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Annual Review of Phytopathology

Volume 59, 2021

Emerging Roles of Posttranslational Modifications in Plant-Pathogenic Fungi and Bacteria

Abstract

Posttranslational modifications (PTMs) play crucial roles in regulating protein function and thereby control many cellular processes and biological phenotypes in both eukaryotes and prokaryotes. Several recent studies illustrate how plant fungal and bacterial pathogens use these PTMs to facilitate development, stress response, and host infection. In this review, we discuss PTMs that have key roles in the biological and infection processes of plant-pathogenic fungi and bacteria. The emerging roles of PTMs during pathogen–plant interactions are highlighted. We also summarize traditional tools and emerging proteomics approaches for PTM research. These discoveries open new avenues for investigating the fundamental infection mechanisms of plant pathogens and the discovery of novel strategies for plant disease control.

Keyword(s): infection process, plant-pathogenic pathogen, plant–pathogen interaction, posttranslational modification, regulatory mechanism
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/content/journals/10.1146/annurev-phyto-021320-010948
2021-08-25
2024-04-23
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Literature Cited

  1. 1. 
    Ba Van V, Kieu Thi Minh P, Nakayashiki H 2013. Substrate-induced transcriptional activation of the MoCel7C cellulase gene is associated with methylation of histone H3 at lysine 4 in the rice blast fungus Magnaporthe oryzae. Appl. Environ. Microbiol. 79:6823–32
     [Google Scholar]
  2. 2. 
    Baidyaroy D, Brosch G, Ahn J-H, Graessle S, Wegener S et al. 2001. A gene related to yeast HOS2 histone deacetylase affects extracellular depolymerase expression and virulence in a plant pathogenic fungus. Plant Cell 13:1609–24
     [Google Scholar]
  3. 3. 
    Barski A, Cuddapah S, Cui K, Roh T-Y, Schones DE et al. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129:823–37
     [Google Scholar]
  4. 4. 
    Benoist P, Muller A, Diem HG, Schwencke J. 1992. High-molecular-mass multicatalytic proteinase complexes produced by the nitrogen-fixing actinomycete Frankia strain BB. J. Bacteriol. 174:1495–504
     [Google Scholar]
  5. 5. 
    Bohnert S, Neumann H, Thines E, Jacob S 2019. Visualizing fungicide action: an in vivo tool for rapid validation of fungicides with target location HOG pathway. Pest Manag. Sci. 75:772–78
     [Google Scholar]
  6. 6. 
    Buettner D. 2016. Behind the lines: actions of bacterial type III effector proteins in plant cells. FEMS Microbiol. Rev. 40:894–937
     [Google Scholar]
  7. 7. 
    Buscaill P, Chandrasekar B, Sanguankiattichai N, Kourelis J, Kaschani F et al. 2019. Glycosidase and glycan polymorphism control hydrolytic release of immunogenic flagellin peptides. Science 364:eaav0748
     [Google Scholar]
  8. 8. 
    Camilli A, Bassler BL. 2006. Bacterial small-molecule signaling pathways. Science 311:1113–16
     [Google Scholar]
  9. 9. 
    Cao Z, Buttani V, Losi A, Gaertner W. 2008. A blue light inducible two-component signal transduction system in the plant pathogen Pseudomonas syringae pv. tomato. Biophys. J. 94:897–905
     [Google Scholar]
  10. 10. 
    Cao Z, Yin Y, Sun X, Han J, Sun QP et al. 2016. An Ash1-like protein MoKMT2H null mutant is delayed for conidium germination and pathogenesis in Magnaporthe oryzae. Biomed. Res. Int. 2016:1575430
     [Google Scholar]
  11. 11. 
    Carabetta VJ, Cristea IM. 2017. Regulation, function, and detection of protein acetylation in bacteria. J. Bacteriol. 199:e00107–17
     [Google Scholar]
  12. 12. 
    Charollais J, Van Der Goot FG. 2009. Palmitoylation of membrane proteins (review. Mol. Membr. Biol. 26:55–66
     [Google Scholar]
  13. 13. 
    Chen H-J, Awakawa T, Sun J-Y, Wakimoto T, Abe I 2013. Epigenetic modifier-induced biosynthesis of novel fusaric acid derivatives in endophytic fungi from Datura stramonium L. Nat. Prod. Bioprospect. 3:20–23
     [Google Scholar]
  14. 14. 
    Chen Q, Li Y, Wang J, Li R, Chen B 2018. cpubi4 is essential for development and virulence in chestnut blight fungus. Front. Microbiol. 9:1286
     [Google Scholar]
  15. 15. 
    Chen X-L, Liu C, Tang B, Ren Z, Wang G-L, Liu W. 2020. Quantitative proteomics analysis reveals important roles of N-glycosylation on ER quality control system for development and pathogenesis in Magnaporthe oryzae. PLOS Pathog. 16:e1008355
     [Google Scholar]
  16. 16. 
    Chen X-L, Shi T, Yang J, Shi W, Gao X et al. 2014. N-Glycosylation of effector proteins by an α-1,3-mannosyltransferase is required for the rice blast fungus to evade host innate immunity. Plant Cell 26:1360–76
     [Google Scholar]
  17. 17. 
    Chen Y, Wang J, Yang N, Wen Z, Sun X et al. 2018. Wheat microbiome bacteria can reduce virulence of a plant pathogenic fungus by altering histone acetylation. Nat. Commun. 9:3429
     [Google Scholar]
  18. 18. 
