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Abstract

Gene silencing guided by small RNAs governs a broad range of cellular processes in eukaryotes. Small RNAs are important components of plant immunity because they contribute to pathogen-triggered transcription reprogramming and directly target pathogen RNAs. Recent research suggests that silencing of pathogen genes by plant small RNAs occurs not only during viral infection but also in nonviral pathogens through a process termed host-induced gene silencing, which involves -species small RNA trafficking. Similarly, small RNAs are also produced by eukaryotic pathogens and regulate virulence. This review summarizes the small RNA pathways in both plants and filamentous pathogens, including fungi and oomycetes, and discusses their role in host–pathogen interactions. We highlight secondarysmall interfering RNAs of plants as regulators of immune receptor gene expression and executors of host-induced gene silencing in invading pathogens. The current status and prospects of -species gene silencing at the host–pathogen interface are discussed.

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2021-08-25
2024-04-25
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Literature Cited

  1. 1. 
    Ah-Fong AM, Bormann-Chung CA, Judelson HS. 2008. Optimization of transgene-mediated silencing in Phytophthora infestans and its association with small-interfering RNAs. Fungal Genet. Biol. 45:1197–205
    [Google Scholar]
  2. 2. 
    Allen E, Xie Z, Gustafson AM, Carrington JC. 2005. microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–21
    [Google Scholar]
  3. 3. 
    Alonso-Peral MM, Li J, Li Y, Allen RS, Schnippenkoetter W et al. 2010. The microRNA159-regulated GAMYB-like genes inhibit growth and promote programmed cell death in Arabidopsis. Plant Physiol 154:757–71
    [Google Scholar]
  4. 4. 
    Alvarez JP, Pekker I, Goldshmidt A, Blum E, Amsellem Z, Eshed Y. 2006. Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell 18:1134–51
    [Google Scholar]
  5. 5. 
    Asman AK, Fogelqvist J, Vetukuri RR, Dixelius C. 2016. Phytophthora infestans Argonaute 1 binds microRNA and small RNAs from effector genes and transposable elements. New Phytol 211:993–1007
    [Google Scholar]
  6. 6. 
    Axtell MJ. 2013. Classification and comparison of small RNAs from plants. Annu. Rev. Plant Biol. 64:137–59
    [Google Scholar]
  7. 7. 
    Bai Y, Lan F, Yang W, Zhang F, Yang K et al. 2015. sRNA profiling in Aspergillus flavus reveals differentially expressed miRNA-like RNAs response to water activity and temperature. Fungal Genet. Biol. 81:113–19
    [Google Scholar]
  8. 8. 
    Baldrich P, Rutter BD, Karimi HZ, Podicheti R, Meyers BC, Innes RW. 2019. Plant extracellular vesicles contain diverse small RNA species and are enriched in 10- to 17-nucleotide “tiny” RNAs. Plant Cell 31:315–24
    [Google Scholar]
  9. 9. 
    Barkan A, Small I. 2014. Pentatricopeptide repeat proteins in plants. Annu. Rev. Plant Biol. 65:415–42
    [Google Scholar]
  10. 10. 
    Baulcombe DC. 2015. VIGS, HIGS and FIGS: small RNA silencing in the interactions of viruses or filamentous organisms with their plant hosts. Curr. Opin. Plant Biol. 26:141–46
    [Google Scholar]
  11. 11. 
    Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P et al. 2007. Control of coleopteran insect pests through RNA interference. Nat. Biotechnol. 25:1322–26
    [Google Scholar]
  12. 12. 
    Beakes GW, Glockling SL, Sekimoto S. 2012. The evolutionary phylogeny of the oomycete “fungi. .” Protoplasma 249:3–19
    [Google Scholar]
  13. 13. 
    Billmyre RB, Calo S, Feretzaki M, Wang X, Heitman J 2013. RNAi function, diversity, and loss in the fungal kingdom. Chromosome Res 21:561–72
    [Google Scholar]
  14. 14. 
    Bollmann SR, Fang Y, Press CM, Tyler BM, Grunwald NJ. 2016. Diverse evolutionary trajectories for small RNA biogenesis genes in the oomycete genus. Phytophthora. Front. Plant Sci 7:284
    [Google Scholar]
  15. 15. 
    Bollmann SR, Press CM, Tyler BM, Grunwald NJ. 2018. Expansion and divergence of Argonaute genes in the oomycete genus Phytophthora. Front. Microbiol 9:2841
    [Google Scholar]
  16. 16. 
