10.1146/annurev-phyto-080614-115928     Document Type: Article

References (138)

1. Aghnoum R, Marcel TC, Johrde A, Pecchioni N, Schweizer P, Niks RE. 2010. Basal resistance of barley to barley powdery mildew: connectingQTLs and candidate genes. Mol. Plant-Microbe Interact. 23:91-102
2. Aghnoum R, Niks RE. 2010. Specificity and levels of nonhost resistance of barley to nonadapted Blumeria graminis forms. New Phytol. 185:275-84
3. Aghnoum R, Niks RE. 2011. Transgressive segregation for very low and high levels of basal resistance to powdery mildew in barley. J. Plant Physiol. 168:45-50
4. Alpy F, Tomasetto C. 2005. Give lipids a START: the StAR-related lipid transfer (START) domain in mammals. J. Cell Sci. 118:2791-801
5. Andrivon D, Pilet F, Montarry J, Hafidi M, Corbière R, et al. 2007. Adaptation of Phytophthora infestans to partial resistance in potato: evidence from French and Moroccan populations. Phytopathology 97:338-43
6. Arru L, Francia E, Pecchioni N. 2003. Isolate-specific QTLs of resistance to leaf stripe (Pyrenophora graminea) in the "Steptoe" × "Morex" spring barley cross. Theor. Appl. Genet. 106:668-75
7. Azzimonti G, Marcel TC, Robert OPS, Lannou C, Paillard S, Goyeau H. 2014. Diversity, specificity and impacts on field epidemics of QTLs involved in components of quantitative resistance in the wheat leaf rust pathosystem. Mol. Breed. 34:549-67
8. Bai Y, Pavan S, Zheng Z, Zappel NF, Reinstädler A, et al. 2008. Naturally occurring broad-spectrum powdery mildew resistance in a central american tomato accession is caused by loss of Mlo function. Mol. Plant-Microbe Interact. 21:30-39
9. Bai Y, van der Hulst R, Bonnema G, Marcel TC, Meijer-Dekens F, et al. 2005. Tomato defense to Oidium neolycopersici: dominant Ol genes confer isolate-dependent resistance via a different mechanism than recessive ol-2. Mol. Plant-Microbe Interact. 18:354-62
10. Barilli E, Sillero JC, Fernández-Aparicio M, Rubiales D. 2009. Identification of resistance to Uromyces pisi (Pers.) Wint. in Pisum spp. germplasm. Field Crops Res. 114:198-203
11. Bos JIB, Armstrong MR, Gilroy EM, Boevink PC, Hein I, et al. 2010. Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. PNAS 107:9909-14
12. Bozkurt TO, Schornack S, Win J, Shindo T, Ilyas M, et al. 2011. Phytophthora infestans effector AVRblb2 prevents secretion of a plant immune protease at the haustorial interface. PNAS 108:20832-37
13. Broers LHM, Jacobs T. 1989. The inheritance of host plant effect on latency period of wheat leaf rust in spring wheat. II. Number of segregating factors and evidence for transgressive segregation in F3 and F5 generations. Euphytica 44:207-14
14. Cao XH, Zhou JH, Gong XP, Zhao GY, Jia JZ, et al. 2012. Identification and validation of a major quantitative trait locus for slow-rusting resistance to stripe rust in wheat. J. Integr. Plant Biol. 54:330-44
15. Chen H, Wang S, Xing Y, Xu C, Hayes PM, et al. 2003. Comparative analyses of genomic locations and pathotype specificities of loci for quantitative resistance to Pyricularia grisea in rice and barley. PNAS 100:2544-49
16. Chen LQ, Hou BH, Lalonde S, TakanagaH, HartungML, et al. 2010. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527-32
17. ChenXW, Hackett CA, Niks RE, Hedley PE, Booth C, et al. 2010. AneQTLanalysis of partial resistance to Puccinia hordei in barley. PLOS ONE 5:e8598
18. Chowdhury ABMNU, Bremer GB, SaltDW, Miller P, Ford MG. 2003. A method of delivering Blumeria graminis f. Sp. Hordei spores for laboratory experiments. Crop Prot. 22:917-22
19. Collins NC, Niks RE, Schulze-Lefert P. 2007. Resistance to cereal rusts at the plant cell wall-what can we learn from other host-pathogen systems? Aust. J. Agric. Res. 58:476-89
20. Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, et al. 2003. SNARE-proteinmediated disease resistance at the plant cell wall. Nature 425:973-77
21. 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
