Skip to main content
SpringerLink
Log in

The Biology of Invasive Growth by the Rice Blast Fungus Magnaporthe oryzae

  • Protocol
  • First Online:
Magnaporthe oryzae

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2356))

Abstract

This introductory chapter describes the life cycle of Magnaporthe oryzae, the causal agent of rice blast disease. During plant infection, M. oryzae forms a specialized infection structure called an appressorium, which generates enormous turgor, applied as a mechanical force to breach the rice cuticle. Appressoria form in response to physical cues from the hydrophobic rice leaf cuticle and nutrient availability. The signaling pathways involved in perception of surface signals are described and the mechanism by which appressoria function is also introduced. Re-polarization of the appressorium requires a septin complex to organize a toroidal F-actin network at the base of the cell. Septin aggregation requires a turgor-dependent sensor kinase, Sln1, necessary for re-polarization of the appressorium and development of a rigid penetration hypha to rupture the leaf cuticle. Once inside the plant, the fungus undergoes secretion of a large set of effector proteins, many of which are directed into plant cells using a specific secretory pathway. Here they suppress plant immunity, but can also be perceived by rice immune receptors, triggering resistances. M. oryzae then manipulates pit field sites, containing plasmodesmata, to facilitate rapid spread from cell to cell in plant tissue, leading to disease symptom development.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Wilson RA, Talbot NJ (2009) Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat Rev Microbiol 7:185–195

    Article  CAS  PubMed  Google Scholar 

  2. Hamer JE, Howard RJ, Chumley FG, Valent B (1988) A mechanism for surface attachment in spores of a plant pathogenic fungus. Science 239:288

    Article  CAS  PubMed  Google Scholar 

  3. Bourett TM, Howard RJ (1990) In vitro development of penetration structures in the rice blast fungus Magnaporthe grisea. Can J Bot 68:329–342

    Article  Google Scholar 

  4. Kershaw MJ, Talbot NJ (2009) Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease. Proc Natl Acad Sci U S A 106:15967–15972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. de Jong JC, McCormack BJ, Smirnoff N, Talbot NJ (1997) Glycerol generates turgor in rice blast. Nature 389:244–244

    Article  CAS  Google Scholar 

  6. Foster AJ, Ryder LS, Kershaw MJ, Talbot NJ (2017) The role of glycerol in the pathogenic lifestyle of the rice blast fungus Magnaporthe oryzae. Environ Microbiol 19(3):1008–1016

    Article  PubMed  Google Scholar 

  7. Mentlak TA, Kombrink A, Shinya T, Ryder LS, Otomo I, Saitoh H, Terauchi R, Nishizawa Y, Shibuya N, Thomma BP, Talbot NJ (2012) Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 24:322–335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Yan X, Talbot NJ (2016) Investigating the cell biology of plant infection by the rice blast fungus Magnaporthe oryzae. Curr Opin Microbiol 34:147–153

    Article  CAS  PubMed  Google Scholar 

  9. 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 90:61–68

    Article  CAS  PubMed  Google Scholar 

  10. Talbot NJ (2003) On the trail of a cereal killer: exploring the biology of Magnaporthe grisea. Ann Rev Microbiol 57:177–202

    Article  CAS  Google Scholar 

  11. Wang X, Valent B (2009) Advances in genetics, genomics and control of rice blast disease. Springer Science & Business Media, Berlin/Heidelberg

    Book  Google Scholar 

  12. Liu W, Zhou X, Li G, Li L, Kong L, Wang C, Zhang H, Xu J-R (2011) Multiple plant surface signals are sensed by different mechanisms in the rice blast fungus for appressorium formation. PLoS Pathog 7:e1001261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Talbot NJ, Ebbole DJ, Hamer JE (1993) Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5:1575–1590

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Pham CL, Rey A, Lo V, Soules M, Ren Q, Meisl G, Knowles TP, Kwan AH, Sunde M (2016) Self-assembly of MPG1, a hydrophobin protein from the rice blast fungus that forms functional amyloid coatings, occurs by a surface-driven mechanism. Sci Rep 6:25288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kulkarni RD, Thon MR, Pan H, Dean RA (2005) Novel G-protein-coupled receptor-like proteins in the plant pathogenic fungus Magnaporthe grisea. Genome Biol 6:R24