    Bologna NG, Voinnet O. 2014. The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu. Rev. Plant Biol. 65:473–503
    [Google Scholar]
  17. 17. 
    Borges F, Martienssen RA. 2015. The expanding world of small RNAs in plants. Nat. Rev. Mol. Cell Biol. 16:727–41
    [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. 
    Cai Q, Qiao L, Wang M, He B, Lin FM et al. 2018. Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science 360:1126–29
    [Google Scholar]
  20. 20. 
    Campo S, Gilbert KB, Carrington JC. 2016. Small RNA-based antiviral defense in the phytopathogenic fungus Colletotrichum higginsianum. PLOS Pathog 12:6e1005640
    [Google Scholar]
  21. 21. 
    Canto-Pastor A, Santos B, Valli AA, Summers W, Schornack S, Baulcombe DC 2019. Enhanced resistance to bacterial and oomycete pathogens by short tandem target mimic RNAs in tomato. PNAS 116:2755–60
    [Google Scholar]
  22. 22. 
    Cantu D, Govindarajulu M, Kozik A, Wang M, Chen X et al. 2011. Next generation sequencing provides rapid access to the genome of Puccinia striiformis f. sp. tritici, the causal agent of wheat stripe rust. PLOS ONE 6:e24230
    [Google Scholar]
  23. 23. 
    Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S et al. 2010. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465:316–21
    [Google Scholar]
  24. 24. 
    Chang SS, Zhang Z, Liu Y. 2012. RNA interference pathways in fungi: mechanisms and functions. Annu. Rev. Microbiol. 66:305–23
    [Google Scholar]
  25. 25. 
    Chen K, Liu L, Zhang X, Yuan Y, Ren S et al. 2018. Phased secondary small interfering RNAs in Panax notoginseng. BMC Genom 19:41
    [Google Scholar]
  26. 26. 
    Chen R, Jiang N, Jiang Q, Sun X, Wang Y et al. 2014. Exploring microRNA-like small RNAs in the filamentous fungus Fusarium oxysporum. PLOS ONE 9:e104956
    [Google Scholar]
  27. 27. 
    Chen X. 2010. Small RNAs: secrets and surprises of the genome. Plant J 61:941–58
    [Google Scholar]
  28. 28. 
    Chen Y, Gao Q, Huang M, Liu Y, Liu Z et al. 2015. Characterization of RNA silencing components in the plant pathogenic fungus Fusarium graminearum. Sci. Rep. 5:12500
    [Google Scholar]
  29. 29. 
    Chen Y, Kistler HC, Ma Z. 2019. Fusarium graminearum trichothecene mycotoxins: biosynthesis, regulation, and management. Annu. Rev. Phytopathol. 57:15–39
    [Google Scholar]
  30. 30. 
    Chisholm ST, Coaker G, Day B, Staskawicz BJ. 2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–14
    [Google Scholar]
  31. 31. 
    Chow FW, Koutsovoulos G, Ovando-Vazquez C, Neophytou K, Bermudez-Barrientos JR et al. 2019. Secretion of an Argonaute protein by a parasitic nematode and the evolution of its siRNA guides. Nucleic Acids Res 47:3594–606
    [Google Scholar]
  32. 32. 
    Colombo M, Raposo G, Thery C. 2014. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell Dev. Biol. 30:255–89
    [Google Scholar]
  33. 33. 
    Cui H, Tsuda K, Parker JE. 2015. Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66:487–511
    [Google Scholar]
  34. 34. 
    de Felippes FF, Ott F, Weigel D. 2011. Comparative analysis of non-autonomous effects of tasiRNAs and miRNAs in Arabidopsis thaliana. Nucleic Acids Res 39:2880–89
    [Google Scholar]
  35. 35. 
    Deng Y, Wang J, Tung J, Liu D, Zhou Y et al. 2018. A role for small RNA in regulating innate immunity during plant growth. PLOS Pathog 14:e1006756
    [Google Scholar]
  36. 36. 
    Dong S, Ma W. 2021. How to win a tug-of-war: the adaptive evolution of Phytophthora effectors. Curr. Opin. Plant Biol. 62:102027
    [Google Scholar]
  37. 37. 
    Dong S, Raffaele S, Kamoun S. 2015. The two-speed genomes of filamentous pathogens: waltz with plants. Curr. Opin. Genet. Dev. 35:57–65
    [Google Scholar]
  38. 38. 
    Dou D, Zhou JM. 2012. Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe 12:484–95
    [Google Scholar]
  39. 39. 