    Connolly LR, Smith KM, Freitag M. 2013. The Fusarium graminearum histone H3 K27 methyltransferase KMT6 regulates development and expression of secondary metabolite gene clusters. PLOS Genet. 9:e1003916
     [Google Scholar]
  19. 19. 
    Corfield AP, Berry M. 2015. Glycan variation and evolution in the eukaryotes. Trends Biochem. Sci. 40:351–59
     [Google Scholar]
  20. 20. 
    Dallery J-F, Adelin E, Le Goff G, Pigne S, Auger A et al. 2019. H3K4 trimethylation by CclA regulates pathogenicity and the production of three families of terpenoid secondary metabolites in Colletotrichum higginsianum. Mol. Plant Pathol. 20:831–42
     [Google Scholar]
  21. 21. 
    de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y et al. 2010. Conserved fungal lysm effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953–55
     [Google Scholar]
  22. 22. 
    De Maayer P, Cowan DA. 2016. Flashy flagella. flagellin modification is relatively common and highly versatile among the Enterobacteriaceae. BMC Genom. 17:377
     [Google Scholar]
  23. 23. 
    Ding S-L, Liu W, Iliuk A, Ribot C, Vallet J et al. 2010. The Tig1 histone deacetylase complex regulates infectious growth in the rice blast fungus Magnaporthe oryzae. Plant Cell 22:2495–508
     [Google Scholar]
  24. 24. 
    Dixon KP, Xu JR, Smirnoff N, Talbot NJ. 1999. Independent signaling pathways regulate cellular turgor during hyperosmotic stress and appressorium-mediated plant infection by Magnaporthe grisea. Plant Cell 11:2045–58
     [Google Scholar]
  25. 25. 
    Doehlemann G, Reissmann S, Assmann D, Fleckenstein M, Kahmann R. 2011. Two linked genes encoding a secreted effector and a membrane protein are essential for Ustilago maydis-induced tumour formation. Mol. Microbiol. 81:751–66
     [Google Scholar]
  26. 26. 
    Doehlemann G, van der Linde K, Amann D, Schwammbach D, Hof A et al. 2009. Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLOS Pathog. 5:e1000290
     [Google Scholar]
  27. 27. 
    Dubey A, Jeon J. 2017. Epigenetic regulation of development and pathogenesis in fungal plant pathogens. Mol. Plant Pathol. 18:887–98
     [Google Scholar]
  28. 28. 
    Dubey A, Lee J, Kwon S, Lee Y-H, Jeon J 2019. A MYST family histone acetyltransferase, MoSAS3, is required for development and pathogenicity in the rice blast fungus. Mol. Plant Pathol. 20:1491–505
     [Google Scholar]
  29. 29. 
    Elhenawy W, Scott NE, Tondo ML, Orellano EG, Foster LJ, Feldman MF. 2016. Protein O-linked glycosylation in the plant pathogen Ralstonia solanacearum. Glycobiology 26:301–11
     [Google Scholar]
  30. 30. 
    Elias-Villalobos A, Barrales RR, Ibeas JI. 2019. Chromatin modification factors in plant pathogenic fungi: insights from Ustilago maydis. Fungal Genet. Biol. 129:52–64
     [Google Scholar]
  31. 31. 
    Elias-Villalobos A, Fernandez-Alvarez A, Moreno-Sanchez I, Helmlinger D, Ibeas JI. 2015. The Hos2 histone deacetylase controls Ustilago maydis virulence through direct regulation of mating-type genes. PLOS Pathog. 11:e1005134
     [Google Scholar]
  32. 32. 
    Fang W, Robinson DA, Raimi OG, Blair DE, Harrison JR et al. 2015. N-Myristoyltransferase is a cell wall target in Aspergillus fumigatus. ACS Chem. Biol. 10:1425–34
     [Google Scholar]
  33. 33. 
    Farazi TA, Waksman G, Gordon JI. 2001. The biology and enzymology of protein N-myristoylation. J. Biol. Chem. 276:39501–4
     [Google Scholar]
  34. 34. 
    Fernandez-Alvarez A, Elias-Villalobos A, Ibeas JI 2009. The O-mannosyltransferase PMT4 is essential for normal appressorium formation and penetration in Ustilago maydis. Plant Cell 21:3397–412
     [Google Scholar]
  35. 35. 
    Fernandez-Alvarez A, Elias-Villalobos A, Jimenez-Martin A, Marin-Menguiano M, Ibeas JI. 2013. Endoplasmic reticulum glucosidases and protein quality control factors cooperate to establish biotrophy in Ustilago maydis. Plant Cell 25:4676–90
     [Google Scholar]
  36. 36. 
    Fernandez-Alvarez A, Marin-Menguiano M, Lanver D, Jimenez-Martin A, Elias-Villalobos A et al. 2012. Identification of O-mannosylated virulence factors in Ustilago maydis. PLOS Pathog. 8:e1002563
     [Google Scholar]
  37. 37. 
    Fernandez J, Marroquin-Guzman M, Nandakumar R, Shijo S, Cornwell KM et al. 2014. Plant defence suppression is mediated by a fungal sirtuin during rice infection by Magnaporthe oryzae. Mol. Microbiol. 94:70–88
     [Google Scholar]
  38. 38. 
    Figaj D, Ambroziak P, Przepiora T, Skorko-Glonek J. 2019. The role of proteases in the virulence of plant pathogenic bacteria. Int. J. Mol. Sci. 20:672
     [Google Scholar]
  39. 39. 
