1932

Abstract

Canola is an important oilseed crop, providing food, feed, and fuel around the world. However, blackleg disease, caused by the ascomycete , causes significant yield losses annually. With the recent advances in genomic technologies, the understanding of the interaction has rapidly increased, with numerous and genes cloned, setting this system up as a model organism for studying plant–pathogen associations. Although the interaction follows Flor's gene-for-gene hypothesis for qualitative resistance, it also puts some unique spins on the interaction. This review discusses the current status of the host–pathogen interaction and highlights some of the future gaps that need addressing moving forward.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-021621-120602
2022-08-26
2024-06-18
Loading full text...

Full text loading...

/deliver/fulltext/phyto/60/1/annurev-phyto-021621-120602.html?itemId=/content/journals/10.1146/annurev-phyto-021621-120602&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Adli M. 2018. The CRISPR tool kit for genome editing and beyond. Nat. Commun. 9:1911
    [Google Scholar]
  2. 2.
    Akcapinar GB, Kappel L, Sezerman OU, Seidl-Seiboth V. 2015. Molecular diversity of LysM carbohydrate-binding motifs in fungi. Curr. Genet. 61:103–13
    [Google Scholar]
  3. 3.
    Albert I, Bohm 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]
  4. 4.
    Albert I, Hua C, Nürnberger T, Pruitt RN, Zhang L. 2019. Surface sensor systems in plant immunity. Plant Physiol 182:1582–96
    [Google Scholar]
  5. 5.
    Amas J, Anderson R, Edwards D, Cowling W, Batley J. 2021. Status and advances in mining for blackleg (Leptosphaeria maculans) quantitative resistance (QR) in oilseed rape (Brassica napus). Theor. Appl. Genet. 134:3123–45
    [Google Scholar]
  6. 6.
    Ansan-Melayah D, Balesdent MH, Delourme R, Pilet ML, Tanguy X et al. 1998. Genes for race-specific resistance against blackleg disease in Brassica napus L. Plant Breed. 117:373–78
    [Google Scholar]
  7. 7.
    Bacete L, Melida H, Miedes E, Molina A. 2018. Plant cell wall-mediated immunity: cell wall changes trigger disease resistance responses. Plant J. 93:614–36
    [Google Scholar]
  8. 8.
    Balesdent MH, Attard A, Kuhn ML, Rouxel T. 2002. New avirulence genes in the phytopathogenic fungus Leptosphaeria maculans. Phytopathology 92:1122–33
    [Google Scholar]
  9. 9.
    Balesdent MH, Fudal I, Ollivier B, Bally P, Grandaubert J et al. 2013. The dispensable chromosome of Leptosphaeria maculans shelters an effector gene conferring avirulence towards Brassica rapa. New Phytol. 198:887–98
    [Google Scholar]
  10. 10.
    Becker MG, Haddadi P, Wan J, Adam L, Walker P et al. 2019. Transcriptome analysis of Rlm2-mediated host immunity in the Brassica napus-Leptosphaeria maculans pathosystem. Mol. Plant-Microbe Interact. 32:1001–12
    [Google Scholar]
  11. 11.
    Becker MG, Zhang X, Walker PL, Wan JC, Millar JL et al. 2017. Transcriptome analysis of the Brassica napus-Leptosphaeria maculans pathosystem identifies receptor, signaling and structural genes underlying plant resistance. Plant J. 90:573–86
    [Google Scholar]
  12. 12.
    Bent AF, Mackey D. 2007. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 45:399–436
    [Google Scholar]
  13. 13.
    Bi G, Zhou JM. 2017. MAP kinase signaling pathways: a hub of plant-microbe interactions. Cell Host Microbe 21:270–73
    [Google Scholar]
  14. 14.
    Birkenbihl RP, Diezel C, Somssich IE. 2012. Arabidopsis WRKY33 is a key transcriptional regulator of hormonal and metabolic responses toward Botrytis cinerea infection. Plant Physiol 159:266–85
    [Google Scholar]
  15. 15.
    Blondeau K, Blaise F, Graille M, Kale SD, Linglin J et al. 2015. Crystal structure of the effector AvrLm4-7 of Leptosphaeria maculans reveals insights into its translocation into plant cells and recognition by resistance proteins. Plant J. 83:610–24
    [Google Scholar]
  16. 16.
    Bourdais G, Burdiak P, Gauthier A, Nitsch L, Salojarvi J et al. 2015. Large-scale phenomics identifies primary and fine-tuning roles for CRKs in responses related to oxidative stress. PLOS Genet. 11:e1005373
    [Google Scholar]
  17. 17.
    Bousset L, Ermel M, Lebreton L. 2018. The full life cycle of Leptosphaeria maculans completed on inoculated oilseed rape incubated under controlled conditions. Plant Pathol. 67:1321–28
    [Google Scholar]
  18. 18.
    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]
  19. 19.
    Brun H, Chevre AM, Fitt BD, Powers S, Besnard AL et al. 2010. Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytol 185:285–99
    [Google Scholar]
  20. 20.