22. Dangl JL, Jones JDG. 2001. Plant pathogens and integrated defence responses to infection. Nature 411:826-33
23. Dardick C, Ronald P. 2006. Plant and animal pathogen recognition receptors signal through non-RD kinases. PLOS Pathog. 2:e2
24. de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y, et al. 2010. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953-55
25. Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11:539-48
26. Doehlemann G, Hemetsberger C. 2013. Apoplastic immunity and its suppression by filamentous plant pathogens. New Phytol. 198:1001-16
27. Dong S, Stam R, Cano LM, Song J, Sklenar J, et al. 2014. Effector specialization in a lineage of the Irish potato famine pathogen. Science 343:552-55
28. Douchkov D, Johrde A, Nowara D, Himmelbach A, Lueck S, et al. 2011. Convergent evidence for a role of WIR1 proteins during the interaction of barley with the powdery mildew fungus Blumeria graminis. J. Plant Physiol. 168:20-29
29. Dyck PL. 1977. Genetics of leaf rust reaction in three introductions of common wheat. Can. J. Genet. Cytol. 19:711-16
30. Dyck PL. 1979. Identification of the gene for adult plant leaf rust resistance in Thatcher. Can. J. Plant Sci. 59:499-501
31. Dyck PL. 1987. The association of a gene for leaf rust resistance with the chromosome 7D suppressor of stem rust resistance in common wheat. Genome 29:467-69
32. Dyck PL, Samborski DJ, Anderson RG. 1966. Inheritance of adult-plant leaf rust resistance derived from the common wheat varieties Exchange and Frontana. Can. J. Genet. Cytol. 8:665-71
33. Eyal Z, Clifford BC, Caldwell RM. 1968. A settling tower for quantitative inoculation of leaf blades of mature small grain plants with urediospores. Phytopathology 58:530-31
34. Fabro G, Steinbrenner J, Coates M, Ishaque N, Baxter L, et al. 2011. Multiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity. PLOS Pathog. 7:e1002348
35. Fernández-Aparicio M, Barilli E, Mansilla F, Rubiales D. 2011. Identification and characterisation of resistance against rust (Puccinia allii ) in garlic (Allium sp.) germplasm. Ann. Appl. Biol. 159:93-98
36. Fernandez J, Wilson RA. 2012. Why no feeding frenzy? Mechanisms of nutrient acquisition and utilization during infection by the rice blast fungus Magnaporthe oryzae. Mol. Plant-Microbe Interact. 25:1286-93
37. Franckowiak JD, Jin Y, Steffenson BJ. 1997. Recommended allele symbols for leaf rust resistance genes in barley. Barley Genet. Newsl. 27:36-44
38. Fu D, Uauy C, Distelfeld A, Blechl A, Epstein L, et al. 2009. A kinase-START gene confers temperaturedependent resistance to wheat stripe rust. Science 323:1357-60
39. Fukuoka S, Okuno K. 2001. QTL analysis and mapping of pi21, a recessive gene for field resistance to rice blast in Japanese upland rice. Theor. Appl. Genet. 103:185-90
40. 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
41. Geffroy V, Sevignac M, De Oliveira JCF, Fouilloux G, Skroch P, et al. 2000. Inheritance of partial resistance against Colletotrichum lindemuthianum in Phaseolus vulgaris and co-localization of quantitative trait loci with genes involved in specific resistance. Mol. Plant-Microbe Interact. 13:287-96
42. Gilroy EM, Taylor RM, Hein I, Boevink P, Sadanandom A, et al. 2011. CMPG1-dependent cell death follows perception of diverse pathogen elicitors at the host plasma membrane and is suppressed by Phytophthora infestans RXLR effector AVR3a. New Phytol. 190:653-66
43. Giraldo MC, Valent B. 2013. Filamentous plant pathogen effectors in action. Nat. Rev. Microbiol. 11:800-14
44. Glazebrook J. 2001. Genes controlling expression of defense responses in Arabidopsis-2001 status. Curr. Opin. Plant Biol. 4:301-8
45. González AM, Marcel TC, Kohutova Z, Stam P, van der Linden CG, et al. 2010. Peroxidase profiling reveals genetic linkage between peroxidase gene clusters and basal host and non-host resistance to rusts and mildew in barley. PLOS ONE 5:e10495
