1932

Abstract

Filamentous plant pathogens threaten global food security and ecosystem resilience. In recent decades, significant strides have been made in deciphering the molecular basis of plant–pathogen interactions, especially the interplay between pathogens’ molecular weaponry and hosts’ defense machinery. Stemming from interdisciplinary investigations into the infection cell biology of filamentous plant pathogens, recent breakthrough discoveries have provided a new impetus to the field. These advances include the biophysical characterization of a novel invasion mechanism (i.e., naifu invasion) and the unraveling of novel effector secretion routes. On the plant side, progress includes the identification of components of cellular networks involved in the uptake of intracellular effectors. This exciting body of research underscores the pivotal role of logistics management by the pathogen throughout the infection cycle, encompassing the precolonization stages up to tissue invasion. More insight into these logistics opens new avenues for developing environmentally friendly crop protection strategies in an era marked by an imperative to reduce the use of agrochemicals.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-032421-121423
2024-11-20
2025-04-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/78/1/annurev-micro-032421-121423.html?itemId=/content/journals/10.1146/annurev-micro-032421-121423&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Ahmad A, Saraswat D, El Gamal A. 2023.. A survey on using deep learning techniques for plant disease diagnosis and recommendations for development of appropriate tools. . Smart Agric. Technol. 3::100083
    [Crossref] [Google Scholar]
  2. 2.
    Ai G, Xia Q, Song T, Li T, Zhu H, et al. 2021.. A Phytophthora sojae CRN effector mediates phosphorylation and degradation of plant aquaporin proteins to suppress host immune signaling. . PLOS Pathog. 17:(3):e1009388
    [Crossref] [Google Scholar]
  3. 3.
    Avrova AO, Boevink PC, Young V, Grenville-Briggs LJ, van West P, et al. 2008.. A novel Phytophthora infestans haustorium–specific membrane protein is required for infection of potato. . Cell. Microbiol. 10:(11):227184
    [Crossref] [Google Scholar]
  4. 4.
    Backhouse D, Willetts HJ. 1987.. Development and structure of infection cushions of Botrytis cinerea. . Trans. Br. Mycol. Soc. 89:(1):8995
    [Crossref] [Google Scholar]
  5. 5.
    de Bary A. 1863.. Recherches sur le développement de quelques champignons parasites. III. Peronospora. . Ann. Sci. Nat. Bot. Ser. 20::3267
    [Google Scholar]
  6. 6.
    Bassani I, Larousse M, Tran QD, Attard A, Galiana E. 2020.. Phytophthora zoospores: from perception of environmental signals to inoculum formation on the host-root surface. . Comput. Struct. Biotechnol. J. 18::376673
    [Crossref] [Google Scholar]
  7. 7.
    Beakes GW, Glockling SL, Sekimoto S. 2012.. The evolutionary phylogeny of the oomycete “fungi. .” Protoplasma 249:(1):319
    [Crossref] [Google Scholar]
  8. 8.
    Bebber DP, Ramotowski MAT, Gurr SJ. 2013.. Crop pests and pathogens move polewards in a warming world. . Nat. Clim. Change 3:(11):98588
    [Crossref] [Google Scholar]
  9. 9.
    Bentham AR, De la Concepcion JC, Mukhi N, Zdrzałek R, Draeger M, et al. 2020.. A molecular roadmap to the plant immune system. . J. Biol. Chem. 295:(44):1491635
    [Crossref] [Google Scholar]
  10. 10.
    Berndt R, Oberwinkler F. 1997.. Haustorial ultrastructure and morphology of Melampsorella and Thekopsora areolata. . Mycologia 89:(5):698705
    [Crossref] [Google Scholar]
  11. 11.
    Bhattacharjee S, Hiller NL, Liolios K, Win J, Kanneganti T-D, et al. 2006.. The malarial host-targeting signal is conserved in the Irish potato famine pathogen. . PLOS Pathog. 2:(5):e50
    [Crossref] [Google Scholar]
  12. 12.
    Bircher U, Hohl HR. 1999.. A role for calcium in appressorium induction in Phytophthora palmivora. . Bot. Helv. 109:(1):5565
    [Google Scholar]
  13. 13.
    Blackwell EM. 1953.. Haustoria of Phytophthora infestans and some other species. . Trans. Br. Mycol. Soc. 36:(2):13858
    [Crossref] [Google Scholar]
  14. 14.
    Boddey JA, O'Neill MT, Lopaticki S, Carvalho TG, Hodder AN, et al. 2016.. Export of malaria proteins requires co-translational processing of the PEXEL motif independent of phosphatidylinositol-3-phosphate binding. . Nat. Commun. 7::10470
    [Crossref] [Google Scholar]
  15. 15.
    Boddy L. 2016.. Pathogens of autotrophs. . In The Fungi, ed. SC Watkinson, L Boddy, NP Money , pp. 24592. Boston:: Academic. , 3rd ed..
    [Google Scholar]
  16. 16.
    Bouwmeester K, Meijer HJG, Govers F. 2011.. At the frontier: RXLR effectors crossing the Phytophthora–host interface. . Front. Plant Sci. 2::75
    [Crossref] [Google Scholar]
  17. 17.
    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:(51):2083237
    [Crossref] [Google Scholar]
  18. 18.