    Dubey H, Kiran K, Jaswal R, Jain P, Kayastha AM et al. 2019. Discovery and profiling of small RNAs from Puccinia triticina by deep sequencing and identification of their potential targets in wheat. Funct. Integr. Genom. 19:391–407
    [Google Scholar]
  40. 40. 
    Dunker F, Trutzenberg A, Rothenpieler JS, Kuhn S, Prols R et al. 2020. Oomycete small RNAs bind to the plant RNA-induced silencing complex for virulence. eLife 9:56096
    [Google Scholar]
  41. 41. 
    Dunoyer P, Melnyk C, Molnar A, Slotkin RK. 2013. Plant mobile small RNAs. Cold Spring Harb. Perspect. Biol. 5:7a017897
    [Google Scholar]
  42. 42. 
    Ellendorff U, Fradin EF, de Jonge R, Thomma BP. 2009. RNA silencing is required for Arabidopsis defence against Verticillium wilt disease. J. Exp. Bot. 60:591–602
    [Google Scholar]
  43. 43. 
    Espino J, Gonzalez M, Gonzalez C, Brito N. 2014. Efficiency of different strategies for gene silencing in Botrytis cinerea. Appl. Microbiol. Biotechnol. 98:9413–24
    [Google Scholar]
  44. 44. 
    Fahlgren N, Bollmann SR, Kasschau KD, Cuperus JT, Press CM et al. 2013. Phytophthora have distinct endogenous small RNA populations that include short interfering and microRNAs. PLOS ONE 8:e77181
    [Google Scholar]
  45. 45. 
    Fei Q, Li P, Teng C, Meyers BC. 2015. Secondary siRNAs from Medicago NB-LRRs modulated via miRNA-target interactions and their abundances. Plant J 83:451–65
    [Google Scholar]
  46. 46. 
    Fei Q, Xia R, Meyers BC. 2013. Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell 25:2400–15
    [Google Scholar]
  47. 47. 
    Fei Q, Zhang Y, Xia R, Meyers BC. 2016. Small RNAs add zing to the zig-zag-zig model of plant defenses. Mol. Plant-Microbe Interact. 29:165–69
    [Google Scholar]
  48. 48. 
    Feldbrugge M, Zarnack K, Vollmeister E, Baumann S, Koepke J et al. 2008. The posttranscriptional machinery of Ustilago maydis. Fungal Genet. Biol. 45:Suppl. 1S40–46
    [Google Scholar]
  49. 49. 
    Gasciolli V, Mallory AC, Bartel DP, Vaucheret H. 2005. Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr. Biol. 15:1494–500
    [Google Scholar]
  50. 50. 
    Ghildiyal M, Zamore PD. 2009. Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 10:94–108
    [Google Scholar]
  51. 51. 
    Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43:205–27
    [Google Scholar]
  52. 52. 
    Govindarajulu M, Epstein L, Wroblewski T, Michelmore RW. 2015. Host-induced gene silencing inhibits the biotrophic pathogen causing downy mildew of lettuce. Plant Biotechnol. J. 13:875–83
    [Google Scholar]
  53. 53. 
    Gowda M, Nunes CC, Sailsbery J, Xue M, Chen F et al. 2010. Genome-wide characterization of methylguanosine-capped and polyadenylated small RNAs in the rice blast fungus Magnaporthe oryzae. Nucleic Acids Res 38:7558–69
    [Google Scholar]
  54. 54. 
    Guo MW, Yang P, Zhang JB, Liu G, Yuan QS et al. 2019. Expression of microRNA-like RNA-2 (Fgmil-2) and bioH1 from a single transcript in Fusarium graminearum are inversely correlated to regulate biotin synthesis during vegetative growth and host infection. Mol. Plant Pathol. 20:1574–81
    [Google Scholar]
  55. 55. 
    Guo N, Ye WW, Wu XL, Shen DY, Wang YC et al. 2011. Microarray profiling reveals microRNAs involving soybean resistance to Phytophthora sojae. Genome 54:954–58
    [Google Scholar]
  56. 56. 
    Guo Z, Li Y, Ding SW. 2019. Small RNA-based antimicrobial immunity. Nat. Rev. Immunol. 19:31–44
    [Google Scholar]
  57. 57. 
    Hou Y, Ma W. 2020. Natural host-induced gene silencing offers new opportunities to engineer disease resistance. Trends Microbiol 28:109–17
    [Google Scholar]
  58. 58. 