46. González AM, Marcel TC, Niks RE. 2012. Evidence for a minor gene-for-minor gene interaction explaining nonhypersensitive polygenic partial disease resistance. Phytopathology 102:1086-93
47. Grand X, Espinoza R, Michel C, Cros S, Chalvon V, et al. 2012. Identification of positive and negative regulators of disease resistance to rice blast fungus using constitutive gene expression patterns. Plant Biotechnol. J. 10:840-50
48. Hemetsberger C, Herrberger C, Zechmann B, Hillmer M, Doehlemann G. 2012. The Ustilago maydis effector Pep1 suppresses plant immunity by inhibition of host peroxidase activity. PLOS Pathog. 8:e1002684
49. Hickey LT, Lawson W, Platz GJ, Dieters M, Franckowiak J. 2012. Origin of leaf rust adult plant resistance gene Rph20 in barley. Genome 55:396-99
50. Ingle RA, Carstens M, Denby KJ. 2006. PAMP recognition and the plant-pathogen arms race. BioEssays 28:880-89
51. Jafary H, Albertazzi G, Marcel TC, Niks RE. 2008. High diversity of genes for nonhost resistance of barley to heterologous rust fungi. Genetics 178:2327-39
52. Jafary H, Szabo LJ, Niks RE. 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
53. Jarosch B, Kogel KH, Schaffrath U. 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. 12:508-14
54. Johnson R. 1981. Durable resistance: definition of, genetic control, and attainment in plant breeding. Phytopathology 71:567-68
55. Johnston PA, Niks RE, Meiyalaghan V, Blanchet E, Pickering RA. 2013. Rph22: mapping of a novel leaf rust resistance gene introgressed from the non-host Hordeum bulbosum L. into cultivated barley (Hordeum vulgare L.). Theor. Appl. Genet. 126:1613-25
56. Jones IT. 1983. Transgressive segregation for enhanced level of adult plant resistance to mildew in the oat cross Mostyn × Maldwyn. Euphytica 32:499-503
57. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:323-29
58. Jorge V, Dowkiw A, Faivre-Rampant P, Bastien C. 2005. Genetic architecture of qualitative and quantitative Melampsora larici-populina leaf rust resistance in hybrid poplar: genetic mapping andQTL detection. New Phytol. 167:113-27
59. Jorgensen JH, Mortensen K. 1977. Primary infection by Erysiphe graminis f. Sp. Hordei of barley mutants with resistance genes in the ml-o locus. Phytopathology 67:678-85
60. Jorgensen LN, Hovmoller MS, Hansen JG, Lassen P, Clark B, et al. 2014. IPM strategies and their dilemmas including an introduction to www.eurowheat.org. J. Integr. Agric. 13:265-81
61. Kaschani F, Shabab M, Bozkurt T, Shindo T, Schornack S, et al. 2010. An effector-targeted protease contributes to defense against Phytophthora infestans and is under diversifying selection in natural hosts. Plant Physiol. 154:1794-804
62. 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
63. King SRF, McLellan H, Boevink PC, Armstrong MR, Bukharova T, et al. 2014. Phytophthora infestans RXLR effector PexRD2 interacts with host MAPKKKε to suppress plant immune signaling. Plant Cell 26:1345-59
64. Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, et al. 2009. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360-63
65. Lagudah ES. 2011. Molecular genetics of race non-specific rust resistance in wheat. Euphytica 179:81-91
66. 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
67. Lewis J, Wan J, Ford R, Gong Y, Fung P, et al. 2012. Quantitative interactor screening with nextgeneration sequencing (QIS-Seq) identifies Arabidopsis thaliana MLO2 as a target of the Pseudomonas syringae type III effector HopZ2. BMC Genomics 13:8
68. Lipka U, Fuchs R, Lipka V. 2008. Arabidopsis non-host resistance to powdery mildews. Curr. Opin. Plant Biol. 11:404-11
69. Lipka U, Fuchs R, Kuhns C, Petutsching E, Lipka V. 2010. Live and let die-Arabidopsis nonhost resistance to powdery mildews. Eur. J. Cell Biol. 89:194-99
70. Lüthje S, Meisrimler C-N, Hopff D, Möller B. 2011. Phylogeny, topology, structure and functions of membrane-bound class III peroxidases in vascular plants. Phytochemistry 72:1124-35
71. Mackey D, McFall AJ. 2006. MAMPs and MIMPs: proposed classifications for inducers of innate immunity. Mol. Microbiol. 61:1365-71