    Cargeeg L, Thurling NJC. 1980. Seedling and adult plant resistance to blackleg (Leptosphaeria maculans (Desm.) Ces. et de Not.) in spring rape (Brassica napus L.). Crop Pasture Sci. 31:37–46
    [Google Scholar]
  21. 21.
    Chalhoub B, Denoeud F, Liu S, Parkin IA, Tang H et al. 2014. Plant genetics. Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345:950–53
    [Google Scholar]
  22. 22.
    Cook DE, Mesarich CH, Thomma BPHJ. 2015. Understanding plant immunity as a surveillance system to detect invasion. Annu. Rev. Phytopathol. 53:541–63
    [Google Scholar]
  23. 23.
    Crouch JH, Lewis BG, Mithen RF. 1994. The effect of a genome substitution on the resistance of Brassica napus to infection by Leptosphaeria maculans. Plant Breed. 112:265–78
    [Google Scholar]
  24. 24.
    de Wit PJ. 2016. Apoplastic fungal effectors in historic perspective; a personal view. New Phytol. 212:805–13
    [Google Scholar]
  25. 25.
    Degrave A, Wagner M, George P, Coudard L, Pinochet X et al. 2021. A new avirulence gene of Leptosphaeria maculans, AvrLm14, identifies a resistance source in American broccoli (Brassica oleracea) genotypes. Mol. Plant Pathol. 22:121599–612
    [Google Scholar]
  26. 26.
    Delourme R, Brun H, Ermel M, Lucas MO, Vallee P et al. 2008. Expression of resistance to Leptosphaeria maculans in Brassica napus double haploid lines in France and Australia is influenced by location. Ann. Appl. Biol. 153:259–69
    [Google Scholar]
  27. 27.
    Delourme R, Chèvre AM, Brun H, Rouxel T, Balesdent MH et al. 2006. Major gene and polygenic resistance to Leptosphaeria maculans in oilseed rape (Brassica napus). Eur. J. Plant Pathol. 114:41–52
    [Google Scholar]
  28. 28.
    Devendrakumar KT, Li X, Zhang Y. 2018. MAP kinase signaling: interplays between plant PAMP- and effector-triggered immunity. Cell. Mol. Life Sci. 75:2981–89
    [Google Scholar]
  29. 29.
    Dion Y, Gugel RK, Rakow GF, Seguin-Swartz G, Landry BS. 1995. RFLP mapping of resistance to the blackleg disease [causal agent, Leptosphaeria maculans (Desm.) Ces. et de Not.] in canola (Brassica napus L.). Theor. Appl. Genet. 91:1190–94
    [Google Scholar]
  30. 30.
    Dixon MS, Golstein C, Thomas CM, van der Biezen EA, Jones JDG. 2000. Genetic complexity of pathogen perception by plants: the example of Rcr3, a tomato gene required specifically by Cf-2. PNAS 97:8807–14
    [Google Scholar]
  31. 31.
    Elliott VL, Marcroft SJ, Howlett BJ, Van de Wouw AP. 2016. Gene-for-gene resistance is expressed in cotyledons, leaves and pods, but not during late stages of stem colonisation in the Leptosphaeria maculans-Brassica napus pathosystem. Plant Breed. 135:200–7
    [Google Scholar]
  32. 32.
    Ferreira MES, Rimmer SR, Williams PH, Osborn TCJP. 1995. Mapping loci controlling Brassica napus resistance to Leptosphaeria maculans under different screening conditions. Phytopathology 85:213–17
    [Google Scholar]
  33. 33.
    Fitt BDL, Brun H, Barbetti MJ, Rimmer SR. 2006. World-wide importance of phoma stem canker (Leptosphaeria maculans and L. biglobosa) on oilseed rape (Brassica napus). Eur. J. Plant Pathol. 114:3–15
    [Google Scholar]
  34. 34.
    Fitt BDL, Huang YJ, van den Bosch F, West JS. 2006. Coexistence of related pathogen species on arable crops in space and time. Annu. Rev. Phytopathol. 44:163–68
    [Google Scholar]
  35. 35.
    Flor HH. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275–96
    [Google Scholar]
  36. 36.
    Fudal I, Ross S, Gout L, Blaise F, Kuhn ML et al. 2007. Heterochromatin-like regions as ecological niches for avirulence genes in the Leptosphaeria maculans genome: map-based cloning of AvrLm6. Mol. Plant-Microbe Interact. 20:459–70
    [Google Scholar]
  37. 37.
    Gadaleta A, Colasuonno P, Giove SL, Blanco A, Giancaspro A. 2019. Map-based cloning of QFhb.mgb-2A identifies a WAK2 gene responsible for Fusarium head blight resistance in wheat. Sci. Rep. 9:6929
    [Google Scholar]
  38. 38.
    Gay EJ, Soyer JL, Lapalu N, Linglin J, Fudal I et al. 2021. Large-scale transcriptomics to dissect 2 years of the life of a fungal phytopathogen interacting with its host plant. BMC Biol 19:55
    [Google Scholar]
  39. 39.