    Fliegmann J, Felix G. 2016. Immunity. flagellin seen from all sides. Nat. Plants 2:16136
     [Google Scholar]
  40. 40. 
    Franck WL, Gokce E, Randall SM, Oh Y, Eyre A et al. 2015. Phosphoproteome analysis links protein phosphorylation to cellular remodeling and metabolic adaptation during Magnaporthe oryzae appressorium development. J. Proteome Res. 14:2408–24
     [Google Scholar]
  41. 41. 
    Fujita M, Kinoshita T. 2012. GPI-anchor remodeling: potential functions of GPI-anchors in intracellular trafficking and membrane dynamics. Biochim. Biophys. Acta 1821:1050–58
     [Google Scholar]
  42. 42. 
    Furukawa K, Randhawa A, Kaur H, Mondal AK, Hohmann S. 2012. Fungal fludioxonil sensitivity is diminished by a constitutively active form of the group III histidine kinase. FEBS Lett. 586:2417–22
     [Google Scholar]
  43. 43. 
    Gareau JR, Lima CD. 2010. The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nat. Rev. Mol. Cell Biol. 11:861–71
     [Google Scholar]
  44. 44. 
    Garrido E, Voss U, Muller P, Castillo-Lluva S, Kahmann R, Perez-Martin J. 2004. The induction of sexual development and virulence in the smut fungus Ustilago maydis depends on Crk1, a novel MAPK protein. Genes Dev. 18:3117–30
     [Google Scholar]
  45. 45. 
    Gold S, Duncan G, Barrett K, Kronstad J. 1994. cAMP regulates morphogenesis in the fungal pathogen Ustilago maydis. Genes Dev. 8:2805–16
     [Google Scholar]
  46. 46. 
    Gonzalez M, Brito N, Frias M, Gonzalez C. 2013. Botrytis cinerea protein O-mannosyltransferases play critical roles in morphogenesis, growth, and virulence. PLOS ONE 8:e65924
     [Google Scholar]
  47. 47. 
    Gu Q, Ji T, Sun X, Huang H, Zhang H et al. 2017. Histone H3 lysine 9 methyltransferase FvDim5 regulates fungal development, pathogenicity and osmotic stress responses in Fusarium verticillioides. FEMS Microbiol. Lett. 364:fnx184
     [Google Scholar]
  48. 48. 
    Gu Q, Tahir HAS, Zhang H, Huang H, Ji T et al. 2017. Involvement of FvSet1 in fumonisin B1 biosynthesis, vegetative growth, fungal virulence, and environmental stress responses in Fusarium verticillioides. Toxins 9:43
     [Google Scholar]
  49. 49. 
    Gu Q, Wang Z, Sun X, Ji T, Huang H et al. 2017. FvSet2 regulates fungal growth, pathogenicity, and secondary metabolism in Fusarium verticillioides. Fungal Genet. Biol. 107:24–30
     [Google Scholar]
  50. 50. 
    Gu Q, Zhang C, Yu F, Yin Y, Shim W-B, Ma Z 2015. Protein kinase FgSch9 serves as a mediator of the target of rapamycin and high osmolarity glycerol pathways and regulates multiple stress responses and secondary metabolism in Fusarium graminearum. Environ. Microbiol. 17:2661–76
     [Google Scholar]
  51. 51. 
    Guo M, Gao F, Zhu X, Nie X, Pan Y, Gao Z. 2015. MoGrr1, a novel F-box protein, is involved in conidiogenesis and cell wall integrity and is critical for the full virulence of Magnaporthe oryzae. Appl. Microbiol. Biotechnol. 99:8075–88
     [Google Scholar]
  52. 52. 
    Guo M, Tan L, Nie X, Zhu X, Pan Y, Gao Z. 2016. The Pmt2p-mediated protein O-mannosylation is required for morphogenesis, adhesive properties, cell wall integrity and full virulence of Magnaporthe oryzae. Front. Microbiol. 7:630
     [Google Scholar]
  53. 53. 
    Harries E, Gandia M, Carmona L, Marcos JF. 2015. The Penicillium digitatum protein O-mannosyltransferase Pmt2 is required for cell wall integrity, conidiogenesis, virulence and sensitivity to the antifungal peptide PAF26. Mol. Plant Pathol. 16:748–61
     [Google Scholar]
  54. 54. 
    Helenius A, Aebi M. 2004. Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73:1019–49
     [Google Scholar]
  55. 55. 
    Hendy AA, Xing J, Chen X, Chen X-L. 2019. The farnesyltransferase β-subunit RAM1 regulates localization of RAS proteins and appressorium-mediated infection in Magnaporthe oryzae. Mol. Plant Pathol. 20:1264–78
     [Google Scholar]
  56. 56. 
    Hershko A, Ciechanover A. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425–79
     [Google Scholar]
  57. 57. 
    Hirai H, Takai R, Kondo M, Furukawa T, Hishiki T et al. 2014. Glycan moiety of flagellin in Acidovorax avenae K1 prevents the recognition by rice that causes the induction of immune responses. Plant Signal. Behav. 9:e972782
     [Google Scholar]
  58. 58. 
    Hou J, Feng H-Q, Chang H-W, Liu Y, Li G-H et al. 2020. The H3K4 demethylase Jar1 orchestrates ROS production and expression of pathogenesis-related genes to facilitate Botrytis cinerea virulence. New Phytol. 225:930–47
     [Google Scholar]
  59. 59. 