72. Manosalva PM, Davidson RM, Liu B, Zhu X, Hulbert SH, 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
73. Marcel TC, Gorguet B, Truong TAM, Kohutova Z, Vels A, Niks RE. 2008. Isolate specificity of quantitative trait loci for partial resistance of barley to Puccinia hordei confirmed in mapping populations and near-isogenic lines. New Phytol. 177:743-55
74. Marcel TC, Varshney R, Barbieri M, Jafary H, de Kock M, et al. 2007. A high-density consensus map of barley to compare the distribution of QTLs for partial resistance to Puccinia hordei and of defence gene homologues. Theor. Appl. Genet. 114:487-500
75. McDonald BA, Linde C. 2002. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40:349-79
76. McGrann GRD, Stavrinides A, Russell J, Corbitt MM, Booth A, 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
77. McIntosh RA. 1992. Close genetic linkage of genes conferring adult-plant resistance to leaf rust and stripe rust in wheat. Plant Pathol. 41:523-27
78. Michelmore RW, Christopoulou M, Caldwell KS. 2013. Impacts of resistance gene genetics, function, and evolution on a durable future. Annu. Rev. Phytopathol. 51:291-319
79. Miclot AS, Wiedemann-Merdinoglu S, Duchêne E, Merdinoglu D, Mestre P. 2012. A standardised method for the quantitative analysis of resistance to grapevine powdery mildew. Eur. J. Plant Pathol. 133:483-95
80. Mundt CC. 2014. Durable resistance: A key to sustainable management of pathogens and pests. Infect. Genet. Evol. 27:446-55
81. Naerstad R, Hermansen A, Bjor T. 2007. Exploiting host resistance to reduce the use of fungicides to control potato late blight. Plant Pathol. 56:156-66
82. Niks RE. 1986. Failure of haustorial development as a factor in slow growth and development of Puccinia hordei in partially resistant barley seedlings. Physiol. Mol. Plant Pathol. 28:309-22
83. Niks RE, Kuiper HJ. 1983. Histology of the relation between minor and major genes for resistance of barley to leaf rust. Phytopa-thology 73:55-59
84. Niks RE, Marcel TC. 2009. Nonhost and basal resistance: how to explain specificity? New Phytol. 182:817-28
85. Niks RE, Rubiales D. 2002. Potentially durable resistance mechanisms in plants to specialised fungal pathogens. Euphytica 124:201-16
86. Niks RE, Walther U, Jaiser U, Martínez F, Rubiales D, et al. 2000. Resistance against barley leaf rust (Puccinia hordei ) in West-European spring barley germplasm. Agronomie 20:769-82
87. Ökmen B, Doehlemann G. 2014. Inside plant: biotrophic strategies to modulate host immunity and metabolism. Curr. Opin. Plant Biol. 20:19-25
88. Park C-H, Chen S, Shirsekar G, Zhou B, Khang CH, et al. 2012. The Magnaporthe oryzae effector AvrPiz-t targets theRINGE3 ubiquitin ligase APIP6 to suppress pathogen-associated molecular pattern-triggered immunity in rice. Plant Cell 24:4748-62
89. Parlevliet JE. 1978. Race-specific aspects of polygenic resistance of barley to leaf rust, Puccinia hordei. Neth. J. Plant Pathol. 84:121-26
90. Parlevliet JE. 1979. Components of resistance that reduce the rate of epidemic development. Annu. Rev. Phytopathol. 17:203-22
91. Parlevliet JE, Leijn M, van Ommeren A. 1985. Accumulating polygenes for partial resistance in barley to barley leaf rust, Puccinia hordei. II. Field evaluation. Euphytica 34:15-20
92. Parlevliet JE, Lindhout WH, van Ommeren A, Kuiper HJ. 1980. Level of partial resistance to leaf rust Puccinia hordei, in West-European barley and how to select for it. Euphytica 29:1-8
93. Parlevliet JE, van Ommeren A. 1975. Partial resistance of barley to leaf rust, Puccinia hordei. II. Relationship between field trials, micro plot tests and latent period. Euphytica 24:293-303
94. Parlevliet JE, van Ommeren A. 1988. Accumulation of partial resistance in barley to barley leaf rust and powdery mildew through recurrent selection against susceptibility. Euphytica 37:261-74