    Gervais J, Plissonneau C, Linglin J, Meyer M, Labadie K et al. 2017. Different waves of effector genes with contrasted genomic location are expressed by Leptosphaeria maculans during cotyledon and stem colonization of oilseed rape. Mol. Plant Pathol. 18:1113–26
    [Google Scholar]
  40. 40.
    Ghanbarnia K, Fudal I, Larkan NJ, Links MG, Balesdent MH et al. 2015. Rapid identification of the Leptosphaeria maculans avirulence gene AvrLm2 using an intraspecific comparative genomics approach. Mol. Plant Pathol. 16:699–709
    [Google Scholar]
  41. 41.
    Ghanbarnia K, Ma L, Larkan NJ, Haddadi P, Fernando WGD, Borhan MH. 2018. Leptosphaeria maculans AvrLm9: a new player in the game of hide and seek with AvrLm4-7. Mol. Plant Pathol. 19:1754–64
    [Google Scholar]
  42. 42.
    Gobert A, Park G, Amtmann A, Sanders D, Maathuis FJ. 2006. Arabidopsis thaliana cyclic nucleotide gated channel 3 forms a non-selective ion transporter involved in germination and cation transport. J. Exp. Bot. 57:791–800
    [Google Scholar]
  43. 43.
    Gout L, Fudal I, Kuhn ML, Blaise F, Eckert M et al. 2006. Lost in the middle of nowhere: the AvrLm1 avirulence gene of the dothideomycete Leptosphaeria maculans. Mol. Microbiol. 60:67–80
    [Google Scholar]
  44. 44.
    Grandaubert J, Lowe RG, Soyer JL, Schoch CL, Van de Wouw AP et al. 2014. Transposable element-assisted evolution and adaptation to host plant within the Leptosphaeria maculans-Leptosphaeria biglobosa species complex of fungal pathogens. BMC Genom. 15:891
    [Google Scholar]
  45. 45.
    Haddadi P, Larkan NJ, Borhan MH. 2019. Dissecting R gene and host genetic background effect on the Brassica napus defense response to Leptosphaeria maculans. Sci. Rep. 9:6947
    [Google Scholar]
  46. 46.
    Haddadi P, Larkan NJ, Van de Wouw A, Zhang Y, Neik TX et al. 2022. Brassica napus genes Rlm4 and Rlm7, conferring resistance to Leptosphaeria maculans, are alleles of the Rlm9 wall-associated kinase-like resistance locus. Plant Biotech. J. https://doi.org/10.1111/pbi.13818
    [Crossref] [Google Scholar]
  47. 47.
    Haddadi P, Ma L, Wang H, Borhan MH. 2016. Genome-wide transcriptomic analyses provide insights into the lifestyle transition and effector repertoire of Leptosphaeria maculans during the colonization of Brassica napus seedlings. Mol. Plant Pathol. 17:1196–210
    [Google Scholar]
  48. 48.
    Hammond KE, Lewis BG, Musa TM. 1985. A systemic pathway in the infection of oilseed rape plants by Leptosphaeria maculans. 344557–65
  49. 49.
    Han X, Kahmann R. 2019. Manipulation of phytohormone pathways by effectors of filamentous plant pathogens. Front. Plant Sci. 10:822
    [Google Scholar]
  50. 50.
    Hane JK, Paxman J, Jones DAB, Oliver RP, de Wit P. 2020.. “ CATAStrophy,” a genome-informed trophic classification of filamentous plant pathogens—how many different types of filamentous plant pathogens are there?. Front. Microbiol. 10:3088
    [Google Scholar]
  51. 51.
    He Z, Ji R, Havlickova L, Wang L, Li Y et al. 2021. Genome structural evolution in Brassica crops. Nat. Plants 7:757–65
    [Google Scholar]
  52. 52.
    Higgins EE, Howell EC, Armstrong SJ, Parkin IAP 2021. A major quantitative trait locus on chromosome A9, BnaPh1, controls homoeologous recombination in Brassica napus. New Phytol. 229:3281–93
    [Google Scholar]
  53. 53.
    Hill WG. 2010. Understanding and using quantitative genetic variation. Philos. Trans. R. Soc. B 365:73–85
    [Google Scholar]
  54. 54.
    Huang YJ, Evans N, Li ZQ, Eckert M, Chevre AM et al. 2006. Temperature and leaf wetness duration affect phenotypic expression of Rlm6-mediated resistance to Leptosphaeria maculans in Brassica napus. New Phytol. 170:129–41
    [Google Scholar]
  55. 55.
    Huang YJ, Paillard S, Kumar V, King GJ, Fitt BDL, Delourme R. 2019. Oilseed rape (Brassica napus) resistance to growth of Leptosphaeria maculans in leaves of young plants contributes to quantitative resistance in stems of adult plants. PLOS ONE 14:e0222540
    [Google Scholar]
  56. 56.
    Huang YJ, Pirie EJ, Evans N, Delourme R, King GJ, Fitt BDL. 2009. Quantitative resistance to symptomless growth of Leptosphaeria maculans (phoma stem canker) in Brassica napus (oilseed rape). Plant Pathol 58:314–23
    [Google Scholar]
  57. 57.