    Article  PubMed  PubMed Central  Google Scholar 

  16. DeZwaan TM, Carroll AM, Valent B, Sweigard JA (1999) Magnaporthe grisea pth11p is a novel plasma membrane protein that mediates appressorium differentiation in response to inductive substrate cues. Plant Cell 11:2013–2030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Liu S, Dean RA (1997) G protein α subunit genes control growth, development, and pathogenicity of Magnaporthe grisea. Mol Plant-Microbe Interact 10:1075–1086

    Article  CAS  PubMed  Google Scholar 

  18. Liu H, Suresh A, Willard FS, Siderovski DP, Lu S, Naqvi NI (2007) Rgs1 regulates multiple Gα subunits in Magnaporthe pathogenesis, asexual growth and thigmotropism. EMBO J 26:690–700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Fang EG, Dean RA (2000) Site-directed mutagenesis of the magB gene affects growth and development in Magnaporthe grisea. Mol Plant-Microbe Interact 13:1214–1227

    Article  CAS  PubMed  Google Scholar 

  20. Ramanujam R, Yishi X, Liu H, Naqvi NI (2012) Structure-function analysis of Rgs1 in Magnaporthe oryzae: role of DEP domains in subcellular targeting. PLoS One 7:e41084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Bölker M (1998) Sex and crime: heterotrimeric G proteins in fungal mating and pathogenesis. Fungal Genet Biol 25:143–156

    Article  PubMed  Google Scholar 

  22. Kang SH, Khang CH, Lee Y-H (1999) Regulation of cAMP-dependent protein kinase during appressorium formation in Magnaporthe grisea. FEMS Microbiol Lett 170:419–423

    Article  CAS  Google Scholar 

  23. Xu J-R, Hamer JE (1996) MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev 10:2696–2706

    Article  CAS  PubMed  Google Scholar 

  24. Adachi K, Hamer JE (1998) Divergent cAMP signaling pathways regulate growth and pathogenesis in the rice blast fungus Magnaporthe grisea. Plant Cell 10:1361–1373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, Thon M, Kulkarni R, Xu J-R, Pan H, Read ND, Lee Y-H, Carbone I, Brown D, Oh YY, Donofrio N, Jeong JS, Soanes DM, Djonovic S, Kolomiets E, Rehmeyer C, Li W, Harding M, Kim S, Lebrun M-H, Bohnert H, Coughlan S, Butler J, Calvo S, Ma L-J, Nicol R, Purcell S, Nusbaum C, Galagan JE, Birren BW (2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434:980–986

    Article  CAS  PubMed  Google Scholar 

  26. Choi W, Dean RA (1997) The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 9:1973–1983

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Gilbert RD, Johnson AM, Dean RA (1996) Chemical signals responsible for appressorium formation in the rice blast fungus Magnaporthe grisea. Physiol Mol Plant Pathol 48:335–346

    Article  CAS  Google Scholar 

  28. Douglas LM, Alvarez FJ, McCreary C, Konopka JB (2005) Septin function in yeast model systems and pathogenic fungi. Eukaryot Cell 4:1503–1512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430

    Article  PubMed  PubMed Central  Google Scholar 

  30. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Wilson RA, Gibson RP, Quispe CF, Littlechild JA, Talbot NJ (2010) An NADPH-dependent genetic switch regulates plant infection by the rice blast fungus. Proc Natl Acad Sci U S A 107:21902–21907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Fernandez J, Wright JD, Hartline D, Quispe CF, Madayiputhiya N, Wilson RA (2012) Principles of carbon catabolite repression in the rice blast fungus: Tps1, Nmr1-3, and a MATE-family pump regulate glucose metabolism during infection. PLoS Genet 8:e1002673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Jiang C, Zhang X, Liu H, Xu J-R (2018) Mitogen-activated protein kinase signaling in plant pathogenic fungi. PLoS Pathog 14:e1006875

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Turrà D, Segorbe D, Di Pietro A (2014) Protein kinases in plant-pathogenic fungi: conserved regulators of infection. Annu Rev Phytopathol 52:267–288

    Article  PubMed  CAS  Google Scholar 

  35. Sakulkoo W, Osés-Ruiz M, Oliveira Garcia E, Soanes DM, Littlejohn GR, Hacker C, Correia A, Valent B, Talbot NJ (2018) A single fungal MAP kinase controls plant cell-to-cell invasion by the rice blast fungus. Science 359:1399–1403