    Huh A, Dubey A, Kim S, Jeon J, Lee Y-H. 2017. MoJMJ1, encoding a histone demethylase containing JmjC domain, is required for pathogenic development of the rice blast fungus, Magnaporthe oryzae. Plant Pathol. J. 33:193–205
     [Google Scholar]
  60. 60. 
    Ichinose Y, Taguchi F, Yamamoto M, Ohnishi-Kameyama M, Atsumi T et al. 2013. Flagellin glycosylation is ubiquitous in a broad range of phytopathogenic bacteria. J. Gen. Plant Pathol. 79:359–65
     [Google Scholar]
  61. 61. 
    Imber M, Pietrzyk-Brzezinska AJ, Antelmann H. 2019. Redox regulation by reversible protein S-thiolation in Gram-positive bacteria. Redox Biol. 20:130–45
     [Google Scholar]
  62. 62. 
    Izawa M, Takekawa O, Arie T, Teraoka T, Yoshida M et al. 2009. Inhibition of histone deacetylase causes reduction of appressorium formation in the rice blast fungus Magnaporthe oryzae. J. Gen. Appl. Microbiol. 55:489–98
     [Google Scholar]
  63. 63. 
    Jacinto E, Hall MN 2003. TOR signalling in bugs. brain and brawn. Nat. Rev. Mol. Cell Biol. 4:117–26
     [Google Scholar]
  64. 64. 
    Jacob S, Foster AJ, Yemelin A, Thines E. 2015. High osmolarity glycerol (HOG) signalling in Magnaporthe oryzae: identification of MoYPD1 and its role in osmoregulation, fungicide action, and pathogenicity. Fungal Biol. 119:580–94
     [Google Scholar]
  65. 65. 
    Jacob S, Schueffler A, Thines E. 2016. Hog1p activation by marasmic acid through inhibition of the histidine kinase SIn1p. Pest Manag. Sci. 72:1268–74
     [Google Scholar]
  66. 66. 
    Janevska S, Baumann L, Sieber CMK, Muensterkoetter M, Ulrich J et al. 2018. Elucidation of the two H3K36me3 histone methyltransferases Set2 and Ash1 in Fusarium fujikuroi unravels their different chromosomal targets and a major impact of Ash1 on genome stability. Genetics 208:153–71
     [Google Scholar]
  67. 67. 
    Janevska S, Gueldener U, Sulyok M, Tudzynski B, Studt L. 2018. Set1 and Kdm5 are antagonists for H3K4 methylation and regulators of the major conidiation-specific transcription factor gene ABA1 in Fusarium fujikuroi. Environ. Microbiol. 20:3343–62
     [Google Scholar]
  68. 68. 
    Jiang C, Zhang X, Liu H, Xu J-R. 2018. Mitogen-activated protein kinase signaling in plant pathogenic fungi. PLOS Pathog. 14:e1006875
     [Google Scholar]
  69. 69. 
    Jiang H, Zhang X, Chen X, Aramsangtienchai P, Tong Z, Lin H. 2018. Protein lipidation: occurrence, mechanisms, biological functions, and enabling technologies. Chem. Rev. 118:43–112
     [Google Scholar]
  70. 70. 
    Kieu Thi Minh P, Inoue Y, Ba Van V Hanh, Hieu N, Nakayashiki T et al. 2015. MoSET1 (histone H3K4 methyltransferase in Magnaportheoryzae) regulates global gene expression during infection-related morphogenesis. PLOS Genet. 11:e1005385
     [Google Scholar]
  71. 71. 
    Kong X, van Diepeningen AD, van der Lee TAJ, Waalwijk C, Xu J et al. 2018. The Fusarium graminearum histone acetyltransferases are important for morphogenesis, DON biosynthesis, and pathogenicity. Front. Microbiol. 9:654
     [Google Scholar]
  72. 72. 
    Koomey M. 2019. O-Linked protein glycosylation in bacteria: snapshots and current perspectives. Curr. Opin. Struct. Biol. 56:198–203
     [Google Scholar]
  73. 73. 
    Ku JWK, Gan Y-H. 2019. Modulation of bacterial virulence and fitness by host glutathione. Curr. Opin. Microbiol. 47:8–13
     [Google Scholar]
  74. 74. 
    Kwon S, Lee J, Jeon J, Kim S, Park S-Y et al. 2018. Role of the histone acetyltransferase Rtt109 in development and pathogenicity of the rice blast fungus. Mol. Plant-Microbe Interact. 31:1200–10
     [Google Scholar]
  75. 75. 
    Lan H, Sun R, Fan K, Yang K, Zhang F et al. 2016. The Aspergillus flavus histone acetyl transferase AflGcnE regulates morphogenesis, aflatoxin biosynthesis, and pathogenicity. Front. Microbiol. 7:1324
     [Google Scholar]
  76. 76. 
    Lee J, Lee J-J, Jeon J 2019. A histone deacetylase. MoHOS2 regulates asexual development and virulence in the rice blast fungus. J. Microbiol. 57:1115–25
     [Google Scholar]
  77. 77. 
    Lee S-H, Lee J, Lee S, Park E-H, Kim K-W et al. 2009. GzSNF1 is required for normal sexual and asexual development in the ascomycete Gibberella zeae. Eukaryot. Cell 8:116–27
     [Google Scholar]
  78. 78. 