    Hubbard M, Zhai C, Peng G. 2020. Exploring mechanisms of quantitative resistance to Leptosphaeria maculans (Blackleg) in the cotyledons of canola (Brassica napus) based on transcriptomic and microscopic analyses. Plants 9:7864
    [Google Scholar]
  58. 58.
    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
    [Google Scholar]
  59. 59.
    Jagodzik P, Tajdel-Zielinska M, Ciesla A, Marczak M, Ludwikow A. 2018. Mitogen-activated protein kinase cascades in plant hormone signaling. Front. Plant Sci. 9:1387
    [Google Scholar]
  60. 60.
    Jarratt-Barnham E, Wang L, Ning Y, Davies JM. 2021. The complex story of plant cyclic nucleotide-gated channels. Int. J. Mol. Sci. 22:874
    [Google Scholar]
  61. 61.
    Jiquel A, Gervais J, Geistodt-Kiener A, Delourme R, Gay EJ et al. 2021. A gene-for-gene interaction involving a ‘late’ effector contributes to quantitative resistance to the stem canker disease in Brassica napus. New Phytol. 231:1510–24
    [Google Scholar]
  62. 62.
    Johal GS, Briggs SP. 1992. Reductase activity encoded by the HM1 disease resistance gene in maize. Science 258:5084985–87
    [Google Scholar]
  63. 63.
    Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:323–29
    [Google Scholar]
  64. 64.
    Jumper J, Evans R, Pritzel A, Green T, Figurnov M et al. 2021. Highly accurate protein structure prediction with AlphaFold. Nature 596:583–89
    [Google Scholar]
  65. 65.
    Kanneganti V, Gupta AK. 2008. Wall associated kinases from plants: an overview. Physiol. Mol. Biol. Plants 14:109–18
    [Google Scholar]
  66. 66.
    Khan M, Subramaniam R, Desveaux D. 2016. Of guards, decoys, baits and traps: pathogen perception in plants by type III effector sensors. Curr. Opin. Microbiol. 29:49–55
    [Google Scholar]
  67. 67.
    Kim PD, Sasek V, Burketova L, Copikova J, Synytsya A et al. 2013. Cell wall components of Leptosphaeria maculans enhance resistance of Brassica napus. J. Agric. Food Chem. 61:5207–14
    [Google Scholar]
  68. 68.
    Kohorn BD. 2016. Cell wall-associated kinases and pectin perception. J. Exp. Bot. 67:489–94
    [Google Scholar]
  69. 69.
    Kourelis J, van der Hoorn RAL. 2018. Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. Plant Cell 30:285–99
    [Google Scholar]
  70. 70.
    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
    [Google Scholar]
  71. 71.
    Kumar V, Paillard S, Fopa-Fomeju B, Falentin C, Deniot G et al. 2018. Multi-year linkage and association mapping confirm the high number of genomic regions involved in oilseed rape quantitative resistance to blackleg. Theor. Appl. Genet. 131:1627–43
    [Google Scholar]
  72. 72.
    Larkan NJ, Lydiate DJ, Parkin IAP, Nelson MN, Epp DJ et al. 2013. The Brassica napus blackleg resistance gene LepR3 encodes a receptor-like protein triggered by the Leptosphaeria maculans effector AVRLM1. New Phytol. 197:595–605
    [Google Scholar]
  73. 73.
    Larkan NJ, Lydiate DJ, Yu F, Rimmer SR, Borhan MH. 2014. Co-localisation of the blackleg resistance genes Rlm2 and LepR3 on Brassica napus chromosome A10. BMC Plant Biol. 14:387
    [Google Scholar]
  74. 74.
    Larkan NJ, Ma L, Borhan MH. 2015. The Brassica napus receptor-like protein RLM2 is encoded by a second allele of the LepR3/Rlm2 blackleg resistance locus. Plant Biotechnol. J. 13:983–92
    [Google Scholar]
  75. 75.
    Larkan NJ, Ma L, Haddadi P, Buchwaldt M, Parkin IAP et al. 2020. The Brassica napus wall-associated kinase-like (WAKL) gene Rlm9 provides race-specific blackleg resistance. Plant J. 104:892–900
    [Google Scholar]
  76. 76.
    Larkan NJ, Parkin IAP, Borhan MH. 2019. Genetic mapping and characterisation of the novel blackleg resistance genes LepR5 and LepR6 Paper presented at the 15th International Rapeseed Congress Berlin: June 19
    [Google Scholar]
  77. 77.
    Larkan NJ, Raman H, Lydiate DJ, Robinson SJ, Yu F et al. 2016. Multi-environment QTL studies suggest a role for cysteine-rich protein kinase genes in quantitative resistance to blackleg disease in Brassica napus. BMC Plant Biol. 16:183
    [Google Scholar]
  78. 78.
    Larkan NJ, Yu F, Lydiate DJ, Rimmer SR, Borhan MH. 2016. Single R gene introgression lines for accurate dissection of the Brassica–Leptosphaeria pathosystem. Front. Plant Sci. 7:1771
    [Google Scholar]
  79. 79.