    Bronkhorst J, Kasteel M, van Veen S, Clough JM, Kots K, et al. 2021.. A slicing mechanism facilitates host entry by plant-pathogenic Phytophthora. . Nat. Microbiol. 6:(8):10006
    [Crossref] [Google Scholar]
  19. 19.
    Bronkhorst J, Kots K, de Jong D, Kasteel M, van Boxmeer T, et al. 2022.. An actin mechanostat ensures hyphal tip sharpness in Phytophthora infestans to achieve host penetration. . Sci. Adv. 8:(23):eabo0875
    [Crossref] [Google Scholar]
  20. 20.
    Cantrill LC, Deverall BJ. 1993.. Isolation of haustoria from wheat leaves infected by the leaf rust fungus. . Physiol. Mol. Plant Pathol. 42:(5):33743
    [Crossref] [Google Scholar]
  21. 21.
    Chethana KWT, Jayawardena RS, Chen Y-J, Konta S, Tibpromma S, et al. 2021.. Diversity and function of appressoria. . Pathogens 10:(6):746
    [Crossref] [Google Scholar]
  22. 22.
    Cheung F, Win J, Lang JM, Hamilton J, Vuong H, et al. 2008.. Analysis of the Pythium ultimum transcriptome using Sanger and pyrosequencing approaches. . BMC Genom. 9::542
    [Crossref] [Google Scholar]
  23. 23.
    Chong J, Harder DE, Rohringer R. 1981.. Ontogeny of mono-and dikaryotic rust haustoria: cytochemical and ultrastructural studies. . Phytopathology 71:(9):97583
    [Crossref] [Google Scholar]
  24. 24.
    Choquer M, Rascle C, Gonçalves IR, de Vallée A, Ribot C, et al. 2021.. The infection cushion of Botrytis cinerea: a fungal “weapon” of plant-biomass destruction. . Environ. Microbiol. 23:(4):2293314
    [Crossref] [Google Scholar]
  25. 25.
    Coffey MD, Wilson UE. 1983.. An ultrastructural study of the late-blight fungus Phytophthora infestans and its interaction with the foliage of two potato cultivars possessing different levels of general (field) resistance. . Can. J. Bot. 61:(10):266985
    [Crossref] [Google Scholar]
  26. 26.
    Cohen C, Gauci FX, Noblin X, Galiana E, Attard A, Thomen P. 2023.. Kinetics of zoospores approaching a root using a microfluidic device. . bioRxiv 2023.06.21.545863. https://doi.org/10.1101/2023.06.21.545863
  27. 27.
    Cooper RM. 1983.. The mechanisms and significance of enzymic degradation of host cell walls by parasites. . In Biochemical Plant Pathology, ed. JA Callow , pp. 10137. New York:: Wiley
    [Google Scholar]
  28. 28.
    Corredor-Moreno P, Saunders DGO. 2020.. Expecting the unexpected: factors influencing the emergence of fungal and oomycete plant pathogens. . New Phytol. 225:(1):11825
    [Crossref] [Google Scholar]
  29. 29.
    Dagdas YF, Yoshino K, Dagdas G, Ryder LS, Bielska E, et al. 2012.. Septin-mediated plant cell invasion by the rice blast fungus, Magnaporthe oryzae. . Science 336:(6088):159095
    [Crossref] [Google Scholar]
  30. 30.
    Derevnina L, Dagdas YF, De la Concepcion JC, Bialas A, Kellner R, et al. 2016.. Nine things to know about elicitins. . New Phytol. 212:(4):88895
    [Crossref] [Google Scholar]
  31. 31.
    Dionysopoulou M, Yan N, Wang B, Pliotas C, Diallinas G. 2022.. Genetic and cellular characterization of MscS-like putative channels in the filamentous fungus Aspergillus nidulans. . Channels 16:(1):14858
    [Crossref] [Google Scholar]
  32. 32.
    Dou D, Kale SD, Wang X, Jiang RHY, Bruce NA, et al. 2008.. RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. . Plant Cell 20:(7):193047
    [Crossref] [Google Scholar]
  33. 33.
    Egea PF. 2020.. Crossing the vacuolar rubicon: structural insights into effector protein trafficking in apicomplexan parasites. . Microorganisms 8:(6):865
    [Crossref] [Google Scholar]
  34. 34.
    Emmett RW, Parbery DG. 1975.. Appressoria. . Annu. Rev. Phytopathol. 13::14765
    [Crossref] [Google Scholar]
  35. 35.
    Enkerli K, Mims CW, Hahn MG. 2011.. Ultrastructure of compatible and incompatible interactions of soybean roots infected with the plant pathogenic oomycete Phytophthora sojae. . Can. J. Bot. 75:(9):1493508
    [Crossref] [Google Scholar]
  36. 36.
    Eseola AB, Ryder LS, Osés-Ruiz M, Findlay K, Yan X, et al. 2021.. Investigating the cell and developmental biology of plant infection by the rice blast fungus Magnaporthe oryzae. . Fungal Genet. Biol. 154::103562
    [Crossref] [Google Scholar]
  37. 37.
    Evangelisti E, Guyon A, Shenhav L, Schornack S. 2023.. FIRE mimics a 14-3-3-binding motif to promote Phytophthora palmivora infection. . Mol. Plant. Microbe Interact. 36:(6):31522
    [Crossref] [Google Scholar]
  38. 38.