    Li D, Agrellos OA, Calderone R. 2010. Histidine kinases keep fungi safe and vigorous. Curr. Opin. Microbiol. 13:424–30
     [Google Scholar]
  79. 79. 
    Li G, Qi X, Sun G, Rocha RO, Segal LM et al. 2020. Terminating rice innate immunity induction requires a network of antagonistic and redox-responsive E3 ubiquitin ligases targeting a fungal sirtuin. New Phytol. 226:523–40
     [Google Scholar]
  80. 80. 
    Li H, Yu C, Chen H, Tian F, He C. 2015. PXO_00987, a putative acetyltransferase, is required for flagellin glycosylation, and regulates flagellar motility, exopolysaccharide production, and biofilm formation in Xanthomonas oryzae pv. oryzae. Microb. Pathog. 85:50–57
     [Google Scholar]
  81. 81. 
    Li W, Ancona V, Zhao Y. 2014. Co-regulation of polysaccharide production, motility, and expression of type III secretion genes by EnvZ/OmpR and GrrS/GrrA systems in Erwinia amylovora. Mol. Genet. Genom. 289:63–75
     [Google Scholar]
  82. 82. 
    Li Y, Wang C, Liu W, Wang G, Kang Z et al. 2011. The HDF1 histone deacetylase gene is important for conidiation, sexual reproduction, and pathogenesis in Fusarium graminearum. Mol. Plant-Microbe Interact. 24:487–96
     [Google Scholar]
  83. 83. 
    Li Y, Xue H, Bian D-r, Xu G, Piao C. 2020. Acetylome analysis of lysine acetylation in the plant pathogenic bacterium Brenneria nigrifluens. MicrobiologyOpen 9:e952
     [Google Scholar]
  84. 84. 
    Li Z, Zhang C, Li C, Zhou J, Xu X et al. 2020. S-Glutathionylation proteome profiling reveals a crucial role of a thioredoxin-like protein in interspecies competition and cariogenecity of Streptococcus mutans. PLOS Pathog. 16:e1008774
     [Google Scholar]
  85. 85. 
    Liang M, Zhang S, Dong L, Kou Y, Lin C et al. 2018. Label-free quantitative proteomics of lysine acetylome identifies substrates of Gcn5 in Magnaporthe oryzae autophagy and epigenetic regulation. mSystems 3:e00270–18
     [Google Scholar]
  86. 86. 
    Lim Y-J, Kim K-T, Lee Y-H. 2018. SUMOylation is required for fungal development and pathogenicity in the rice blast fungus Magnaporthe oryzae. Mol. Plant Pathol. 19:2134–48
     [Google Scholar]
  87. 87. 
    Liu C, Li Z, Xing J, Yang J, Wang Z et al. 2018. Global analysis of sumoylation function reveals novel insights into development and appressorium-mediated infection of the rice blast fungus. New Phytol. 219:1031–47
     [Google Scholar]
  88. 88. 
    Liu C, Xing J, Cai X, Hendy A, He W et al. 2020. GPI7-mediated glycosylphosphatidylinositol anchoring regulates appressorial penetration and immune evasion during infection of Magnaporthe oryzae. Environ. Microbiol. 22:2581–95
     [Google Scholar]
  89. 89. 
    Liu Y, Liu N, Yin Y, Chen Y, Jiang J, Ma Z. 2015. Histone H3K4 methylation regulates hyphal growth. secondary metabolism and multiple stress responses in Fusarium graminearum. Environ. Microbiol. 17:4615–30
     [Google Scholar]
  90. 90. 
    Lodge JK, Jackson-Machelski E, Toffaletti DL, Perfect JR, Gordon JI 1994. Targeted gene replacement demonstrates that myristoyl-CoA:protein N-myristoyltransferase is essential for viability of Cryptococcus neoformans. PNAS 91:12008–12
     [Google Scholar]
  91. 91. 
    Lommel M, Strahl S. 2009. Protein O-mannosylation. conserved from bacteria to humans. Glycobiology 19:816–28
     [Google Scholar]
  92. 92. 
    Lopez-Fernandez L, Ruiz-Roldan C, Pareja-Jaime Y, Prieto A, Khraiwesh H, Roncero MIG. 2013. The Fusarium oxysporumgnt2, encoding a putative N-acetylglucosamine transferase, is involved in cell wall architecture and virulence. PLOS ONE 8:e84690
     [Google Scholar]
  93. 93. 
    Marroquin-Guzman M, Sun G, Wilson RA. 2017. Glucose-ABL1-TOR signaling modulates cell cycle tuning to control terminal appressorial cell differentiation. PLOS Genet. 13:e1006557
     [Google Scholar]
  94. 94. 
    Marroquin-Guzman M, Wilson RA. 2015. GATA-dependent glutaminolysis drives appressorium formation in Magnaporthe oryzae by suppressing TOR inhibition of cAMP/PKA signaling. PLOS Pathog. 11:e1004851
     [Google Scholar]
  95. 95. 
    Miguel-Rojas C, Hera C 2016. The F-box protein Fbp1 functions in the invasive growth and cell wall integrity mitogen-activated protein kinase (MAPK) pathways in Fusarium oxysporum. Mol. Plant Pathol. 17:55–64
     [Google Scholar]
  96. 96. 
    Mitchell TK, Dean RA. 1995. The cAMP-dependent protein-kinase catalytic subunit is required for appressorium formation and pathogenesis by the rice blast pathogen Magnaporthe grisea. Plant Cell 7:1869–78
     [Google Scholar]
  97. 97. 