    Hou Y, Zhai Y, Feng L, Karimi HZ, Rutter BD et al. 2019. A Phytophthora effector suppresses trans-kingdom RNAi to promote disease susceptibility. Cell Host Microbe 25:153–65.e5
    [Google Scholar]
  59. 59. 
    Howell MD, Fahlgren N, Chapman EJ, Cumbie JS, Sullivan CM et al. 2007. Genome-wide analysis of the RNA-DEPENDENT RNA POLYMERASE6/DICER-LIKE4 pathway in Arabidopsis reveals dependency on miRNA- and tasiRNA-directed targeting. Plant Cell 19:926–42
    [Google Scholar]
  60. 60. 
    Huang G, Allen R, Davis EL, Baum TJ, Hussey RS 2006. Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. PNAS 103:14302–6
    [Google Scholar]
  61. 61. 
    Hudzik C, Hou Y, Ma W, Axtell MJ. 2020. Exchange of small regulatory RNAs between plants and their pests. Plant Physiol 182:51–62
    [Google Scholar]
  62. 62. 
    Huot B, Yao J, Montgomery BL, He SY. 2014. Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol. Plant 7:1267–87
    [Google Scholar]
  63. 63. 
    Jahan SN, Asman AK, Corcoran P, Fogelqvist J, Vetukuri RR, Dixelius C. 2015. Plant-mediated gene silencing restricts growth of the potato late blight pathogen Phytophthora infestans. J. Exp. Bot. 66:2785–94
    [Google Scholar]
  64. 64. 
    Ji L, Chen X 2012. Regulation of small RNA stability: methylation and beyond. Cell Res 22:624–36
    [Google Scholar]
  65. 65. 
    Jia J, Lu W, Zhong C, Zhou R, Xu J et al. 2017. The 25–26 nt small RNAs in Phytophthora parasitica are associated with efficient silencing of homologous endogenous genes. Front. Microbiol 8:773
    [Google Scholar]
  66. 66. 
    Jin Y, Zhao JH, Zhao P, Zhang T, Wang S, Guo HS 2019. A fungal milRNA mediates epigenetic repression of a virulence gene in Verticillium dahliae. Philos. Trans. R. Soc. Lond. B 374:20180309
    [Google Scholar]
  67. 67. 
    Jones JD, Dangl JL. 2006. The plant immune system. Nature 444:323–29
    [Google Scholar]
  68. 68. 
    Kadotani N, Nakayashiki H, Tosa Y, Mayama S. 2003. RNA silencing in the phytopathogenic fungus Magnaporthe oryzae. Mol. Plant-Microbe Interact. 16:769–76
    [Google Scholar]
  69. 69. 
    Kadotani N, Nakayashiki H, Tosa Y, Mayama S. 2004. One of the two Dicer-like proteins in the filamentous fungi Magnaporthe oryzae genome is responsible for hairpin RNA-triggered RNA silencing and related small interfering RNA accumulation. J. Biol. Chem. 279:44467–74
    [Google Scholar]
  70. 70. 
    Kamoun S, Furzer O, Jones JD, Judelson HS, Ali GS et al. 2015. The top 10 oomycete pathogens in molecular plant pathology. Mol. Plant Pathol. 16:413–34
    [Google Scholar]
  71. 71. 
    Karasov TL, Chae E, Herman JJ, Bergelson J 2017. Mechanisms to mitigate the trade-off between growth and defense. Plant Cell 29:666–80
    [Google Scholar]
  72. 72. 
    Kettles GJ, Hofinger BJ, Hu P, Bayon C, Rudd JJ et al. 2019. sRNA profiling combined with gene function analysis reveals a lack of evidence for cross-kingdom RNAi in the wheat–Zymoseptoria tritici pathosystem. Front. Plant Sci. 10:892
    [Google Scholar]
  73. 73. 
    Khatabi B, Arikit S, Xia R, Winter S, Oumar D et al. 2016. High-resolution identification and abundance profiling of cassava (Manihot esculenta Crantz) microRNAs. BMC Genom 17:85
    [Google Scholar]
  74. 74. 
    Kim G, LeBlanc ML, Wafula EK, dePamphilis CW, Westwood JH. 2014. Plant science. Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science 345:808–11
    [Google Scholar]
  75. 75. 
    Klosterman SJ, Atallah ZK, Vallad GE, Subbarao KV. 2009. Diversity, pathogenicity, and management of Verticillium species. Annu. Rev. Phytopathol. 47:39–62
    [Google Scholar]
  76. 76. 