    Evangelisti E, Shenhav L, Yunusov T, Le Naour-Vernet M, Rink P, Schornack S. 2019.. Hydrodynamic shape changes underpin nuclear rerouting in branched hyphae of an oomycete pathogen. . mBio 10:(5):e01516-19
    [Crossref] [Google Scholar]
  39. 39.
    Evangelisti E, Turner C, McDowell A, Shenhav L, Yunusov T, et al. 2021.. Deep learning–based quantification of arbuscular mycorrhizal fungi in plant roots. . New Phytol. 232:(5):220719
    [Crossref] [Google Scholar]
  40. 40.
    Evangelisti E, Yunusov T, Shenhav L, Schornack S. 2019.. N-acetyltransferase AAC(3)-I confers gentamicin resistance to Phytophthora palmivora and Phytophthora infestans. . BMC Microbiol. 19::265
    [Crossref] [Google Scholar]
  41. 41.
    Fabro G. 2022.. Oomycete intracellular effectors: specialised weapons targeting strategic plant processes. . New Phytol. 233:(3):107482
    [Crossref] [Google Scholar]
  42. 42.
    Fang Y, Wang Z, Zhang S, Peng Q, Liu X. 2021.. Characterization and proteome analysis of the extracellular vesicles of Phytophthora capsici. . J. Proteom. 238::104137
    [Crossref] [Google Scholar]
  43. 43.
    Fawke S, Doumane M, Schornack S. 2015.. Oomycete interactions with plants: infection strategies and resistance principles. . Microbiol. Mol. Biol. Rev. 79:(3):26380
    [Crossref] [Google Scholar]
  44. 44.
    Fernandez J, Orth K. 2018.. Rise of a cereal killer: the biology of Magnaporthe oryzae biotrophic growth. . Trends Microbiol. 26:(7):58297
    [Crossref] [Google Scholar]
  45. 45.
    Figueroa M, Ortiz D, Henningsen EC. 2021.. Tactics of host manipulation by intracellular effectors from plant pathogenic fungi. . Curr. Opin. Plant Biol. 62::102054
    [Crossref] [Google Scholar]
  46. 46.
    Fischer LS, Klingner C, Schlichthaerle T, Strauss MT, Böttcher R, et al. 2021.. Quantitative single-protein imaging reveals molecular complex formation of integrin, talin, and kindlin during cell adhesion. . Nat. Commun. 12::919
    [Crossref] [Google Scholar]
  47. 47.
    Fletcher K, Gil J, Bertier LD, Kenefick A, Wood KJ, et al. 2019.. Genomic signatures of heterokaryosis in the oomycete pathogen Bremia lactucae. . Nat. Commun. 10::2645
    [Crossref] [Google Scholar]
  48. 48.
    Franceschetti M, Maqbool A, Jiménez-Dalmaroni MJ, Pennington HG, Kamoun S, Banfield MJ. 2017.. Effectors of filamentous plant pathogens: commonalities amid diversity. . Microbiol. Mol. Biol. Rev. 81:(2):e00066
    [Crossref] [Google Scholar]
  49. 49.
    Frank AB. 1887.. Ueber einige neue und weniger bekannte Pflanzenkrankheiten. II. . Ber. Dtsch. Bot. Ges. 1::5863
    [Google Scholar]
  50. 50.
    Gabriela M, Matthews KM, Boshoven C, Kouskousis B, Jonsdottir TK, et al. 2022.. A revised mechanism for how Plasmodium falciparum recruits and exports proteins into its erythrocytic host cell. . PLOS Pathog. 18:(2):e1009977
    [Crossref] [Google Scholar]
  51. 51.
    Garnica DP, Nemri A, Upadhyaya NM, Rathjen JP, Dodds PN. 2014.. The ins and outs of rust haustoria. . PLOS Pathog. 10:(9):e1004329
    [Crossref] [Google Scholar]
  52. 52.
    Gaulin E, Jacquet C, Bottin A, Dumas B. 2007.. Root rot disease of legumes caused by Aphanomyces euteiches. . Mol. Plant Pathol. 8:(5):53948
    [Crossref] [Google Scholar]
  53. 53.
    Giraldo MC, Dagdas YF, Gupta YK, Mentlak TA, Yi M, et al. 2013.. Two distinct secretion systems facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae. . Nat. Commun. 4::1996
    [Crossref] [Google Scholar]
  54. 54.
    Grenville-Briggs LJ, Anderson VL, Fugelstad J, Avrova AO, Bouzenzana J, et al. 2008.. Cellulose synthesis in Phytophthora infestans is required for normal appressorium formation and successful infection of potato. . Plant Cell 20:(3):72038
    [Crossref] [Google Scholar]
  55. 55.
    Grenville-Briggs LJ, Avrova AO, Bruce CR, Williams A, Whisson SC, et al. 2005.. Elevated amino acid biosynthesis in Phytophthora infestans during appressorium formation and potato infection. . Fungal Genet. Biol. 42:(3):24456
    [Crossref] [Google Scholar]
  56. 56.
    Grünwald NJ, LeBoldus JM, Hamelin RC. 2019.. Ecology and evolution of the sudden oak death pathogen Phytophthora ramorum. . Annu. Rev. Phytopathol. 57::30121
    [Crossref] [Google Scholar]
  57. 57.
    Hahn M, Mendgen K. 1992.. Isolation by ConA binding of haustoria from different rust fungi and comparison of their surface qualities. . Protoplasma 170:(3):95103
    [Crossref] [Google Scholar]
  58. 58.