    Motteram J, Lovegrove A, Pirie E, Marsh J, Devonshire J et al. 2011. Aberrant protein N-glycosylation impacts upon infection-related growth transitions of the haploid plant-pathogenic fungus Mycosphaerella graminicola. Mol. Microbiol. 81:415–33
     [Google Scholar]
  98. 98. 
    Muller AU, Weber-Ban E. 2019. The bacterial proteasome at the core of diverse degradation pathways. Front. Mol. Biosci. 6:23
     [Google Scholar]
  99. 99. 
    Nathues E, Joergens C, Lorenz N, Tudzynski P. 2007. The histidine kinase CpHK2 has impact on spore germination. oxidative stress and fungicide resistance, and virulence of the ergot fungus Claviceps purpurea. Mol. Plant Pathol. 8:653–65
     [Google Scholar]
  100. 100. 
    O'Malley MR, Chien C-F, Peck SC, Lin N-C, Anderson JC. 2020. A revised model for the role of GacS/GacA in regulating type III secretion by Pseudomonas syringae pv. tomato DC3000. Mol. Plant Pathol. 21:139–44
     [Google Scholar]
  101. 101. 
    Oh Y, Franck WL, Han S-O, Shows A, Gokce E et al. 2012. Polyubiquitin is required for growth, development and pathogenicity in the rice blast fungus Magnaporthe oryzae. PLOS ONE 7:e42868
     [Google Scholar]
  102. 102. 
    Oliveira-Garcia E, Deising HB 2016. The glycosylphosphatidylinositol anchor biosynthesis genes GPI12, GAA1, and GPI8 are essential for cell-wall integrity and pathogenicity of the maize anthracnose fungus Colletotrichum graminicola. Mol. Plant-Microbe Interact. 29:889–901
     [Google Scholar]
  103. 103. 
    Ospina-Giraldo MD, Mullins E, Kang S. 2003. Loss of function of the Fusarium oxysporumSNF1 gene reduces virulence on cabbage and Arabidopsis. Curr. Genet. 44:49–57
     [Google Scholar]
  104. 104. 
    Pan Y, Pan R, Tan L, Zhang Z, Guo M. 2019. Pleiotropic roles of O-mannosyltransferase MoPmt4 in development and pathogenicity of Magnaporthe oryzae. Curr. Genet. 65:223–39
     [Google Scholar]
  105. 105. 
    Petrocelli S, Arana MR, Cabrini MN, Casabuono AC, Moyano L et al. 2016. Deletion of pilA, a minor pilin-like gene, from Xanthomonas citri subsp. citri influences bacterial physiology and pathogenesis. Curr. Microbiol. 73:904–14
     [Google Scholar]
  106. 106. 
    Prakash C, Manjrekar J, Chattoo BB. 2016. Skp1, a component of E3 ubiquitin ligase, is necessary for growth, sporulation, development and pathogenicity in rice blast fungus (Magnaporthe oryzae. Mol. Plant Pathol. 17:903–19
     [Google Scholar]
  107. 107. 
    Qian B, Liu X, Jia J, Cai Y, Chen C et al. 2018. MoPpe1 partners with MoSap1 to mediate TOR and cell wall integrity signalling in growth and pathogenicity of the rice blast fungus Magnaporthe oryzae. Environ. Microbiol. 20:3964–79
     [Google Scholar]
  108. 108. 
    Rabut G, Peter M. 2008. Function and regulation of protein neddylation. ‘Protein modifications: beyond the usual suspects’ review series. EMBO Rep. 9:969–76
     [Google Scholar]
  109. 109. 
    Rispail N, Di Pietro A. 2010. The two-component histidine kinase Fhk1 controls stress adaptation and virulence of Fusarium oxysporum. Mol. Plant Pathol. 11:395–407
     [Google Scholar]
  110. 110. 
    Rittenour WR, Harris SD. 2013. Glycosylphosphatidylinositol-anchored proteins in Fusarium graminearum: inventory, variability, and virulence. PLOS ONE 8:e81603
     [Google Scholar]
  111. 111. 
    Roesler SM, Kramer K, Finkemeier I, Humpf H-U, Tudzynski B. 2016. The SAGA complex in the rice pathogen Fusarium fujikuroi: structure and functional characterization. Mol. Microbiol. 102:951–74
     [Google Scholar]
  112. 112. 
    Ryder LS, Dagdas YF, Kershaw MJ, Venkataraman C, Madzvamuse A et al. 2019. A sensor kinase controls turgor-driven plant infection by the rice blast fungus. Nature 574:423–27
     [Google Scholar]
  113. 113. 
    Sakulkoo W, Oses-Ruiz M, Garcia EO, Soanes DM, Littlejohn GR et al. 2018. A single fungal MAP kinase controls plant cell-to-cell invasion by the rice blast fungus. Science 359:1399–403
     [Google Scholar]
  114. 114. 
    Santiago-Tirado FH, Peng T, Yang M, Hang HC, Doering TL. 2015. A single protein S-acyl transferase acts through diverse substrates to determine cryptococcal morphology, stress tolerance, and pathogenic outcome. PLOS Pathog. 11:e1004908
     [Google Scholar]
  115. 115. 