    Article  CAS  PubMed  Google Scholar 

  36. Bruno KS, Tenjo F, Li L, Hamer JE, Xu JR (2004) Cellular localization and role of kinase activity of PMK1 in Magnaporthe grisea. Eukaryot Cell 3:1525–1532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Zhao X, Kim Y, Park G, Xu J-R (2005) A mitogen-activated protein kinase Cascade regulating infection-related morphogenesis in Magnaporthe grisea. Plant Cell Online 17:1317–1329

    Article  CAS  Google Scholar 

  38. Li G, Zhou X, Xu J-R (2012) Genetic control of infection-related development in Magnaporthe oryzae. Curr Opin Microbiol 15:678–684

    Article  CAS  PubMed  Google Scholar 

  39. Zhao X, Xu J-R (2007) A highly conserved MAPK-docking site in Mst7 is essential for Pmk1 activation in Magnaporthe grisea. Mol Microbiol 63:881–894

    Article  CAS  PubMed  Google Scholar 

  40. Zhang S, Jiang C, Zhang Q, Qi L, Li C, Xu J-R (2016) Thioredoxins are involved in the activation of the PMK1 MAP kinase pathway during appressorium penetration and invasive growth in Magnaporthe oryzae. Environ Microbiol 18:3768–3784

    Article  CAS  PubMed  Google Scholar 

  41. Qi L, Kim Y, Jiang C, Li Y, Peng Y, Xu J-R (2015) Activation of Mst11 and feedback inhibition of germ tube growth in Magnaporthe oryzae. Mol Plant-Microbe Interact 28:881–891

    Article  CAS  PubMed  Google Scholar 

  42. Zhou X, Zhao X, Xue C, Dai Y, Xu J-R (2014) Bypassing both surface attachment and surface recognition requirements for Appressorium formation by overactive Ras signaling in Magnaporthe oryzae. Mol Plant-Microbe Interact 27:996–1004

    Article  CAS  PubMed  Google Scholar 

  43. Li G, Zhang X, Tian H, Choi Y-E, Tao WA, Xu J-R (2017) MST50 is involved in multiple MAP kinase signaling pathways in Magnaporthe oryzae. Environ Microbiol 19:1959–1974

    Article  CAS  PubMed  Google Scholar 

  44. Park G, Xue C, Zhao X, Kim Y, Orbach M, Xu JR (2006) Multiple upstream signals converge on the adaptor protein Mst50 in Magnaporthe grisea. Plant Cell 18:2822–2835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Nishimura M, Park G, Xu J-R (2003) The G-beta subunit MGB1 is involved in regulating multiple steps of infection-related morphogenesis in Magnaporthe grisea. Mol Microbiol 50:231–243

    Article  CAS  PubMed  Google Scholar 

  46. Kou Y, Tan YH, Ramanujam R, Naqvi NI (2017) Structure-function analyses of the Pth11 receptor reveal an important role for CFEM motif and redox regulation in rice blast. New Phytol 214:330–342

    Article  CAS  PubMed  Google Scholar 

  47. Ryder LS, Talbot NJ (2015) Regulation of appressorium development in pathogenic fungi. Curr Opin Plant Biol 26:8–13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Zhang H, Xue C, Kong L, Li G, Xu J-R (2011) A Pmk1-interacting gene is involved in appressorium differentiation and plant infection in Magnaporthe oryzae. Eukaryot Cell 10:1062–1070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Kim S, Park SY, Kim KS, Rho HS, Chi MH, Choi J, Park J, Kong S, Park J, Goh J, Lee YH (2009) Homeobox transcription factors are required for conidiation and appressorium development in the rice blast fungus Magnaporthe oryzae. PLoS Genet 5:e1000757

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Yue X, Que Y, Xu L, Deng S, Peng Y, Talbot NJ, Wang Z (2016) ZNF1 encodes a putative C2H2 zinc-finger protein essential for appressorium differentiation by the Rice blast fungus Magnaporthe oryzae. Mol Plant-Microbe Interact 29:22–35

    Article  CAS  PubMed  Google Scholar 

  51. Soanes DM, Chakrabarti A, Paszkiewicz KH, Dawe AL, Talbot NJ (2012) Genome-wide transcriptional profiling of appressorium development by the Rice blast fungus Magnaporthe oryzae. PLoS Pathog 8:e1002514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Saunders DG, Aves SJ, Talbot NJ (2010) Cell cycle-mediated regulation of plant infection by the rice blast fungus. Plant Cell 22:497–507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Oses-Ruiz M, Talbot NJ (2017) Cell cycle-dependent regulation of plant infection by the rice blast fungus Magnaporthe oryzae. Commun Integr Biol 10:e1372067