    Kuan T, Zhai Y, Ma W. 2016. Small RNAs regulate plant responses to filamentous pathogens. Semin. Cell Dev. Biol. 56:190–200
    [Google Scholar]
  77. 77. 
    Kulcheski FR, de Oliveira LF, Molina LG, Almerao MP, Rodrigues FA et al. 2011. Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genom 12:307
    [Google Scholar]
  78. 78. 
    Lee HC, Li L, Gu W, Xue Z, Crosthwaite SK et al. 2010. Diverse pathways generate microRNA-like RNAs and Dicer-independent small interfering RNAs in fungi. Mol. Cell 38:803–14
    [Google Scholar]
  79. 79. 
    Li F, Pignatta D, Bendix C, Brunkard JO, Cohn MM et al. 2012. MicroRNA regulation of plant innate immune receptors. PNAS 109:1790–95
    [Google Scholar]
  80. 80. 
    Li L, Habring A, Wang K, Weigel D. 2020. Atypical resistance protein RPW8/HR triggers oligomerization of the NLR immune receptor RPP7 and autoimmunity. Cell Host Microbe 27:405–17.e6
    [Google Scholar]
  81. 81. 
    Li S, Le B, Ma X, Li S, You C et al. 2016. Biogenesis of phased siRNAs on membrane-bound polysomes in Arabidopsis. eLife 5:e22750
    [Google Scholar]
  82. 82. 
    Li Y, Liu X, Yin Z, You Y, Zou Y et al. 2020. MicroRNA-like milR236, regulated by transcription factor MoMsn2, targets histone acetyltransferase MoHat1 to play a role in appressorium formation and virulence of the rice blast fungus Magnaporthe oryzae. Fungal Genet. Biol. 137:103349
    [Google Scholar]
  83. 83. 
    Li Y, Zhang Q, Zhang J, Wu L, Qi Y, Zhou JM. 2010. Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity. Plant Physiol 152:2222–31
    [Google Scholar]
  84. 84. 
    Liu J, Cheng X, Liu D, Xu W, Wise R, Shen QH. 2014. The miR9863 family regulates distinct Mla alleles in barley to attenuate NLR receptor-triggered disease resistance and cell-death signaling. PLOS Genet 10:e1004755
    [Google Scholar]
  85. 85. 
    Liu L, Chen X. 2018. Intercellular and systemic trafficking of RNAs in plants. Nat. Plants 4:869–78
    [Google Scholar]
  86. 86. 
    Liu T, Hu J, Zuo Y, Jin Y, Hou J 2016. Identification of microRNA-like RNAs from Curvularia lunata associated with maize leaf spot by bioinformation analysis and deep sequencing. Mol. Genet. Genom. 291:587–96
    [Google Scholar]
  87. 87. 
    Ma KW, Ma W. 2016. Phytohormone pathways as targets of pathogens to facilitate infection. Plant Mol. Biol. 91:713–25
    [Google Scholar]
  88. 88. 
    Ma W, Chen C, Liu Y, Zeng M, Meyers BC et al. 2018. Coupling of microRNA-directed phased small interfering RNA generation from long noncoding genes with alternative splicing and alternative polyadenylation in small RNA-mediated gene silencing. New Phytol 217:1535–50
    [Google Scholar]
  89. 89. 
    Matzke MA, Mosher RA. 2014. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat. Rev. Genet. 15:394–408
    [Google Scholar]
  90. 90. 
    Melnyk CW, Molnar A, Baulcombe DC. 2011. Intercellular and systemic movement of RNA silencing signals. EMBO J 30:3553–63
    [Google Scholar]
  91. 91. 
    Melonek J, Zhou R, Bayer PE, Edwards D, Stein N, Small I. 2019. High intraspecific diversity of restorer-of-fertility-like genes in barley. Plant J 97:281–95
    [Google Scholar]
  92. 92. 
    Meng H, Wang Z, Wang Y, Zhu H, Huang B. 2017. Dicer and Argonaute genes involved in RNA interference in the entomopathogenic fungus Metarhizium robertsii. Appl. Environ. Microbiol. 83:7e03230–16
    [Google Scholar]
  93. 93. 
    Mochama P, Jadhav P, Neupane A, Lee Marzano SY 2018. Mycoviruses as triggers and targets of RNA silencing in white mold fungus Sclerotinia sclerotiorum. Viruses 10:4214
    [Google Scholar]
  94. 94. 