    Hajra D, Nair AV, Chakravortty D. 2021.. An elegant nano-injection machinery for sabotaging the host: role of type III secretion system in virulence of different human and animal pathogenic bacteria. . Phys. Life Rev. 38::2554
    [Crossref] [Google Scholar]
  59. 59.
    Hardham AR. 2001.. The cell biology behind Phytophthora pathogenicity. . Aust. Plant Pathol. 30:(2):9198
    [Crossref] [Google Scholar]
  60. 60.
    Hardham AR. 2005.. Phytophthora cinnamomi. . Mol. Plant Pathol. 6:(6):589604
    [Crossref] [Google Scholar]
  61. 61.
    Hardham AR. 2007.. Cell biology of plant-oomycete interactions. . Cell. Microbiol. 9:(1):3139
    [Crossref] [Google Scholar]
  62. 62.
    Haswell ES, Meyerowitz EM. 2006.. MscS-like proteins control plastid size and shape in Arabidopsis thaliana. . Curr. Biol. 16:(1):111
    [Crossref] [Google Scholar]
  63. 63.
    Haswell ES, Phillips R, Rees DC. 2011.. Mechanosensitive channels: What can they do and how do they do it?. Structure 19:(10):135669
    [Crossref] [Google Scholar]
  64. 64.
    He M, Su J, Xu Y, Chen J, Chern M, et al. 2020.. Discovery of broad-spectrum fungicides that block septin-dependent infection processes of pathogenic fungi. . Nat. Microbiol. 5:(12):156575
    [Crossref] [Google Scholar]
  65. 65.
    Ho C-M, Beck JR, Lai M, Cui Y, Goldberg DE, et al. 2018.. Malaria parasite translocon structure and mechanism of effector export. . Nature 561:(7721):7075
    [Crossref] [Google Scholar]
  66. 66.
    Jiang R, He Q, Song J, Liu Z, Yu J, et al. 2023.. A Phytophthora infestans RXLR effector AVR8 suppresses plant immunity by targeting a desumoylating isopeptidase DeSI2. . Plant J. 115:(2):398413
    [Crossref] [Google Scholar]
  67. 67.
    Judelson HS, Ah-Fong AMV. 2018.. Exchanges at the plant–oomycete interface that influence disease. . Plant Physiol. 179:(4):1198211
    [Crossref] [Google Scholar]
  68. 68.
    Kagda MS, Martínez-Soto D, Ah-Fong AMV, Judelson HS. 2020.. Invertases in Phytophthora infestans localize to haustoria and are programmed for infection-specific expression. . mBio 11:(5):e01251-20
    [Crossref] [Google Scholar]
  69. 69.
    Kajornchaiyakul P, Brown JF. 1976.. The infection process and factors affecting infection of sunflower by Albugo tragopogi. . Trans. Br. Mycol. Soc. 66:(1):9195
    [Crossref] [Google Scholar]
  70. 70.
    Kale SD, Gu B, Capelluto DGS, Dou D, Feldman E, et al. 2010.. External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. . Cell 142:(2):28495
    [Crossref] [Google Scholar]
  71. 71.
    Kang Z, Huang LL, Buchenauer H. 2002.. Ultrastructural changes and localization of lignin and callose in compatible and incompatible interactions between wheat and Puccinia striiformis. . Z. Pflanzenkrankh. Pflanzenschutz 109::2537
    [Google Scholar]
  72. 72.
    Kanja C, Hammond-Kosack KE. 2020.. Proteinaceous effector discovery and characterization in filamentous plant pathogens. . Mol. Plant Pathol. 21:(10):135376
    [Crossref] [Google Scholar]
  73. 73.
    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:(4):1794804
    [Crossref] [Google Scholar]
  74. 74.
    Kasteel M, Ketelaar T, Govers F. 2023.. Fatal attraction: how Phytophthora zoospores find their host. . Semin. Cell Dev. Biol. 148/149::1321
    [Crossref] [Google Scholar]
  75. 75.
    Kay J, Meijer HJG, ten Have A, van Kan JAL. 2011.. The aspartic proteinase family of three Phytophthora species. . BMC Genom. 12::254
    [Crossref] [Google Scholar]
  76. 76.
    Kebdani N, Pieuchot L, Deleury E, Panabières F, Le Berre J-Y, Gourgues M. 2010.. Cellular and molecular characterization of Phytophthora parasitica appressorium–mediated penetration. . New Phytol. 185:(1):24857
    [Crossref] [Google Scholar]
  77. 77.
    Kefauver JM, Ward AB, Patapoutian A. 2020.. Discoveries in structure and physiology of mechanically activated ion channels. . Nature 587:(7835):56776
    [Crossref] [Google Scholar]
  78. 78.
    Kemen E, Gardiner A, Schultz-Larsen T, Kemen AC, Balmuth AL, et al. 2011.. Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. . PLOS Biol. 9:(7):e1001094
    [Crossref] [Google Scholar]
  79. 79.
    Kots K, Meijer HJG, Bouwmeester K, Govers F, Ketelaar T. 2017.. Filamentous actin accumulates during plant cell penetration and cell wall plug formation in Phytophthora infestans. . Cell. Mol. Life Sci. 74:(5):90920
    [Crossref] [Google Scholar]
  80. 80.