    Lazar N, Mesarich CH, Petit-Houdenot Y, Talbi N, de la Sierra-Gallay IL et al. 2020. A new family of structurally conserved fungal effectors displays epistatic interactions with plant resistance proteins. bioRxiv 423041. https://doi.org/10.1101/2020.12.17.423041
    [Crossref]
  80. 80.
    Leontovycova H, Trda L, Dobrev PI, Sasek V, Gay E et al. 2020. Auxin biosynthesis in the phytopathogenic fungus Leptosphaeria maculans is associated with enhanced transcription of indole-3-pyruvate decarboxylase LmIPDC2 and tryptophan aminotransferase LmTAM1. Res. Microbiol. 171:174–84
    [Google Scholar]
  81. 81.
    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]
  82. 82.
    Liebrand TWH, van den Burg HA, Joosten MHAJ. 2014. Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends Plant Sci 19:123–32
    [Google Scholar]
  83. 83.
    Liu X, Salokas K, Weldatsadik RG, Gawriyski L, Varjosalo M. 2020. Combined proximity labeling and affinity purification-mass spectrometry workflow for mapping and visualizing protein interaction networks. Nat. Protoc. 15:3182–211
    [Google Scholar]
  84. 84.
    Long Y, Wang Z, Sun Z, Fernando DW, McVetty PB, Li G. 2011. Identification of two blackleg resistance genes and fine mapping of one of these two genes in a Brassica napus canola cultivar ‘Surpass 400. ’. Theor. Appl. Genet. 122:1223–31
    [Google Scholar]
  85. 85.
    Lorrai R, Ferrari S. 2021. Host cell wall damage during pathogen infection: mechanisms of perception and role in plant-pathogen interactions. Plants 10:2399
    [Google Scholar]
  86. 86.
    Lowe RG, Cassin A, Grandaubert J, Clark BL, Van de Wouw AP et al. 2014. Genomes and transcriptomes of partners in plant-fungal-interactions between canola (Brassica napus) and two Leptosphaeria species. PLOS ONE 9:e103098
    [Google Scholar]
  87. 87.
    Ludwig AA, Saitoh H, Felix G, Freymark G, Miersch O et al. 2005. Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. PNAS 102:10736–41
    [Google Scholar]
  88. 88.
    Ma L, Djavaheri M, Wang H, Larkan NJ, Haddadi P et al. 2018. Leptosphaeria maculans effector protein AvrLm1 modulates plant immunity by enhancing MAP kinase 9 phosphorylation. iScience 3:177–91
    [Google Scholar]
  89. 89.
    Marcroft SJ, Elliott VL, Cozijnsen AJ, Salisbury PA, Howlett BJ, Van de Wouw AP. 2012. Identifying resistance genes to Leptosphaeria maculans in Australian Brassica napus cultivars based on reactions to isolates with known avirulence genotypes. Crop Pasture Sci 63:338–50
    [Google Scholar]
  90. 90.
    Mayerhofer R, Good AG, Bansal VK, Thiagarajah MR, Stringam GR. 1997. Molecular mapping of resistance to Leptosphaeria maculans in Australian cultivars of Brassica napus. Genome 40:294–301
    [Google Scholar]
  91. 91.
    Mayerhofer R, Wilde K, Mayerhofer M, Lydiate D, Bansal VK et al. 2005. Complexities of chromosome landing in a highly duplicated genome: toward map-based cloning of a gene controlling blackleg resistance in Brassica napus. Genetics 171:1977–88
    [Google Scholar]
  92. 92.
    McDonald MC, McDonald BA, Solomon PS. 2015. Recent advances in the Zymoseptoria tritici–wheat interaction: insights from pathogenomics. Front. Plant Sci. 6:102
    [Google Scholar]
  93. 93.
    Neik TX, Ghanbarnia K, Ollivier B, Scheben A, Severn-Ellis A et al. 2022. Two independent approaches converge to the cloning of a new Leptosphaeria maculans avirulence effector gene, AvrLmS-Lep2. Mol. Plant Pathol. 23:573348
    [Google Scholar]
  94. 94.
    Nie J, Zhou W, Liu J, Tan N, Zhou JM, Huang L. 2021. A receptor-like protein from Nicotiana benthamiana mediates VmE02 PAMP-triggered immunity. New Phytol. 229:2260–72
    [Google Scholar]
  95. 95.
    Novakova M, Sasek V, Trda L, Krutinova H, Mongin T et al. 2016. Leptosphaeria maculans effector AvrLm4-7 affects salicylic acid (SA) and ethylene (ET) signalling and hydrogen peroxide (H2O2) accumulation in Brassica napus. Mol. Plant Pathol. 17:818–31
    [Google Scholar]
  96. 96.
    Okuyama Y, Kanzaki H, Abe A, Yoshida K, Tamiru M et al. 2011. A multifaceted genomics approach allows the isolation of the rice Pia-blast resistance gene consisting of two adjacent NBS-LRR protein genes. Plant J. 66:467–79
    [Google Scholar]
  97. 97.