    Mueth NA, Ramachandran SR, Hulbert SH. 2015. Small RNAs from the wheat stripe rust fungus (Puccinia striiformis f.sp. tritici).. BMC Genom 16:718
    [Google Scholar]
  95. 95. 
    Nakayashiki H, Kadotani N, Mayama S. 2006. Evolution and diversification of RNA silencing proteins in fungi. J. Mol. Evol. 63:127–35
    [Google Scholar]
  96. 96. 
    Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N et al. 2006. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–39
    [Google Scholar]
  97. 97. 
    Nowara D, Gay A, Lacomme C, Shaw J, Ridout C et al. 2010. HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell 22:3130–41
    [Google Scholar]
  98. 98. 
    Nunes CC, Gowda M, Sailsbery J, Xue M, Chen F et al. 2011. Diverse and tissue-enriched small RNAs in the plant pathogenic fungus, Magnaporthe oryzae. BMC Genom 12:288
    [Google Scholar]
  99. 99. 
    Pais M, Yoshida K, Giannakopoulou A, Pel MA, Cano LM et al. 2018. Gene expression polymorphism underpins evasion of host immunity in an asexual lineage of the Irish potato famine pathogen. BMC Evol. Biol. 18:93
    [Google Scholar]
  100. 100. 
    Parizotto EA, Dunoyer P, Rahm N, Himber C, Voinnet O. 2004. In vivo investigation of the transcription, processing, endonucleolytic activity, and functional relevance of the spatial distribution of a plant miRNA. Genes Dev 18:2237–42
    [Google Scholar]
  101. 101. 
    Park MS, Sim G, Kehling AC, Nakanishi K 2020. Human Argonaute2 and Argonaute3 are catalytically activated by different lengths of guide RNA. PNAS 117:28576–78
    [Google Scholar]
  102. 102. 
    Qiao Y, Liu L, Xiong Q, Flores C, Wong J et al. 2013. Oomycete pathogens encode RNA silencing suppressors. Nat. Genet. 45:330–33
    [Google Scholar]
  103. 103. 
    Qutob D, Chapman BP, Gijzen M. 2013. Transgenerational gene silencing causes gain of virulence in a plant pathogen. Nat. Commun. 4:1349
    [Google Scholar]
  104. 104. 
    Rabouille C. 2017. Pathways of unconventional protein secretion. Trends Cell Biol 27:230–40
    [Google Scholar]
  105. 105. 
    Raman V, Simon SA, Demirci F, Nakano M, Meyers BC, Donofrio NM. 2017. Small RNA functions are required for growth and development of Magnaporthe oryzae. Mol. Plant-Microbe Interact. 30:517–30
    [Google Scholar]
  106. 106. 
    Rogers K, Chen X. 2013. Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25:2383–99
    [Google Scholar]
  107. 107. 
    Ronemus M, Vaughn MW, Martienssen RA. 2006. MicroRNA-targeted and small interfering RNA-mediated mRNA degradation is regulated by Argonaute, Dicer, and RNA-dependent RNA polymerase in Arabidopsis. Plant Cell 18:1559–74
    [Google Scholar]
  108. 108. 
    Rutter BD, Innes RW. 2018. Extracellular vesicles as key mediators of plant-microbe interactions. Curr. Opin. Plant Biol. 44:16–22
    [Google Scholar]
  109. 109. 
    Sarkies P, Miska EA. 2014. Small RNAs break out: the molecular cell biology of mobile small RNAs. Nat. Rev. Mol. Cell Biol. 15:525–35
    [Google Scholar]
  110. 110. 
    Shao Y, Tang J, Chen S, Wu Y, Wang K et al. 2019. milR4 and milR16 mediated fruiting body development in the medicinal fungus Cordyceps militaris. Front. Microbiol. 10:83
    [Google Scholar]
  111. 111. 
    Shivaprasad PV, Chen HM, Patel K, Bond DM, Santos BA, Baulcombe DC. 2012. A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24:859–74
    [Google Scholar]
  112. 112. 
    Skopelitis DS, Hill K, Klesen S, Marco CF, von Born P et al. 2018. Gating of miRNA movement at defined cell-cell interfaces governs their impact as positional signals. Nat. Commun. 9:3107
    [Google Scholar]
  113. 113. 
    Smith LM, Burbano HA, Wang X, Fitz J, Wang G et al. 2015. Rapid divergence and high diversity of miRNAs and miRNA targets in the Camelineae. Plant J 81:597–610
    [Google Scholar]
  114. 114. 
