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PreprintCited by 139Plant Disease Resistance and GeneticsPlant Pathogens and Fungal DiseasesFungal and yeast genetics research

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The transcriptional landscape of plant infection by the rice blast fungus Magnaporthe oryzae reveals distinct families of temporally co-regulated and structurally conserved effectors

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Yan, Xia, Tang, Bozeng, Ryder, Lauren S., MacLean, Dan, Were, Vincent M., Eseola, Alice Bisola, Cruz-Mireles, Neftaly, Foster, Andrew J., Osés-Ruiz, Miriam, Talbot, Nicholas J.·2022·The Plant Cell
DOI 10.1101/2022.07.18.500532PMC PMC10118281

Preprint — published as 10.1093/plcell/koad036

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Abstract

The rice blast fungus Magnaporthe oryzae causes a devastating disease which threatens global rice production. In spite of intense study, the biology of plant tissue invasion during blast disease remains poorly understood. Here we report a high resolution, transcriptional profiling study of the entire plant-associated development of the blast fungus. Our analysis revealed major temporal changes in fungal gene expression during plant infection. Pathogen gene expression could be classified into 10 modules of temporally co-expressed genes, providing evidence of induction of pronounced shifts in primary and secondary metabolism, cell signalling and transcriptional regulation. A set of 863 genes encoding secreted proteins are differentially expressed at specific stages of infection, and 546 were predicted to be effectors and named MEP ( M agnaporthe e ffector p rotein) genes. Computational prediction of structurally-related MEPs , including the MAX effector family, revealed their temporal co-regulation in the same co-expression modules. We functionally characterised 32 MEP genes and demonstrate that Mep effectors are predominantly targeted to the cytoplasm of rice cells via the biotrophic interfacial complex (BIC), and use a common unconventional secretory pathway. Taken together, our study reveals major changes in gene expression associated with blast disease and identifies a diverse repertoire of effectors critical to successful infection.

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Research works printed but not linked: 109