95. Parlevliet JE, Zadoks JC. 1977. The integrated concept of disease resistance: A new view including horizontal and vertical resistance in plants. Euphytica 26:5-21
96. Passardi F, Cosio C, Penel C, Dunand C. 2005. Peroxidases have more functions than a Swiss army knife. Plant Cell Rep. 24:255-65
97. Pavan S, Jacobsen E, Visser RGF, Bai Y. 2010. Loss of susceptibility as a novel breeding strategy for durable and broad-spectrum resistance. Mol. Breed. 25:1-12
98. Pawson T. 1995. Protein modules and signalling networks. Nature 373:573-80
99. Perchepied L, Dogimont C, Pitrat M. 2005. Strain-specific and recessive QTLs involved in the control of partial resistance to Fusarium oxysporum f. Sp. Melonis race 1.2 in a recombinant inbred line population of melon. Theor. Appl. Genet. 111:65-74
100. Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ. 2009. Shades of gray: the world of quantitative disease resistance. Trends Plant Sci. 14:21-29
101. Qi X, Fufa F, Niks RE, Lindhout P, Stam P. 2000. The evidence for abundance of QTLs for partial resistance to Puccinia hordei on the barley genome. Mol. Breed. 6:1-9
102. Qi X, Jiang GL, Chen WQ, Niks RE, Stam P, et al. 1999. Isolate-specific QTLs for partial resistance to Puccinia hordei in barley. Theor. Appl. Genet. 99:877-84
103. Qi X, Niks RE, Stam P, Lindhout P. 1998. Identification of QTLs for partial resistance to leaf rust (Puccinia hordei ) in barley. Theor. Appl. Genet. 96:1205-15
104. Roderick HW, Jones IT. 1991. The evaluation of adult plant resistance to powdery mildew (Erysiphe graminis f. Sp. Avenae) in transgressive lines of oats. Euphytica 53:143-49
105. Rooney HCE, van't Klooster JW, van der Hoorn RAL, Joosten MHAJ, Jones JDG, et al. 2005. Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308:1783-86
106. Rubiales D, Niks RE. 1995. Characterization of Lr34, a major gene conferring nonhypersensitive resistance to wheat leaf rust. Plant Dis. 79:1208-12
107. Rubiales D, Fondevilla S, Chen W, Gentzbittel L, Higgins TJV, et al. 2015. Achievements and challenges in legume breeding for pest and disease resistance. Crit. Rev. Plant Sci. 34:195-236
108. Schmidt SM, Kuhn H, Micali C, Liller C, Kwaaitaal M, Panstruga R. 2014. Interaction of a Blumeria graminis f. Sp. Hordei effector candidate with a barley ARF-GAP suggests that host vesicle trafficking is a fungal pathogenicity target. Mol. Plant Pathol. 15:535-49
109. Schouten HJ, Krauskopf J, Visser RGF, Bai YL. 2014. Identification of candidate genes required for susceptibility to powdery or downy mildew in cucumber. Euphytica 200:475-86
110. Schwarzbach E. 2004. Efficient low cost methods in epidemiology of airborne pathogens. Presented at Int. Cereal Rusts Powdery Mildews Conf., 11th, Norwich, UK
111. Schweizer P, Stein N. 2011. Large-scale data integration reveals colocalization of gene functional groups with Meta-QTL for multiple disease resistance in barley. Mol. Plant-Microbe Interact. 24:1492-501
112. Shabab M, Shindo T, Gu C, Kaschani F, Pansuriya T, et al. 2008. Fungal effector protein AVR2 targets diversifying defense-related Cys proteases of tomato. Plant Cell 20:1169-83
113. Sillero JC, Rubiales D. 2002. Histological characterization of the resistance of faba bean to faba bean rust. Phytopathology 92:294-99
114. Singh RP. 1992. Genetic association of leaf rust resistance gene Lr34 with adult plant resistance to stripe rust in bread wheat. Genetics 82:835-38
115. Song J, Win J, Tian M, Schornack S, Kaschani F, et al. 2009. Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. PNAS 106:1654-59
116. Spielmeyer W, McIntosh RA, Kolmer J, Lagudah ES. 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
117. St. Clair DA. 2010. Quantitative disease resistance and quantitative resistance loci in breeding. Annu. Rev. Phytopathol. 48:247-68
118. Tanaka S, Brefort T, Neidig N, Djamei A, Kahnt J, et al. 2014. A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize. ELife 3:e01355