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Oses-Ruiz M, Sakulkoo W, Littlejohn GR, Martin-Urdiroz M, Talbot NJ (2017) Two independent S-phase checkpoints regulate appressorium-mediated plant infection by the rice blast fungus Magnaporthe oryzae. Proc Natl Acad Sci U S A 114:E237–E244

    Article  CAS  PubMed  Google Scholar 

  55. Saunders DG, Dagdas YF, Talbot NJ (2010) Spatial uncoupling of mitosis and cytokinesis during appressorium-mediated plant infection by the rice blast fungus Magnaporthe oryzae. Plant Cell 22:2417–2428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Osmani AH, O'Donnell K, Pu RT, Osmani SA (1991) Activation of the nimA protein kinase plays a unique role during mitosis that cannot be bypassed by absence of the bimE checkpoint. EMBO J 10:2669–2679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Rhind N, Russell P (1998) Mitotic DNA damage and replication checkpoints in yeast. Curr Opin Cell Biol 10:749–758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Veneault-Fourrey C, Barooah M, Egan M, Wakley G, Talbot NJ (2006) Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science 312:580–583

    Article  CAS  PubMed  Google Scholar 

  59. Liu XH, Lu JP, Zhang L, Dong B, Min H, Lin FC (2007) Involvement of a Magnaporthe grisea serine/threonine kinase gene, MgATG1, in appressorium turgor and pathogenesis. Eukaryot Cell 6:997–1005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Shen Q, Liang M, Yang F, Deng YZ, Naqvi NI (2020) Ferroptosis contributes to developmental cell death in rice blast. New Phytol 227(6):1831–1846

    Article  CAS  PubMed  Google Scholar 

  61. Armentrout V, Downer A (1987) Infection cushion development by Rhizoctonia solani on cotton. Phytopathology 77:619–623

    Article  Google Scholar 

  62. Mendgen K, Hahn M, Deising H (1996) Morphogenesis and mechanisms of penetration by plant pathogenic fungi. Annu Rev Phytopathol 34:367–386

    Article  CAS  PubMed  Google Scholar 

  63. Talbot NJ (2019) Appressoria. Curr Biol 29:R144–r146

    Article  CAS  PubMed  Google Scholar 

  64. Skamnioti P, Gurr SJ (2007) Magnaporthe grisea Cutinase2 mediates appressorium differentiation and host penetration and is required for full virulence. Plant Cell 19:2674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Chang HX, Miller LA, Hartman GL (2014) Melanin-independent accumulation of turgor pressure in appressoria of Phakopsora pachyrhizi. Phytopathology 104:977–984

    Article  PubMed  Google Scholar 

  66. Loehrer M, Botterweck J, Jahnke J, Mahlmann DM, Gaetgens J, Oldiges M, Horbach R, Deising H, Schaffrath U (2014) In vivo assessment by Mach–Zehnder double-beam interferometry of the invasive force exerted by the Asian soybean rust fungus (Phakopsora pachyrhizi). New Phytol 203:620–631

    Article  CAS  PubMed  Google Scholar 

  67. Ludwig N, Löhrer M, Hempel M, Mathea S, Schliebner I, Menzel M, Kiesow A, Schaffrath U, Deising HB, Horbach R (2013) Melanin is not required for turgor generation but enhances cell-wall rigidity in appressoria of the corn pathogen Colletotrichum graminicola. Mol Plant-Microbe Interact 27:315–327

    Article  Google Scholar 

  68. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Ryder LS, Dagdas YF, Kershaw MJ, Venkataraman C, Madzvamuse A, Yan X, Cruz-Mireles N, Soanes DM, Oses-Ruiz M, Styles V, Sklenar J, Menke FLH, Talbot NJ (2019) A sensor kinase controls turgor-driven plant infection by the rice blast fungus. Nature 574:423–427

    Article  CAS  PubMed  Google Scholar 

  70. Tao W, Deschenes RJ, Fassler JS (1999) Intracellular glycerol levels modulate the activity of Sln1p, a Saccharomyces cerevisiae two-component regulator. J Biol Chem 274:360–367