    Kwaaitaal M, Nielsen ME, Böhlenius H, Thordal-Christensen H. 2017.. The plant membrane surrounding powdery mildew haustoria shares properties with the endoplasmic reticulum membrane. . J. Exp. Bot. 68:(21/22):573143
    [Crossref] [Google Scholar]
  81. 81.
    Le S, Hu X, Yao M, Chen H, Yu M, et al. 2017.. Mechanotransmission and mechanosensing of human α-actinin 1. . Cell Rep. 21:(10):271423
    [Crossref] [Google Scholar]
  82. 82.
    Lee S, Kim J, Kim M-S, Min CW, Kim ST, et al. 2023.. A Phytophthora nucleolar effector, Pi23226, targets to host ribosome biogenesis for inducing necrotrophic cell death. . Plant Commun. 4:(5):100606
    [Crossref] [Google Scholar]
  83. 83.
    Li G, Dulal N, Gong Z, Wilson RA. 2023.. Unconventional secretion of Magnaporthe oryzae effectors in rice cells is regulated by tRNA modification and codon usage control. . Nat. Microbiol. 8::170616
    [Crossref] [Google Scholar]
  84. 84.
    Li L, Collier B, Spanu PD. 2019.. Isolation of powdery mildew haustoria from infected barley. . Bio-Protocol 9:(14):e3299
    [Crossref] [Google Scholar]
  85. 85.
    Li P, Li W, Zhou X, Situ J, Xie L, et al. 2023.. Peronophythora litchii RXLR effector P. litchii avirulence homolog 202 destabilizes a host ethylene biosynthesis enzyme. . Plant Physiol. 193:(1):75674
    [Crossref] [Google Scholar]
  86. 86.
    Li P, Zhang L, Mo X, Ji H, Bian H, et al. 2019.. Rice aquaporin PIP1;3 and harpin Hpa1 of bacterial blight pathogen cooperate in a type III effector translocation. . J. Exp. Bot. 70:(12):305773
    [Crossref] [Google Scholar]
  87. 87.
    Li T, Ai G, Fu X, Liu J, Zhu H, et al. 2022.. A Phytophthora capsici RXLR effector manipulates plant immunity by targeting RAB proteins and disturbing the protein trafficking pathway. . Mol. Plant Pathol. 23:(12):172136
    [Crossref] [Google Scholar]
  88. 88.
    Lin X, Wang S, de Rond L, Bertolin N, Wouters RHM, et al. 2020.. Divergent evolution of PcF/SCR74 effectors in oomycetes is associated with distinct recognition patterns in solanaceous plants. . mBio 11:(3):e00947
    [Google Scholar]
  89. 89.
    Littlefield LJ, Heath MC. 1979.. Ultrastructure of Rust Fungi. New York:: Academic
    [Google Scholar]
  90. 90.
    Liu J, Wang X. 2021.. Plant diseases and pests detection based on deep learning: a review. . Plant Methods 17:(1):22
    [Crossref] [Google Scholar]
  91. 91.
    Liu T, Song T, Zhang X, Yuan H, Su L, et al. 2014.. Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. . Nat. Commun. 5::4686
    [Crossref] [Google Scholar]
  92. 92.
    Lucas J, Hayter J, Crute I. 1995.. The downy mildews: host specificity and pathogenesis. . In Pathogenesis and Host Specificity in Plant Diseases, Vol. 2: Eukaryotes, ed. U Singh, R Singh , pp. 21734. Oxford, UK:: Permagon
    [Google Scholar]
  93. 93.
    Ludwig N, Reissmann S, Schipper K, Gonzalez C, Assmann D, et al. 2021.. A cell surface–exposed protein complex with an essential virulence function in Ustilago maydis. . Nat. Microbiol. 6:(6):72230
    [Crossref] [Google Scholar]
  94. 94.
    Manners JM, Gay JL. 1982.. Transport, translocation and metabolism of 14C-photosynthates at the host-parasite interface of Pisum sativum and Erysiphe pisi. . New Phytol. 91:(2):22144
    [Crossref] [Google Scholar]
  95. 95.
    Marapana DS, Dagley LF, Sandow JJ, Nebl T, Triglia T, et al. 2018.. Plasmepsin V cleaves malaria effector proteins in a distinct endoplasmic reticulum translocation interactome for export to the erythrocyte. . Nat. Microbiol. 3:(9):101022
    [Crossref] [Google Scholar]
  96. 96.
    Marra M, Camoni L, Visconti S, Fiorillo A, Evidente A. 2021.. The surprising story of fusicoccin: a wilt-inducing phytotoxin, a tool in plant physiology and a 14-3-3-targeted drug. . Biomolecules 11:(9):1393
    [Crossref] [Google Scholar]
  97. 97.
    Martin TJ, Ellingboe AH. 1978.. Genetic control of 32P transfer from wheat to Erysiphe graminis f. sp. tritici during primary infection. . Physiol. Plant Pathol. 13:(1):111
    [Crossref] [Google Scholar]
  98. 98.
    Martin-Urdiroz M, Oses-Ruiz M, Ryder LS, Talbot NJ. 2016.. Investigating the biology of plant infection by the rice blast fungus Magnaporthe oryzae. . Fungal Genet. Biol. 90::6168
    [Crossref] [Google Scholar]
  99. 99.
    McKinney LV, Nielsen LR, Collinge DB, Thomsen IM, Hansen JK, Kjaer ED. 2014.. The ash dieback crisis: Genetic variation in resistance can prove a long-term solution. . Plant Pathol. 63:(3):48599
    [Crossref] [Google Scholar]
  100. 100.