  1. 10.1186/1471-2105-15-293 · DOI
  2. 2021, The transcriptional landscape of Arabidopsis thaliana pattern-triggered immunity, Nature Plants, 7, 579, 10.1038/s41477-021-00874-5 · DOI
  3. 10.1105/tpc.104.022715 · DOI
  4. 10.1038/nbt.3519 · DOI · Paper page
  5. 10.1111/nph.13948 · DOI
  6. 10.1105/tpc.112.107201 · DOI
  7. 10.1007/s00438-002-0691-4 · DOI
  8. 2012, Identification and Characterization of In planta–Expressed Secreted Effector Proteins from Magnaporthe oryzae That Induce Cell Death in Rice, Mol Plant Microbe Interact, 26, 191
  9. 2017, The transcriptional landscape of Rhizoctonia solani AG1-IA during infection of soybean as defined by RNA-seq, PLoS One, 12, e0184095, 10.1371/journal.pone.0184095 · DOI
  10. 2021, From appressorium to transpressorium-Defining the morphogenetic basis of host cell invasion by the rice blast fungus, PLoS Pathog, 17, e1009779, 10.1371/journal.ppat.1009779 · DOI
  11. 10.1126/science.1222934 · DOI
  12. 10.1371/journal.ppat.1005228 · DOI
  13. 2018, Polymorphic residues in rice NLRs expand binding and response to effectors of the blast pathogen, Nat Plants, 4, 576, 10.1038/s41477-018-0194-x · DOI
  14. 10.1038/nature03449 · DOI
  15. 2016, Identification and characterization of the peroxin 1 gene MoPEX1 required for infection-related morphogenesis and pathogenicity in Magnaporthe oryzae, Sci Rep, 6, 36292, 10.1038/srep36292 · DOI
  16. 10.1186/s12864-016-2684-4 · DOI
  17. 10.1371/journal.ppat.1004801 · DOI
  18. 2017, The Nep1-like protein family of Magnaporthe oryzae is dispensable for the infection of rice plants, Sci Rep, 7, 4372, 10.1038/s41598-017-04430-0 · DOI
  19. 10.1016/j.tim.2017.12.007 · DOI
  20. 2014, Mechanisms of nutrient acquisition and utilization during fungal infections of leaves, Annu Rev Phytopathol, 52, 155, 10.1146/annurev-phyto-102313-050135 · DOI
  21. 10.1371/journal.pgen.1002673 · DOI
  22. Franceschetti, M. , Maqbool, A. , Jimenez-Dalmaroni, M.J. , Pennington, H.G. , Kamoun, S. , and Banfield, M.J . (2017). Effectors of Filamentous Plant Pathogens: Commonalities amid Diversity. Microbiol Mol Biol Rev 81. · DOI
  23. 2017, Tpc1 is an important Zn(II)2Cys6 transcriptional regulator required for polarized growth and virulence in the rice blast fungus, PLoS Pathog, 13, e1006516, 10.1371/journal.ppat.1006516 · DOI
  24. 10.1038/ncomms2996 · DOI
  25. 10.1073/pnas.1810705115 · DOI
  26. 2019, Functional Identification of Novel Cell Death-inducing Effector Proteins from Magnaporthe oryzae, Rice (N Y, 12, 59, 10.1186/s12284-019-0312-z · DOI
  27. 10.1105/tpc.15.00552 · DOI
  28. 10.1038/s41586-020-2536-x · DOI
  29. 10.1126/science.aam9654 · DOI
  30. 10.1073/pnas.1807297116 · DOI
  31. 2016, Emergence of wheat blast in Bangladesh was caused by a South American lineage of Magnaporthe oryzae, BMC Biology, 14, 84, 10.1186/s12915-016-0309-7 · DOI
  32. Johnson, N.L. , Kotz, S. , and Kemp, A.W . (1992). Univariate Discrete Distributions. New York: Wiley Second Edition.
  33. 10.1038/nature05286 · DOI · Paper page
  34. 10.1146/annurev.phyto.44.070505.143436 · DOI
  35. 10.1105/tpc.106.046300 · DOI
  36. 10.1371/journal.pone.0049423 · DOI
  37. 10.1534/genetics.118.301490 · DOI
  38. 10.1105/tpc.109.069666 · DOI
  39. 10.1371/journal.pgen.1000757 · DOI
  40. 2020, Two nuclear effectors of the rice blast fungus modulate host immunity via transcriptional reprogramming, Nat Commun, 11, 5845, 10.1038/s41467-020-19624-w · DOI
  41. 10.1371/journal.ppat.1002643 · DOI
  42. 2021, Accurate plant pathogen effector protein classification ab initio with deepredeff: an ensemble of convolutional neural networks, BMC Bioinformatics, 22, 372, 10.1186/s12859-021-04293-3 · DOI
  43. 10.1111/j.1365-313X.2005.02386.x · DOI
  44. 10.1186/1471-2105-9-559 · DOI · Paper page
  45. 10.1105/tpc.17.00764 · DOI
  46. 10.1101/2022.06.06.494979 · DOI
  47. 2016, Harbouring public good mutants within a pathogen population can increase both fitness and virulence, eLife, 5, e18678, 10.7554/eLife.18678 · DOI
  48. 10.1094/MPMI.1997.10.9.1075 · DOI
  49. 10.1371/journal.ppat.1001261 · DOI
  50. Liu, X. , and Zhang, Z . (2021). A double-edged sword: reactive oxygen species (ROS) during the rice blast fungus and host interaction. FEBS J. · DOI
  51. 10.1111/1462-2920.12903 · DOI
  52. 10.1146/annurev-arplant-043014-114623 · DOI
  53. Maqbool, A. , Saitoh, H. , Franceschetti, M. , Stevenson, C.E. , Uemura, A. , Kanzaki, H. , Kamoun, S. , Terauchi, R. , and Banfield, M.J . (2015). Structural basis of pathogen recognition by an integrated HMA domain in a plant NLR immune receptor. Elife 4. · DOI
  54. 2017, The Magnaporthe oryzae nitrooxidative stress response suppresses rice innate immunity during blast disease, Nat Microbiol, 2, 17054, 10.1038/nmicrobiol.2017.54 · DOI
  55. 10.1105/tpc.111.092957 · DOI