    Son H, Park AR, Lim JY, Shin C, Lee YW. 2017. Genome-wide exonic small interference RNA-mediated gene silencing regulates sexual reproduction in the homothallic fungus Fusarium graminearum. PLOS Genet 13:e1006595
    [Google Scholar]
  115. 115. 
    Takemoto D, Jones DA, Hardham AR. 2003. GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. Plant J 33:775–92
    [Google Scholar]
  116. 116. 
    Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J. 2003. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74–77
    [Google Scholar]
  117. 117. 
    Trieu TA, Calo S, Nicolas FE, Vila A, Moxon S et al. 2015. A non-canonical RNA silencing pathway promotes mRNA degradation in basal fungi. PLOS Genet 11:e1005168
    [Google Scholar]
  118. 118. 
    Vetukuri RR, Asman AK, Tellgren-Roth C, Jahan SN, Reimegard J et al. 2012. Evidence for small RNAs homologous to effector-encoding genes and transposable elements in the oomycete Phytophthora infestans. PLOS ONE 7:e51399
    [Google Scholar]
  119. 119. 
    Vetukuri RR, Avrova AO, Grenville-Briggs LJ, Van West P, Soderbom F et al. 2011. Evidence for involvement of Dicer-like, Argonaute and histone deacetylase proteins in gene silencing in Phytophthora infestans. Mol. Plant Pathol. 12:772–85
    [Google Scholar]
  120. 120. 
    Wang B, Sun Y, Song N, Zhao M, Liu R et al. 2017. Puccinia striiformis f. sp. tritici microRNA-like RNA 1 (Pst-milR1), an important pathogenicity factor of Pst, impairs wheat resistance to Pst by suppressing the wheat pathogenesis-related 2 gene. New Phytol 215:338–50
    [Google Scholar]
  121. 121. 
    Wang L, Chen H, Li J, Shu H, Zhang X et al. 2020. Effector gene silencing mediated by histone methylation underpins host adaptation in an oomycete plant pathogen. Nucleic Acids Res 48:1790–99
    [Google Scholar]
  122. 122. 
    Wang M, Weiberg A, Dellota E Jr., Yamane D, Jin H. 2017. Botrytis small RNA Bc-siR37 suppresses plant defense genes by cross-kingdom RNAi. RNA Biol 14:421–28
    [Google Scholar]
  123. 123. 
    Wang Q, Li T, Xu K, Zhang W, Wang X et al. 2016. The tRNA-derived small RNAs regulate gene expression through triggering sequence-specific degradation of target transcripts in the oomycete pathogen Phytophthora sojae. Front. Plant Sci. 7:1938
    [Google Scholar]
  124. 124. 
    Weiberg A, Wang M, Lin FM, Zhao H, Zhang Z et al. 2013. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:118–23
    [Google Scholar]
  125. 125. 
    Whisson SC, Boevink PC, Wang S, Birch PR 2016. The cell biology of late blight disease. Curr. Opin. Microbiol. 34:127–35
    [Google Scholar]
  126. 126. 
    Whisson SC, Vetukuri RR, Avrova AO, Dixelius C. 2012. Can silencing of transposons contribute to variation in effector gene expression in Phytophthora infestans?. Mob. Genet. Elements 2:110–14
    [Google Scholar]
  127. 127. 
    Williamson B, Tudzynski B, Tudzynski P, van Kan JA. 2007. Botrytis cinerea: the cause of grey mould disease. Mol. Plant Pathol. 8:561–80
    [Google Scholar]
  128. 128. 
    Wilson RA, Talbot NJ. 2009. Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat. Rev. Microbiol. 7:185–95
    [Google Scholar]
  129. 129. 
    Wong J, Gao L, Yang Y, Zhai J, Arikit S et al. 2014. Roles of small RNAs in soybean defense against Phytophthora sojae infection. Plant J 79:928–40
    [Google Scholar]
  130. 130. 
    Xia R, Meyers BC, Liu Z, Beers EP, Ye S, Liu Z. 2013. MicroRNA superfamilies descended from miR390 and their roles in secondary small interfering RNA biogenesis in eudicots. Plant Cell 25:1555–72
    [Google Scholar]
  131. 131. 
    Xia R, Xu J, Arikit S, Meyers BC. 2015. Extensive families of miRNAs and PHAS loci in Norway spruce demonstrate the origins of complex phasiRNA networks in seed plants. Mol. Biol. Evol. 32:2905–18
    [Google Scholar]
  132. 132. 