    Pang EC, Halloran GM. 1996. The genetics of adult-plant blackleg (Leptosphaeria maculans) resistance from Brassica juncea in B. napus. Theor. Appl. Genet. 92:382–87
    [Google Scholar]
  98. 98.
    Park J, Kim T-H, Takahashi Y, Schwab R, Dressano K et al. 2019. Chemical genetic identification of a lectin receptor kinase that transduces immune responses and interferes with abscisic acid signaling. Plant J. Cell Mol. Biol. 98:492–510
    [Google Scholar]
  99. 99.
    Parlange F, Daverdin G, Fudal I, Kuhn ML, Balesdent MH et al. 2009. Leptosphaeria maculans avirulence gene AvrLm4-7 confers a dual recognition specificity by the Rlm4 and Rlm7 resistance genes of oilseed rape, and circumvents Rlm4-mediated recognition through a single amino acid change. Mol. Microbiol. 71:851–63
    [Google Scholar]
  100. 100.
    Paterson AH, Lander ES, Hewitt JD, Peterson S, Lincoln SE, Tanksley SD. 1988. Resolution of quantitative traits into Mendelian factors by using a complete linkage map of restriction fragment length polymorphisms. Nature 335:721–26
    [Google Scholar]
  101. 101.
    Petit-Houdenot Y, Degrave A, Meyer M, Blaise F, Ollivier B et al. 2019. A two genes-for-one gene interaction between Leptosphaeria maculans and Brassica napus. New Phytol. 223:397–411
    [Google Scholar]
  102. 102.
    Piasecka A, Jedrzejczak-Rey N, Bednarek P. 2015. Secondary metabolites in plant innate immunity: conserved function of divergent chemicals. New Phytol. 206:948–64
    [Google Scholar]
  103. 103.
    Plissonneau C, Daverdin G, Ollivier B, Blaise F, Degrave A et al. 2016. A game of hide and seek between avirulence genes AvrLm4-7 and AvrLm3 in Leptosphaeria maculans. New Phytol. 209:1613–24
    [Google Scholar]
  104. 104.
    Plissonneau C, Rouxel T, Chevre AM, Van de Wouw AP, Balesdent MH. 2018. One gene–one name: the AvrLmJ1 avirulence gene of Leptosphaeria maculans is AvrLm5. Mol. Plant Pathol. 19:1012–16
    [Google Scholar]
  105. 105.
    Raman H, Raman R, Coombes N, Song J, Diffey S et al. 2016. Genome-wide association study identifies new loci for resistance to Leptosphaeria maculans in canola. Front. Plant Sci. 7:1513
    [Google Scholar]
  106. 106.
    Raman H, Raman R, Diffey S, Qiu Y, McVittie B et al. 2018. Stable quantitative resistance loci to blackleg disease in canola (Brassica napus L.) over continents. Front. Plant Sci. 9:1622
    [Google Scholar]
  107. 107.
    Raman H, Raman R, Kilian A, Detering F, Long Y et al. 2013. A consensus map of rapeseed (Brassica napus L.) based on diversity array technology markers: applications in genetic dissection of qualitative and quantitative traits. BMC Genom. 14:277
    [Google Scholar]
  108. 108.
    Raman H, Raman R, Qiu Y, Zhang Y, Batley J, Liu S. 2021. The Rlm13 gene, a new player of Brassica napus–Leptosphaeria maculans interaction maps on chromosome C03 in canola. Front. Plant Sci. 12:654604
    [Google Scholar]
  109. 109.
    Raman R, Diffey S, Barbulescu DM, Coombes N, Luckett D et al. 2020. Genetic and physical mapping of loci for resistance to blackleg disease in canola (Brassica napus L.). Sci. Rep. 10:4416
    [Google Scholar]
  110. 110.
    Raman R, Taylor B, Marcroft S, Stiller J, Eckermann P et al. 2012. Molecular mapping of qualitative and quantitative loci for resistance to Leptosphaeria maculans causing blackleg disease in canola (Brassica napus L.). Theor. Appl. Genet. 125:405–18
    [Google Scholar]
  111. 111.
    Rayapuram C, Jensen MK, Maiser F, Shanir JV, Hornshoj H et al. 2012. Regulation of basal resistance by a powdery mildew-induced cysteine-rich receptor-like protein kinase in barley. Mol. Plant Pathol. 13:135–47
    [Google Scholar]
  112. 112.
    Rimmer SR. 2006. Resistance genes to Leptosphaeria maculans in Brassica napus. Can. J. Plant Pathol. 28:S288–S97
    [Google Scholar]
  113. 113.
    Rimmer RS, Borhan MH, Zhu B, Somers D. 1999. Mapping resistance genes in Brassica napus to Leptosphaeria maculans. Proceedings of the 10th International Rapeseed Congress Paris: GCIRC
    [Google Scholar]
  114. 114.