    Mendgen K. 1981.. Nutrient uptake in rust fungi. . Phytopathology 71:(9):98389
    [Crossref] [Google Scholar]
  101. 101.
    Micali CO, Neumann U, Grunewald D, Panstruga R, O'Connell R. 2011.. Biogenesis of a specialized plant-fungal interface during host cell internalization of Golovinomyces orontii haustoria. . Cell Microbiol. 13:(2):21026
    [Crossref] [Google Scholar]
  102. 102.
    Michels L, Bronkhorst J, Kasteel M, de Jong D, Albada B, et al. 2022.. Molecular sensors reveal the mechano-chemical response of Phytophthora infestans walls and membranes to mechanical and chemical stress. . Cell Surface 8::100071
    [Crossref] [Google Scholar]
  103. 103.
    Mims CW, Richardson EA, Holt BF III, Dangl JL. 2004.. Ultrastructure of the host–pathogen interface in Arabidopsis thaliana leaves infected by the downy mildew Hyaloperonospora parasitica. . Can. J. Bot. 82:(7):10018
    [Crossref] [Google Scholar]
  104. 104.
    Nakayama Y, Yoshimura K, Iida H. 2012.. Organellar mechanosensitive channels in fission yeast regulate the hypo-osmotic shock response. . Nat. Commun. 3::1020
    [Crossref] [Google Scholar]
  105. 105.
    Ngou BPM, Ding P, Jones JDG. 2022.. Thirty years of resistance: zig-zag through the plant immune system. . Plant Cell 34:(5):144778
    [Crossref] [Google Scholar]
  106. 106.
    O'Gara E, Howard K, McComb J, Colquhoun IJ, Hardy GESJ. 2015.. Penetration of suberized periderm of a woody host by Phytophthora cinnamomi. . Plant Pathol. 64:(1):20715
    [Crossref] [Google Scholar]
  107. 107.
    Oliveira-Garcia E, Tamang TM, Park J, Dalby M, Martin-Urdiroz M, et al. 2023.. Clathrin-mediated endocytosis facilitates the internalization of Magnaporthe oryzae effectors into rice cells. . Plant Cell 35:(7):252751
    [Crossref] [Google Scholar]
  108. 108.
    Papalazarou V, Machesky LM. 2021.. The cell pushes back: The Arp2/3 complex is a key orchestrator of cellular responses to environmental forces. . Curr. Opin. Cell Biol. 68::3744
    [Crossref] [Google Scholar]
  109. 109.
    Peresypkin VF, Loban VL, Voloshin NV. 1979.. Ultrastructure of haustoria and intercellular hyphae of Puccinia triticina Eriks mycelium. . Mikrobiol. Zh. 41:(3):24547
    [Google Scholar]
  110. 110.
    Pirc K, Clifton LA, Yilmaz N, Saltalamacchia A, Mally M, et al. 2022.. An oomycete NLP cytolysin forms transient small pores in lipid membranes. . Sci. Adv. 8:(10):eabj9406
    [Crossref] [Google Scholar]
  111. 111.
    Polonio Á, Seoane P, Claros MG, Pérez-García A. 2019.. The haustorial transcriptome of the cucurbit pathogen Podosphaera xanthii reveals new insights into the biotrophy and pathogenesis of powdery mildew fungi. . BMC Genom. 20::543
    [Crossref] [Google Scholar]
  112. 112.
    Rafiei V, Vélëz H, Tzelepis G. 2021.. The role of glycoside hydrolases in phytopathogenic fungi and oomycetes virulence. . Int. J. Mol. Sci. 22:(17):9359
    [Crossref] [Google Scholar]
  113. 113.
    Rose JKC, Ham K-S, Darvill AG, Albersheim P. 2002.. Molecular cloning and characterization of glucanase inhibitor proteins: coevolution of a counterdefense mechanism by plant pathogens. . Plant Cell 14:(6):132945
    [Crossref] [Google Scholar]
  114. 114.
    Rutter BD, Innes RW. 2023.. Extracellular vesicles in phytopathogenic fungi. . Extracell. Vesicles Circ. Nucleic Acids 4:(1):7288
    [Crossref] [Google Scholar]
  115. 115.
    Ryder LS, Cruz-Mireles N, Molinari C, Eisermann I, Eseola AB, Talbot NJ. 2022.. The appressorium at a glance. . J. Cell Sci. 135:(14):jcs259857
    [Crossref] [Google Scholar]
  116. 116.
    Ryder LS, Lopez SG, Michels L, Eseola AB, Sprakel J, et al. 2023.. A molecular mechanosensor for real-time visualization of appressorium membrane tension in Magnaporthe oryzae. . Nat. Microbiol. 8::150819
    [Crossref] [Google Scholar]
  117. 117.
    Schoina C, Verbeek-de Kruif N, Govers F, Bouwmeester K. 2019.. Clade 5 aspartic proteases of Phytophthora infestans are virulence factors implied in RXLR effector cleavage. . Eur. J. Plant Pathol. 154:(1):1729
    [Crossref] [Google Scholar]
  118. 118.
    Schornack S, van Damme M, Bozkurt TO, Cano LM, Smoker M, et al. 2010.. Ancient class of translocated oomycete effectors targets the host nucleus. . PNAS 107:(40):1742126
    [Crossref] [Google Scholar]
  119. 119.