119. Tian M, Win J, Song J, van der Hoorn R, van der Knaap E, Kamoun S. 2007. A Phytophthora infestans cystatin-like protein targets a novel tomato papain-like apoplastic protease. Plant Physiol. 143:364-77
120. Torp J, Jensen HP, Jorgensen JH. 1978. Powdery mildew resistance genes in 106 Northwest European spring barley varieties. Kgl. Vet. Landbohojsk.Årsskr. 1978:75-102
121. Uauy C, Brevis JC, Chen X, Khan I, Jackson L, et al. 2005. High-temperature adult-plant (HTAP) stripe rust resistance gene Yr36 from Triticum turgidum ssp. dicoccoides is closely linked to the grain protein content locus Gpc-B1. Trends Microbiol. 112:97-105
122. van den Burg HA, Harrison SJ, Joosten MHAJ, Vervoort J, De Wit PJGM. 2006. Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol. Plant-Microbe Interact. 19:1420-30
123. van den Burg HA, Westerink N, Francoijs K-J, Roth R, Woestenenk E, et al. 2003. Natural disulfide bond-disrupted mutants ofAVR4of the tomato pathogen Cladosporium fulvum are sensitive to proteolysis, circumvent Cf-4-mediated resistance, but retain their chitin binding ability. J. Biol. Chem. 278:27340-46
124. van der Hoorn RAL, Kamoun S. 2008. From guard to decoy: A new model for perception of plant pathogen effectors. Plant Cell 20:2009-17
125. van Esse HP, van't Klooster JW, Bolton MD, Yadeta KA, van Baarlen P, et al. 2008. The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. Plant Cell 20:1948-63
126. Vergne E, Grand X, Ballini E, Chalvon V, Saindrenan P, et al. 2010. Preformed expression of defense is a hallmark of partial resistance to rice blast fungal pathogen Magnaporthe oryzae. BMC Plant Biol. 10:206
127. WallworkH, Johnson R. 1984. Transgressive segregation for resistance to yellow rust in wheat. Euphytica 33:123-32
128. Wang L, Wang Y, Marcel TC, Niks RE, Qi X. 2010. The phenotypic expression of QTLs for partial resistance to barley leaf rust during plant development. Theor. Appl. Genet. 121:857-64
129. Yeo FKS, Hensel G, Vozábová T, Martin-Sanz A, Marcel TC, et al. 2014. Golden SusPtrit: A genetically well transformable barley line for studies on the resistance to rust fungi. Theor. Appl. Genet. 127:325-37
130. Zahirul IT, Talukdar ZI, Tharreau D, Price AH. 2004. Quantitative trait loci analysis suggests that partial resistance to rice blast is mostly determined by race-specific interactions. New Phytol. 162:197-209
131. Zhan J, Fitt BDL, Pinnschmidt HO, Oxley SJP, Newton AC. 2008. Resistance, epidemiology and sustainable management of Rhynchosporium secalis populations on barley. Plant Pathol. 57:1-14
132. Zhang M, Li Q, Liu T, Liu L, Shen D, et al. 2015. Two cytoplasmic effectors of Phytophthora sojae regulate plant cell death via interactions with plant catalases. Plant Physiol. 167:164-75
133. Zhang NW, Pelgrom K, Niks RE, Visser RGF, Jeuken MJW. 2009. Three combined quantitative trait loci from nonhost Lactuca saligna are sufficient to provide complete resistance of lettuce against Bremia lactucae. Mol. Plant-Microbe Interact. 22:1160-68
134. Zhang W-J, Pedersen C, Kwaaitaal M, Gregersen PL, Morch SM, et al. 2012. Interaction of barley powdery mildew effector candidate CSEP0055 with the defence protein PR17c. Mol. Plant Pathol. 13:1110-19
135. Zhang Y, Lubberstedt T, Xu ML. 2013. The genetic and molecular basis of plant resistance to pathogens. J. Genet. Genomics 40:23-35
136. Zheng Z, Nonomura T, Appiano M, Pavan S, Matsuda Y, et al. 2013. Loss of function in Mlo orthologs reduces susceptibility of pepper and tomato to powdery mildew disease caused by Leveillula taurica. PLOS ONE 8:e70723
137. Zhu YJ, Zuo SM, Chen ZX, Chen XG, Li G, et al. 2014. Identification of two major rice sheath blight resistance QTLs, qSB1-1(HJX74) and qSB11(HJX74), in field trials using chromosome segment substitution lines. Plant Dis. 98:1112-21
138. Zimmermann G, Baumlein H, Mock H, Himmelbach A, Schweizer P. 2006. The multigene family encoding germin-like proteins of barley: regulation and function in basal host resistance. Plant Physiol. 142:181-92