  56. 10.1105/tpc.7.11.1869 · DOI
  57. 10.1007/s00299-016-1943-9 · DOI
  58. 10.1016/j.mib.2007.04.005 · DOI
  59. 10.1105/tpc.107.055228 · DOI
  60. 2016, Magnaporthe oryzae Glycine-Rich Secretion Protein, Rbf1 Critically Participates in Pathogenicity through the Focal Formation of the Biotrophic Interfacial Complex, PLoS Pathog, 12, e1005921, 10.1371/journal.ppat.1005921 · DOI
  61. 10.1093/nar/25.2.451 · DOI
  62. 2021, Appressorium-mediated plant infection by Magnaporthe oryzae is regulated by a Pmk1-dependent hierarchical transcriptional network, Nat Microbiol, 6, 1383, 10.1038/s41564-021-00978-w · DOI
  63. 10.1105/tpc.112.105429 · DOI
  64. 10.1094/MPMI.2002.15.3.183 · DOI
  65. 10.1105/tpc.105.038422 · DOI
  66. 2013, Global expression profiling of transcription factor genes provides new insights into pathogenicity and stress responses in the rice blast fungus, PLoS Pathog, 9, e1003350, 10.1371/journal.ppat.1003350 · DOI
  67. 10.1111/j.1365-313X.2009.03912.x · DOI
  68. 10.1038/nchembio.1885 · DOI
  69. 10.1038/nmeth.4324 · DOI · Paper page
  70. 2020, Widespread distribution of resistance to triazole fungicides in Brazilian populations of the wheat blast pathogen, Plant Pathology, 70, 436
  71. 2020, Leucine biosynthesis is required for infection-related morphogenesis and pathogenicity in the rice blast fungus Magnaporthe oryzae, Curr Genet, 66, 155, 10.1007/s00294-019-01009-2 · DOI
  72. 10.1086/519860 · DOI
  73. 10.1104/pp.114.255927 · DOI
  74. 10.1038/s41586-019-1637-x · DOI
  75. 10.1126/science.aaq0892 · DOI
  76. Sangappillai, V. , and Nadarajah, K . (2020). Fatty Acid Synthase Beta Dehydratase in the Lipid Biosynthesis Pathway Is Required for Conidiogenesis, Pigmentation and Appressorium Formation in Magnaporthe oryzae S6. Int J Mol Sci 21. · DOI
  77. 10.1105/tpc.109.072447 · DOI
  78. 10.3389/fmicb.2016.00600 · DOI
  79. 2021, Computational Structural Genomics Unravels Common Folds and Novel Families in the Secretome of Fungal Phytopathogen Magnaporthe oryzae, Mol Plant Microbe Interact, 34, 1267, 10.1094/MPMI-03-21-0071-R · DOI
  80. 2017, Identification and characterization of suppressors of plant cell death (SPD) effectors from Magnaporthe oryzae, Mol Plant Pathol, 18, 850, 10.1111/mpp.12449 · DOI
  81. 10.1111/mpp.12869 · DOI
  82. 10.1371/journal.ppat.1002514 · DOI
  83. 2022, EffectorP 3.0: Prediction of Apoplastic and Cytoplasmic Effectors in Fungi and Oomycetes, Mol Plant Microbe Interact, 35, 146, 10.1094/MPMI-08-21-0201-R · DOI
  84. 2018, When resistance gene pyramids are not durable-the role of pathogen diversity, Mol Plant Pathol, 19, 521, 10.1111/mpp.12636 · DOI
  85. 10.1371/journal.pgen.1007814 · DOI
  86. 10.1094/MPMI.1998.11.5.404 · DOI
  87. 10.1105/tpc.5.11.1575 · DOI
  88. 10.1128/aem.59.2.585-593.1993 · DOI
  89. 10.1007/s00253-018-9456-9 · DOI
  90. 1993, Host Range, Mating Type, and Fertility of Pyricularia grisea from Wheat in Brazil, Plant Disease, 77, 1211, 10.1094/PD-77-1211 · DOI
  91. 10.1093/genetics/127.1.87 · DOI
  92. 10.1126/science.aam9517 · DOI
  93. 2017, RNA-seq analysis provides insight into reprogramming of culm development in Zizania latifolia induced by Ustilago esculenta, Plant Mol Biol, 95, 533, 10.1007/s11103-017-0658-9 · DOI
  94. 10.1073/pnas.1006839107 · DOI
  95. 2019, Transcriptomic Hallmarks of Tumor Plasticity and Stromal Interactions in Brain Metastasis, Cell Rep, 27, 1277, 10.1016/j.celrep.2019.03.085 · DOI
  96. 10.1186/s13059-019-1891-0 · DOI
  97. 10.1073/pnas.95.21.12713 · DOI
  98. Yamaguchi, I . (2004). Overview on the Chemical Control of Rice Blast Disease. In Rice Blast: Interaction with Rice and Control, S. Kawasaki , ed (Dordrecht: Springer Netherlands), pp. 1-13. · DOI
  99. 10.1371/journal.ppat.1002385 · DOI
  100. 2013, The MET13 methylenetetrahydrofolate reductase gene is essential for infection-related morphogenesis in the rice blast fungus Magnaporthe oryzae, PLoS One, 8, e76914, 10.1371/journal.pone.0076914 · DOI
  101. 10.1094/MPMI-02-18-0052-R · DOI
  102. 10.1105/tpc.109.066324 · DOI
  103. 10.1089/omi.2011.0118 · DOI · Paper page
  104. 2016, ZNF1 Encodes a Putative C2H2 Zinc-Finger Protein Essential for Appressorium Differentiation by the Rice Blast Fungus Magnaporthe oryzae, Mol Plant Microbe Interact, 29, 22, 10.1094/MPMI-09-15-0201-R · DOI
  105. 2017, Transcriptome Analyses Shed New Insights into Primary Metabolism and Regulation of Blumeria graminis f. sp. tritici during Conidiation, Front Plant Sci, 8, 1146, 10.3389/fpls.2017.01146 · DOI
  106. 2022, NLRs guard metabolism to coordinate pattern- and effector-triggered immunity, Nature, 601, 245, 10.1038/s41586-021-04219-2 · DOI
  107. 10.1007/s00294-010-0319-x · DOI
  108. 10.1371/journal.ppat.1002450 · DOI
  109. 10.5598/imafungus.2016.07.01.09 · DOI