    Seidl MF, Schneider A, Govers F, Snel B. 2013.. A predicted functional gene network for the plant pathogen Phytophthora infestans as a framework for genomic biology. . BMC Genom. 14::483
    [Crossref] [Google Scholar]
  120. 120.
    Seidl MF, van den Ackerveken G. 2019.. Activity and phylogenetics of the broadly occurring family of microbial Nep1-like proteins. . Annu. Rev. Phytopathol. 57::36786
    [Crossref] [Google Scholar]
  121. 121.
    Seo Y-E, Lee H-Y, Kim H, Yan X, Park SA, et al. 2023.. The Phytophthora capsici RxLR effector CRISIS2 triggers cell death via suppressing plasma membrane H+-ATPase in the host plant. . J. Exp. Bot. 74:(5):167589
    [Crossref] [Google Scholar]
  122. 122.
    Sharma R, Xia X, Cano LM, Evangelisti E, Kemen E, et al. 2015.. Genome analyses of the sunflower pathogen Plasmopara halstedii provide insights into effector evolution in downy mildews and Phytophthora. . BMC Genom. 16::741
    [Crossref] [Google Scholar]
  123. 123.
    Shepherd VA, Beilby MJ, Bisson MA. 2004.. When is a cell not a cell? A theory relating coenocytic structure to the unusual electrophysiology of Ventricaria ventricosa (Valonia ventricosa). . Protoplasma 223:(2–4):7991
    [Google Scholar]
  124. 124.
    Shimony C, Friend J. 1975.. Ultrastructure of the interaction between Phytophthora infestans and leaves of two cultivars of potato (Solanum tuberosum L.) Orion and Majestic. . New Phytol. 74:(1):5965
    [Crossref] [Google Scholar]
  125. 125.
    Silva MC, Nicole M, Rijo L, Geiger JP, Rodrigues, et al. 1999.. Cytochemical aspects of the plant–rust fungus interface during the compatible interaction Coffea arabica (cv. Caturra)–Hemileia vastatrix (race III). . Int. J. Plant Sci. 160:(1):7991
    [Crossref] [Google Scholar]
  126. 126.
    Song T, Ma Z, Shen D, Li Q, Li W, et al. 2015.. An oomycete CRN effector reprograms expression of plant HSP genes by targeting their promoters. . PLOS Pathog. 11:(12):e1005348
    [Crossref] [Google Scholar]
  127. 127.
    Sperschneider J, Dodds PN. 2022.. EffectorP 3.0: prediction of apoplastic and cytoplasmic effectors in fungi and oomycetes. . Mol. Plant. Microbe Interact. 35:(2):14656
    [Crossref] [Google Scholar]
  128. 128.
    Sperschneider J, Dodds PN, Singh KB, Taylor JM. 2018.. ApoplastP: prediction of effectors and plant proteins in the apoplast using machine learning. . New Phytol. 217:(4):176478
    [Crossref] [Google Scholar]
  129. 129.
    Stassen JHM, den Boer E, Vergeer PWJ, Andel A, Ellendorff U, et al. 2013.. Specific in planta recognition of two GKLR proteins of the downy mildew Bremia lactucae revealed in a large effector screen in lettuce. . Mol. Plant. Microbe Interact. 26:(11):125970
    [Crossref] [Google Scholar]
  130. 130.
    Stukenbrock E, Gurr S. 2023.. Address the growing urgency of fungal disease in crops. . Nature 617:(7959):3134
    [Crossref] [Google Scholar]
  131. 131.
    Sukharev SI, Martinac B, Arshavsky VY, Kung C. 1993.. Two types of mechanosensitive channels in the Escherichia coli cell envelope: solubilization and functional reconstitution. . Biophys. J. 65:(1):17783
    [Crossref] [Google Scholar]
  132. 132.
    Sun Y, Tayagui A, Garrill A, Nock V. 2020.. Microfluidic platform for integrated compartmentalization of single zoospores, germination and measurement of protrusive force generated by germ tubes. . Lab Chip 20:(22):414151
    [Crossref] [Google Scholar]
  133. 133.
    Thordal-Christensen H, Birch PRJ, Spanu PD, Panstruga R. 2018.. Why did filamentous plant pathogens evolve the potential to secrete hundreds of effectors to enable disease?. Mol. Plant Pathol. 19:(4):78185
    [Crossref] [Google Scholar]
  134. 134.
    Tian M, Benedetti B, Kamoun S. 2005.. A second Kazal-like protease inhibitor from Phytophthora infestans inhibits and interacts with the apoplastic pathogenesis-related protease P69B of tomato. . Plant Physiol. 138:(3):178593
    [Crossref] [Google Scholar]
  135. 135.
    Tian M, Huitema E, da Cunha L, Torto-Alalibo T, Kamoun S. 2004.. A Kazal-like extracellular serine protease inhibitor from Phytophthora infestans targets the tomato pathogenesis–related protease P69B. . J. Biol. Chem. 279:(25):2637077
    [Crossref] [Google Scholar]
  136. 136.
    Tian M, Win J, Savory E, Burkhardt A, Held M, et al. 2011.. 454 Genome sequencing of Pseudoperonospora cubensis reveals effector proteins with a QXLR translocation motif. . Mol. Plant. Microbe Interact. 24:(5):54353
    [Crossref] [Google Scholar]
  137. 137.