    Schirawski J, Bohnert HU, Steinberg G, Snetselaar K, Adamikowa L, Kahmann R. 2005. Endoplasmic reticulum glucosidase II is required for pathogenicity of Ustilago maydis. Plant Cell 17:3532–43
     [Google Scholar]
  116. 116. 
    Schotanus K, Soyer JL, Connolly LR, Grandaubert J, Happel P et al. 2015. Histone modifications rather than the novel regional centromeres of Zymoseptoria tritici distinguish core and accessory chromosomes. Epigenet. Chromatin 8:41
     [Google Scholar]
  117. 117. 
    Schulz BL, Jen FEC, Power PM, Jones CE, Fox KL et al. 2013. Identification of bacterial protein O-oligosaccharyltransferases and their glycoprotein substrates. PLOS ONE 8:e62768
     [Google Scholar]
  118. 118. 
    Schumacher J, Studt L, Tudzynski P. 2019. The putative H3K36 demethylase BcKDM1 affects virulence, stress responses and photomorphogenesis in Botrytis cinerea. Fungal Genet. Biol. 123:14–24
     [Google Scholar]
  119. 119. 
    Shi H-B, Chen G-Q, Chen Y-P, Dong B, Lu J-P et al. 2016. MoRad6-mediated ubiquitination pathways are essential for development and pathogenicity in Magnaporthe oryzae. Environ. Microbiol. 18:4170–87
     [Google Scholar]
  120. 120. 
    Shi H-B, Chen N, Zhu X-M, Liang S, Li L et al. 2019. F-box proteins MoFwd1, MoCdc4 and MoFbx15 regulate development and pathogenicity in the rice blast fungus Magnaporthe oryzae. Environ. Microbiol. 21:3027–45
     [Google Scholar]
  121. 121. 
    Skaar JR, Pagan JK, Pagano M. 2013. Mechanisms and function of substrate recruitment by F-box proteins. Nat. Rev. Mol. Cell Biol. 14:369–81
     [Google Scholar]
  122. 122. 
    Song F, Geng Q, Wang X, Gao X, He X et al. 2020. Gas chromatography-mass spectrometry profiling of volatile compounds reveals metabolic changes in a non-aflatoxigenic Aspergillus flavus induced by 5-azacytidine. Toxins 12:57
     [Google Scholar]
  123. 123. 
    Studt L, Janevska S, Arndt B, Boedi S, Sulyok M et al. 2017. Lack of the COMPASS component Ccl1 reduces H3K4 trimethylation levels and affects transcription of secondary metabolite genes in two plant-pathogenic Fusarium species. Front. Microbiol. 7:2144
     [Google Scholar]
  124. 124. 
    Studt L, Schmidt FJ, Jahn L, Sieber CMK, Connolly LR et al. 2013. Two histone deacetylases, FfHda1 and FfHda2, are important for Fusarium fujikuroi secondary metabolism and virulence. Appl. Environ. Microbiol. 79:7719–34
     [Google Scholar]
  125. 125. 
    Sun S, Deng Y, Cai E, Yang M, Li L et al. 2019. The farnesyltransferase β-subunit Ram1 regulates Sporisorium scitamineum mating. pathogenicity and cell wall integrity. Front. Microbiol. 10:976
     [Google Scholar]
  126. 126. 
    Sun X, Li Z, Liu H, Yang J, Liang W et al. 2017. Large-scale identification of lysine acetylated proteins in vegetative hyphae of the rice blast fungus. Sci. Rep. 7:15316
     [Google Scholar]
  127. 127. 
    Taguchi F, Takeuchi K, Katoh E, Murata K, Suzuki T et al. 2006. Identification of glycosylation genes and glycosylated amino acids of flagellin in Pseudomonas syringae pv. tabaci. Cell Microbiol. 8:923–38
     [Google Scholar]
  128. 128. 
    Takeuchi K, Ono H, Yoshida M, Ishii T, Katoh E et al. 2007. Flagellin glycans from two pathovars of Pseudomonas syringae contain rhamnose in D and L configurations in different ratios and modified 4-amino-4,6-dideoxyglucose. J. Bacteriol. 189:6945–56
     [Google Scholar]
  129. 129. 
    Takeuchi K, Taguchi F, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y. 2003. Flagellin glycosylation island in Pseudomonas sytingae pv. glycinea and its role in host specificity. J. Bacteriol. 185:6658–65
     [Google Scholar]
  130. 130. 
    Torreblanca J, Stumpferl S, Basse CW. 2003. Histone deacetylase Hda1 acts as repressor of the Ustilago maydis biotrophic marker gene mig1. Fungal Genet. Biol. 38:22–32
     [Google Scholar]
  131. 131. 
    Turrà D, Segorbe D, Pietro AD. 2014. Protein kinases in plant-pathogenic fungi: conserved regulators of infection. Annu. Rev. Phytopathol. 52:267–88
     [Google Scholar]
  132. 132. 
    van der Veen AG, Ploegh HL. 2012. Ubiquitin-like proteins. Annu. Rev. Biochem. 81:323–57
     [Google Scholar]
  133. 133. 
    Viaud M, Fillinger S, Liu W, Polepalli JS, Le Pecheur P et al. 2006. A class III histidine kinase acts as a novel virulence factor in Botrytis cinerea. Mol. Plant-Microbe Interact. 19:1042–50
     [Google Scholar]
  134. 134. 
    Vu Van L, Rossius M, Antelmann H. 2015. Redox regulation by reversible protein S-thiolation in bacteria. Front. Microbiol. 6:187
     [Google Scholar]
  135. 135. 