    Rimmer SR, van den Berg CGJ. 1992. Resistance of oilseed Brassica spp. to blackleg caused by Leptosphaeria maculans. Can. J. Plant Pathol. 14:56–66
    [Google Scholar]
  115. 115.
    Rocafort M, Fudal I, Mesarich CH. 2020. Apoplastic effector proteins of plant-associated fungi and oomycetes. Curr. Opin. Plant Biol. 56:9–19
    [Google Scholar]
  116. 116.
    Romeis T, Ludwig AA, Martin R, Jones JD. 2001. Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J. 20:5556–67
    [Google Scholar]
  117. 117.
    Romeis T, Piedras P, Jones JD. 2000. Resistance gene-dependent activation of a calcium-dependent protein kinase in the plant defense response. Plant Cell 12:803–16
    [Google Scholar]
  118. 118.
    Rouxel T, Grandaubert J, Hane JK, Hoede C, Van de Wouw AP et al. 2011. Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat-induced point mutations. Nat. Commun. 2:202
    [Google Scholar]
  119. 119.
    Saintenac C, Lee WS, Cambon F, Rudd JJ, King RC et al. 2018. Wheat receptor-kinase-like protein Stb6 controls gene-for-gene resistance to fungal pathogen Zymoseptoria tritici. Nat. Genet. 50:368–74
    [Google Scholar]
  120. 120.
    Sasek V, Novakova M, Jindrichova B, Boka K, Valentova O, Burketova L. 2012. Recognition of avirulence gene AvrLm1 from hemibiotrophic ascomycete Leptosphaeria maculans triggers salicylic acid and ethylene signaling in Brassica napus. Mol. Plant-Microbe Interact. 25:1238–50
    [Google Scholar]
  121. 121.
    Schnippenkoetter W, Hoque M, Maher R, Van de Wouw A, Hands P et al. 2021. Comparison of non-subjective relative fungal biomass measurements to quantify the Leptosphaeria maculans–Brassica napus interaction. Plant Methods 17:122
    [Google Scholar]
  122. 122.
    Schön M, Töller A, Diezel C, Roth C, Westphal L et al. 2013. Analyses of wrky18 wrky40 plants reveal critical roles of SA/EDS1 signaling and indole-glucosinolate biosynthesis for Golovinomyces orontii resistance and a loss-of resistance towards Pseudomonas syringae pv. tomato AvrRPS4. Mol. Plant-Microbe Interact. 26:7758–67
    [Google Scholar]
  123. 123.
    Schulz P, Herde M, Romeis T. 2013. Calcium-dependent protein kinases: hubs in plant stress signaling and development. Plant Physiol. 163:523–30
    [Google Scholar]
  124. 124.
    Shinya T, Nakagawa T, Kaku H, Shibuya N. 2015. Chitin-mediated plant-fungal interactions: catching, hiding and handshaking. Curr. Opin. Plant Biol. 26:64–71
    [Google Scholar]
  125. 125.
    Sonah H, Zhang X, Deshmukh RK, Borhan MH, Fernando WG, Belanger RR. 2016. Comparative transcriptomic analysis of virulence factors in Leptosphaeria maculans during compatible and incompatible interactions with canola. Front. Plant Sci. 7:1784
    [Google Scholar]
  126. 126.
    Song J-M, Guan Z, Hu J, Guo C, Yang Z et al. 2020. Eight high-quality genomes reveal pan-genome architecture and ecotype differentiation of Brassica napus. Nat. Plants 6:34–45
    [Google Scholar]
  127. 127.
    Sprague SJ, Balesdent M-H, Brun H, Hayden HL, Marcroft SJ et al. 2006. Major gene resistance in Brassica napus (oilseed rape) is overcome by changes in virulence of populations of Leptosphaeria maculans in France and Australia. Eur. J. Plant Pathol. 114:33–40
    [Google Scholar]
  128. 128.
    Stotz HU, Mitrousia GK, de Wit PJGM, Fitt BDL. 2014. Effector-triggered defence against apoplastic fungal pathogens. Trends Plant Sci 19:491–500
    [Google Scholar]
  129. 129.
    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]
  130. 130.
    Tsuda K, Somssich IE. 2015. Transcriptional networks in plant immunity. New Phytol. 206:932–47
    [Google Scholar]
  131. 131.
    Urquhart AS, Idnurm A. 2019. Limitations of transcriptome-based prediction of pathogenicity genes in the plant pathogen Leptosphaeria maculans. FEMS Microbiol. Lett. 366:7fnz080
    [Google Scholar]
  132. 132.
    Vaattovaara A, Brandt B, Rajaraman S, Safronov O, Veidenberg A et al. 2019. Mechanistic insights into the evolution of DUF26-containing proteins in land plants. Commun. Biol. 2:56
    [Google Scholar]
  133. 133.
    Van de Wouw AP, Howlett BJ. 2012. Estimating frequencies of virulent isolates in field populations of a plant pathogenic fungus, Leptosphaeria maculans, using high-throughput pyrosequencing. J. Appl. Microbiol. 113:1145–53
    [Google Scholar]
  134. 134.