    Tomczynska I, Stumpe M, Mauch F. 2018.. A conserved RxLR effector interacts with host RABA-type GTPases to inhibit vesicle-mediated secretion of antimicrobial proteins. . Plant J. 95:(2):187203
    [Crossref] [Google Scholar]
  138. 138.
    Turner NC, Graniti A. 1969.. Fusicoccin: a fungal toxin that opens stomata. . Nature 223:(5210):107071
    [Crossref] [Google Scholar]
  139. 139.
    Virel A, Backman L. 2007.. A comparative and phylogenetic analysis of the α-actinin rod domain. . Mol. Biol. Evol. 24:(10):225465
    [Crossref] [Google Scholar]
  140. 140.
    Voegele RT, Struck C, Hahn M, Mendgen K. 2001.. The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. . PNAS 98:(14):813338
    [Crossref] [Google Scholar]
  141. 141.
    von Chamier L, Laine RF, Jukkala J, Spahn C, Krentzel D, et al. 2021.. Democratising deep learning for microscopy with ZeroCostDL4Mic. . Nat. Commun. 12::2276
    [Crossref] [Google Scholar]
  142. 142.
    Wang H, Guo B, Yang B, Li H, Xu Y, et al. 2021.. An atypical Phytophthora sojae RxLR effector manipulates host vesicle trafficking to promote infection. . PLOS Pathog. 17:(11):e1010104
    [Crossref] [Google Scholar]
  143. 143.
    Wang H, Wang S, Wang W, Xu L, Welsh LRJ, et al. 2023.. Uptake of oomycete RXLR effectors into host cells by clathrin-mediated endocytosis. . Plant Cell 35:(7):250426
    [Crossref] [Google Scholar]
  144. 144.
    Wang J, Tian L, Zhang D-D, Short DPG, Zhou L, et al. 2018.. SNARE-encoding genes VdSec22 and VdSso1 mediate protein secretion required for full virulence in Verticillium dahliae. . Mol. Plant. Microbe Interact. 31:(6):65164
    [Crossref] [Google Scholar]
  145. 145.
    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:(1):20515
    [Crossref] [Google Scholar]
  146. 146.
    Wang S, Welsh L, Thorpe P, Whisson SC, Boevink PC, Birch PRJ. 2018.. The Phytophthora infestans haustorium is a site for secretion of diverse classes of infection-associated proteins. . mBio 9:(4):e01216-18
    [Crossref] [Google Scholar]
  147. 147.
    Wang Z, Li T, Zhang X, Feng J, Liu Z, et al. 2023.. A Phytophthora infestans RXLR effector targets a potato ubiquitin-like domain–containing protein to inhibit the proteasome activity and hamper plant immunity. . New Phytol. 238:(2):78197
    [Crossref] [Google Scholar]
  148. 148.
    Wang Z, Zeng J, Deng J, Hou X, Zhang J, et al. 2023.. Pathogen-derived extracellular vesicles: emerging mediators of plant–microbe interactions. . Mol. Plant. Microbe Interact. 36:(4):21827
    [Crossref] [Google Scholar]
  149. 149.
    Wawra S, Trusch F, Matena A, Apostolakis K, Linne U, et al. 2017.. The RxLR motif of the host targeting effector AVR3a of Phytophthora infestans is cleaved before secretion. . Plant Cell 29:(6):118495
    [Crossref] [Google Scholar]
  150. 150.
    Webster J, Weber R. 2007.. Straminipila: minor fungal phyla. . In Introduction to Fungi, pp. 6774. Cambridge, UK:: Cambridge Univ. Press. , 3rd ed..
    [Google Scholar]
  151. 151.
    Whipps JM, Cooke RC. 1978.. Comparative physiology of Albugo tragopogonis–infected and Puccinia lagenophorae–infected plants of Senecio squalidus L. . New Phytol. 81:(2):30719
    [Crossref] [Google Scholar]
  152. 152.
    Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, et al. 2007.. A translocation signal for delivery of oomycete effector proteins into host plant cells. . Nature 450:(7166):11518
    [Crossref] [Google Scholar]
  153. 153.
    Yuen J. 2021.. Pathogens which threaten food security: Phytophthora infestans, the potato late blight pathogen. . Food Secur. 13:(2):24753
    [Crossref] [Google Scholar]
  154. 154.
    Zhang S, Xu J-R. 2014.. Effectors and effector delivery in Magnaporthe oryzae. . PLOS Pathog. 10:(1):e1003826
    [Crossref] [Google Scholar]
  155. 155.
    Zhao W, Dong S, Ye W, Hua C, Meijer HJG, et al. 2011.. Genome-wide identification of Phytophthora sojae SNARE genes and functional characterization of the conserved SNARE PsYKT6. . Fungal Genet. Biol. 48:(3):24151
    [Crossref] [Google Scholar]
  156. 156.
    Zheng L, Mackrill JJ. 2016.. Calcium signaling in oomycetes: an evolutionary perspective. . Front. Physiol. 7::123
    [Crossref] [Google Scholar]
  157. 157.
    Zhu J, Qiao Q, Sun Y, Xu Y, Shu H, et al. 2023.. Divergent sequences of tetraspanins enable plants to specifically recognize microbe-derived extracellular vesicles. . Nat. Commun. 14::4877
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-micro-032421-121423
Loading
/content/journals/10.1146/annurev-micro-032421-121423
Loading

Data & Media loading...

  • 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