    Wang B, Wu G, Li K, Ling J, Zhao Y, Liu F. 2020. A glycoside hydrolase family 99-like domain-containing protein modifies outer membrane proteins to maintain Xanthomonas pathogenicity and viability in stressful environments. Phytopathology. https://doi.org/10.1094/PHYTO-08-20-0327-R
    [Crossref] [Google Scholar]
  136. 136. 
    Wang C, Zhang S, Hou R, Zhao Z, Zheng Q et al. 2011. Functional analysis of the kinome of the wheat scab fungus Fusarium graminearum. PLOS Pathog. 7:e1002460
     [Google Scholar]
  137. 137. 
    Wang D, Korban SS, Zhao Y. 2009. The Rcs phosphorelay system is essential for pathogenicity in Erwinia amylovora. Mol. Plant Pathol. 10:277–90
     [Google Scholar]
  138. 138. 
    Wang F-F, Cheng S-T, Wu Y, Ren B-Z, Qian W. 2017. A bacterial receptor PcrK senses the plant hormone cytokinin to promote adaptation to oxidative stress. Cell Rep. 21:2940–51
     [Google Scholar]
  139. 139. 
    Wang L, Cei X, Xing J, Liu C, Hendy A, Chen X-L. 2019. URM1-mediated ubiquitin-like modification is required for oxidative stress adaptation during infection of the rice blast fungus. Front. Microbiol. 10:2039
     [Google Scholar]
  140. 140. 
    Wang R-J, Peng J, Li QX, Peng Y-L. 2017. Phosphorylation-mediated regulatory networks in mycelia of Pyricularia oryzae revealed by phosphoproteomic analyses. Mol. Cell. Proteom. 16:1669–82
     [Google Scholar]
  141. 141. 
    Wei ZM, Kim JF, Beer SV. 2000. Regulation of hrp genes and type III protein secretion in Erwinia amylovora by HrpX/HrpY, a novel two-component system, and HrpS. Mol. Plant-Microbe Interact. 13:1251–62
     [Google Scholar]
  142. 142. 
    Wiehle L, Breiling A 2016. Chromatin immunoprecipitation. Polycomb Group Proteins: Methods and Protocols C Lanzuolo, B Bodega 7–21 New York: Springer
     [Google Scholar]
  143. 143. 
    Wiemann P, Sieber CMK, Von Bargen KW, Studt L, Niehaus E-M et al. 2013. Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. PLOS Pathog. 9:e1003475
     [Google Scholar]
  144. 144. 
    Wu X, Vellaichamy A, Wang D, Zamdborg L, Kelleher NL et al. 2013. Differential lysine acetylation profiles of Erwinia amylovora strains revealed by proteomics. J. Proteom. 79:60–71
     [Google Scholar]
  145. 145. 
    Xu JR, Hamer JE. 1996. MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev. 10:2696–706
     [Google Scholar]
  146. 146. 
    Xu JR, Staiger CJ, Hamer JE 1998. Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. PNAS 95:12713–18
     [Google Scholar]
  147. 147. 
    Xu Y, Zhou H, Zhao G, Yang J, Luo Y et al. 2020. Genetical and O-glycoproteomic analyses reveal the roles of three protein O-mannosyltransferases in phytopathogen Fusarium oxysporum f.sp. cucumerinum. Fungal Genet. Biol. 134:103285
     [Google Scholar]
  148. 148. 
    Yang K, Zhuang Z, Zhang F, Song F, Zhong H et al. 2015. Inhibition of aflatoxin metabolism and growth of Aspergillus flavus in liquid culture by a DNA methylation inhibitor. Food Addit. Contam. Part A 32:554–63
     [Google Scholar]
  149. 149. 
    Yi M, Park J-H, Ahn J-H, Lee Y-H. 2008. MoSNF1 regulates sporulation and pathogenicity in the rice blast fungus Magnaporthe oryzae. Fungal Genet. Biol. 45:1172–81
     [Google Scholar]
  150. 150. 
    Yin Z, Chen C, Yang J, Feng W, Liu X et al. 2019. Histone acetyltransferase MoHat1 acetylates autophagy-related proteins MoAtg3 and MoAtg9 to orchestrate functional appressorium formation and pathogenicity in Magnaporthe oryzae. Autophagy 15:1234–57
     [Google Scholar]
  151. 151. 
    Yun Y, Liu Z, Yin Y, Jiang J, Chen Y et al. 2015. Functional analysis of the Fusarium graminearum phosphatome. New Phytol. 207:119–34
     [Google Scholar]
  152. 152. 
    Zhang FL, Casey PJ. 1996. Protein prenylation. molecular mechanisms and functional consequences. Annu. Rev. Biochem. 65:241–69
     [Google Scholar]
  153. 153. 
    Zhang S, Liang M, Naqvi NI, Lin C, Qian W et al. 2017. Phototrophy and starvation-based induction of autophagy upon removal of Gcn5-catalyzed acetylation of Atg7 in Magnaporthe oryzae. Autophagy 13:1318–30
     [Google Scholar]
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Emerging Roles of Posttranslational Modifications in Plant-Pathogenic Fungi and Bacteria
Annual Review of Phytopathology 59, 99 (2021); https://doi.org/10.1146/annurev-phyto-021320-010948
/content/journals/10.1146/annurev-phyto-021320-010948
/content/journals/10.1146/annurev-phyto-021320-010948
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