    Xia R, Zhu H, An YQ, Beers EP, Liu Z. 2012. Apple miRNAs and tasiRNAs with novel regulatory networks. Genome Biol 13:R47
    [Google Scholar]
  133. 133. 
    Xu M, Guo Y, Tian R, Gao C, Guo F et al. 2020. Adaptive regulation of virulence genes by microRNA-like RNAs in Valsa mali. New Phytol 227:899–913
    [Google Scholar]
  134. 134. 
    Yang F. 2015. Genome-wide analysis of small RNAs in the wheat pathogenic fungus Zymoseptoria tritici. Fungal Biol 119:631–40
    [Google Scholar]
  135. 135. 
    Yang L, Mu X, Liu C, Cai J, Shi K et al. 2015. Overexpression of potato miR482e enhanced plant sensitivity to Verticillium dahliae infection. J. Integr. Plant Biol. 57:1078–88
    [Google Scholar]
  136. 136. 
    Yang M, Woolfenden HC, Zhang Y, Fang X, Liu Q et al. 2020. Intact RNA structurome reveals mRNA structure-mediated regulation of miRNA cleavage in vivo. Nucleic Acids Res 48:8767–81
    [Google Scholar]
  137. 137. 
    Ye W, Ma W. 2016. Filamentous pathogen effectors interfering with small RNA silencing in plant hosts. Curr. Opin. Microbiol. 32:1–6
    [Google Scholar]
  138. 138. 
    Yi M, Valent B. 2013. Communication between filamentous pathogens and plants at the biotrophic interface. Annu. Rev. Phytopathol. 51:587–611
    [Google Scholar]
  139. 139. 
    Yin C, Ramachandran SR, Zhai Y, Bu C, Pappu HR, Hulbert SH. 2019. A novel fungal effector from Puccinia graminis suppressing RNA silencing and plant defense responses. New Phytol 222:1561–72
    [Google Scholar]
  140. 140. 
    Yin C, Zhu H, Jiang Y, Shan Y, Gong L. 2020. Silencing Dicer-like genes reduces virulence and sRNA generation in Penicillium italicum, the cause of citrus blue mold. Cells 9:2363
    [Google Scholar]
  141. 141. 
    Yu Y, Jia T, Chen X. 2017. The ‘how’ and ‘where’ of plant microRNAs. New Phytol 216:1002–17
    [Google Scholar]
  142. 142. 
    Zeng W, Wang J, Wang Y, Lin J, Fu Y et al. 2018. Dicer-like proteins regulate sexual development via the biogenesis of perithecium-specific microRNAs in a plant pathogenic fungus Fusarium graminearum. Front. Microbiol. 9:818
    [Google Scholar]
  143. 143. 
    Zhai J, Jeong DH, De Paoli E, Park S, Rosen BD et al. 2011. MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev 25:2540–53
    [Google Scholar]
  144. 144. 
    Zhang T, Jin Y, Zhao JH, Gao F, Zhou BJ et al. 2016. Host-induced gene silencing of the target gene in fungal cells confers effective resistance to the cotton wilt disease pathogen Verticillium dahliae. Mol. Plant 9:939–42
    [Google Scholar]
  145. 145. 
    Zhang T, Zhao YL, Zhao JH, Wang S, Jin Y et al. 2016. Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen. Nat. Plants 2:16153
    [Google Scholar]
  146. 146. 
    Zhang Y, Xia R, Kuang H, Meyers BC. 2016. The diversification of plant NBS-LRR defense genes directs the evolution of microRNAs that target them. Mol. Biol. Evol. 33:2692–705
    [Google Scholar]
  147. 147. 
    Zhao Y, Li Y, Qiu M, Ma W, Wang Y 2018. Generating gene silenced mutants in Phytophthora sojae. Methods Mol. Biol. 1848:275–86
    [Google Scholar]
  148. 148. 
    Zheng Y, Wang Y, Wu J, Ding B, Fei Z. 2015. A dynamic evolutionary and functional landscape of plant phased small interfering RNAs. BMC Biol 13:32
    [Google Scholar]
  149. 149. 
    Zhou J, Fu Y, Xie J, Li B, Jiang D et al. 2012. Identification of microRNA-like RNAs in a plant pathogenic fungus Sclerotinia sclerotiorum by high-throughput sequencing. Mol. Genet. Genom. 287:275–82
    [Google Scholar]
  150. 150. 
    Zhou JM, Zhang Y. 2020. Plant immunity: danger perception and signaling. Cell 181:978–89
    [Google Scholar]
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