    Van de Wouw AP, Howlett BJ. 2020. Advances in understanding the Leptosphaeria maculans–Brassica pathosystem and their impact on disease management. Can. J. Plant Pathol. 42:149–63
    [Google Scholar]
  135. 135.
    Van de Wouw AP, Marcroft SJ, Barbetti MJ, Hua L, Salisbury PA et al. 2009. Dual control of avirulence in Leptosphaeria maculans towards a Brassica napus cultivar with ‘sylvestris-derived’ resistance suggests involvement of two resistance genes. Plant Pathol. 58:305–13
    [Google Scholar]
  136. 136.
    van der Burgh AM, Joosten MHAJ. 2019. Plant immunity: thinking outside and inside the box. Trends Plant Sci 24:587–601
    [Google Scholar]
  137. 137.
    van der Burgh AM, Postma J, Robatzek S, Joosten MHAJ. 2019. Kinase activity of SOBIR1 and BAK1 is required for immune signalling. Mol. Plant Pathol. 20:410–22
    [Google Scholar]
  138. 138.
    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
    [Google Scholar]
  139. 139.
    Velasquez AC, Castroverde CDM, He SY. 2018. Plant-pathogen warfare under changing climate conditions. Curr. Biol. 28:R619–R34
    [Google Scholar]
  140. 140.
    Wan WL, Frohlich K, Pruitt RN, Nurnberger T, Zhang L. 2019. Plant cell surface immune receptor complex signaling. Curr. Opin. Plant Biol. 50:18–28
    [Google Scholar]
  141. 141.
    Wang H, Sun S, Ge W, Zhao L, Hou B et al. 2020. Horizontal gene transfer of Fhb7 from fungus underlies Fusarium head blight resistance in wheat. Science 368:6493eaba5435
    [Google Scholar]
  142. 142.
    Wang S, Boevink PC, Welsh L, Zhang R, Whisson SC, Birch PRJ. 2017. Delivery of cytoplasmic and apoplastic effectors from Phytophthora infestans haustoria by distinct secretion pathways. New Phytol. 216:205–15
    [Google Scholar]
  143. 143.
    Williams PH. 1985. The crucifer genetics cooperative. Plant Mol. Biol. Rep. 3:129–44
    [Google Scholar]
  144. 144.
    Yang K, Rong W, Qi L, Li J, Wei X, Zhang Z. 2013. Isolation and characterization of a novel wheat cysteine-rich receptor-like kinase gene induced by Rhizoctonia cerealis. Sci. Rep. 3:3021
    [Google Scholar]
  145. 145.
    Yoshioka K, Moeder W, Kang HG, Kachroo P, Masmoudi K et al. 2006. The chimeric Arabidopsis CYCLIC NUCLEOTIDE-GATED ION CHANNEL11/12 activates multiple pathogen resistance responses. Plant Cell 18:747–63
    [Google Scholar]
  146. 146.
    Yu F, Gugel RK, Kutcher HR, Peng G, Rimmer SR. 2013. Identification and mapping of a novel blackleg resistance locus LepR4 in the progenies from Brassica napus × B. rapa subsp. sylvestris. Theor. Appl. Genet. 126:307–15
    [Google Scholar]
  147. 147.
    Yu F, Lydiate DJ, Gugel RK, Sharpe AG, Rimmer SR. 2012. Introgression of Brassica rapa subsp. sylvestris blackleg resistance into B. napus. Mol. Breed. 30:1495–506
    [Google Scholar]
  148. 148.
    Yu F, Lydiate DJ, Rimmer SR. 2005. Identification of two novel genes for blackleg resistance in Brassica napus. Theor. Appl. Genet. 110:969–79
    [Google Scholar]
  149. 149.
    Yu X, Xu G, Li B, de Souza Vespoli L, Liu H et al. 2019. The receptor kinases BAK1/SERK4 regulate Ca2+ channel-mediated cellular homeostasis for cell death containment. Curr. Biol. 29:3778–90.e8
    [Google Scholar]
  150. 150.
    Zhan S, Griswold C, Lukens L. 2021. Zea mays RNA-seq estimated transcript abundances are strongly affected by read mapping bias. BMC Genom 22:285
    [Google Scholar]
  151. 151.
    Zhao C, Tang Y, Wang J, Zeng Y, Sun H et al. 2021. A mis-regulated cyclic nucleotide-gated channel mediates cytosolic calcium elevation and activates immunity in Arabidopsis. New Phytol. 230:1078–94
    [Google Scholar]
  152. 152.
    Zheng X, Koopmann B, Ulber B, von Tiedemann A. 2020. A global survey on diseases and pests in oilseed rape—current challenges and innovative strategies of control. Front. Agron. 2:15
    [Google Scholar]
  153. 153.
    Zuo W, Chao Q, Zhang N, Ye J, Tan G et al. 2015. A maize wall-associated kinase confers quantitative resistance to head smut. Nat. Genet. 47:151–57
    [Google Scholar]
/content/journals/10.1146/annurev-phyto-021621-120602
Loading
/content/journals/10.1146/annurev-phyto-021621-120602
Loading

Data & Media loading...

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