Metadata

Authors
Yan, X., Tang, B., Ryder, L. S., MacLean, D., Were, V. M., Eseola, A. B., Cruz-Mireles, N., Foster, A. J., Osés-Ruiz, M., & Talbot, N. J.
Affiliations
University of East Anglia (GB)
Corresponding author
Talbot, Nicholas J.
ORCID
Venue
The Plant Cell
Publisher
openRxiv
Published
2022-07-19
Volume
35
Issue
5
Pages
1360-1385
ISSN
1040-4651 (ISSN-L)
DOI
10.1101/2022.07.18.500532
PMC
PMC10118281
OpenAlex
W4321331851
Cited by
139
References
1
Citations by year
2026: 33 · 2025: 42 · 2024: 38 · 2023: 26
FWCI
24.58
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • The Plant Cell (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Academica-e (Universidad Pública de Navarra) (submittedVersion, cc-by)
  • UEA Digital Repository (University of East Anglia) (submittedVersion)
Funders
  • Gatsby Charitable Foundation
  • University of Exeter
  • European Commission (2007–2013, FP7 2007-2013, FP7/2007, 294702)
  • Directorate for Biological Sciences
  • Biotechnology and Biological Sciences Research Council (BB/Y002997/1, BB/V016342/1, BBS/E/J/000PR9797)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Disease Resistance and Genetics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Pathogens and Fungal Diseases
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Keywords
Magnaporthe oryzae, rice blast, effectors, secreted proteins, unconventional secretion, plant-pathogen interaction, fungal secondary metabolism, transcriptional regulation
MeSH terms
Ascomycota, Cytoplasm, Fungal Proteins, Plant Diseases, Oryza, Signal Transduction, Magnaporthe

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