    Article  CAS  PubMed  Google Scholar 

  71. Zhang H, Liu K, Zhang X, Song W, Zhao Q, Dong Y, Guo M, Zheng X, Zhang Z (2010) A two-component histidine kinase, MoSLN1, is required for cell wall integrity and pathogenicity of the rice blast fungus, Magnaporthe oryzae. Curr Genet 56(6):517–528

    Article  CAS  PubMed  Google Scholar 

  72. Ryder LS, Dagdas YF, Mentlak TA, Kershaw MJ, Thornton CR, Schuster M, Chen J, Wang Z, Talbot NJ (2013) NADPH oxidases regulate septin-mediated cytoskeletal remodeling during plant infection by the rice blast fungus. Proc Natl Acad Sci 110:3179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Dagdas YF, Yoshino K, Dagdas G, Ryder LS, Bielska E, Steinberg G, Talbot NJ (2012) Septin-mediated plant cell invasion by the rice blast fungus, Magnaporthe oryzae. Science 336:1590–1595

    Article  CAS  PubMed  Google Scholar 

  74. Bourett TM, Howard RJ (1992) Actin in penetration pegs of the fungal rice blast pathogen, Magnaporthe grisea. Protoplasma 168:20–26

    Article  CAS  Google Scholar 

  75. Delgado-Álvarez DL, Callejas-Negrete OA, Gomez N, Freitag M, Roberson RW, Smith LG, Mouriño-Pérez RR (2010) Visualization of F-actin localization and dynamics with live cell markers in Neurospora crassa. Fungal Genet Biol 47:573–586

    Article  PubMed  CAS  Google Scholar 

  76. Delgado-Álvarez DL, Bartnicki-García S, Seiler S, Mouriño-Pérez RR (2014) Septum development in Neurospora crassa: the septal actomyosin tangle. PLoS One 9:e96744

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Upadhyay S, Shaw BD (2008) The role of actin, fimbrin and endocytosis in growth of hyphae in aspergillus nidulans. Mol Microbiol 68:690–705

    Article  CAS  PubMed  Google Scholar 

  78. Berepiki A, Lichius A, Shoji JY, Tilsner J, Read ND (2010) F-actin dynamics in Neurospora crassa. Eukaryot Cell 9:547–557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Roberson RW (1992) The actin cytoskeleton in hyphal cells of Sclerotium rolfsii. Mycologia 84:41–51

    Article  CAS  Google Scholar 

  80. Taheri-Talesh N, Horio T, Araujo-Bazán L, Dou X, Espeso EA, Peñalva MA, Osmani SA, Oakley BR (2008) The tip growth apparatus of aspergillus nidulans. Mol Biol Cell 19:1439–1449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Berepiki A, Lichius A, Read ND (2011) Actin organization and dynamics in filamentous fungi. Nat Rev Microbiol 9:876–887

    Article  CAS  PubMed  Google Scholar 

  82. Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, Bista M, Bradke F, Jenne D, Holak TA, Werb Z, Sixt M, Wedlich-Soldner R (2008) Lifeact: a versatile marker to visualize F-actin. Nat Methods 5:605–607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Gilden J, Krummel MF (2010) Control of cortical rigidity by the cytoskeleton: emerging roles for septins. Cytoskeleton (Hoboken) 67:477–486. https://doi.org/10.1002/cm.20461

    Article  CAS  Google Scholar 

  84. Van Ngo H, Mostowy S (2019) Role of septins in microbial infection. J Cell Sci 132:jcs226266. https://journals.biologists.com/jcs/article/132/9/jcs226266/57414/Role-of-septins-in-microbial-infection

  85. Hartwell LH (1971) Genetic control of the cell division cycle in yeast IV. Genes controlling bud emergence and cytokinesis. Exp Cell Res 69:265–276

    Article  CAS  PubMed  Google Scholar 

  86. Spiliotis ET, Nelson WJ (2006) Here come the septins: novel polymers that coordinate intracellular functions and organization. J Cell Sci 119:4–10

    Article  CAS  PubMed  Google Scholar 

  87. Tosa Y, Osue J, Eto Y, Oh H-S, Nakayashiki H, Mayama S, Leong SA (2005) Evolution of an Avirulence gene, AVR1-CO39, concomitant with the evolution and differentiation of Magnaporthe oryzae. Mol Plant-Microbe Interact 18:1148–1160

    Article  CAS  PubMed  Google Scholar 

  88. Sirajuddin M, Farkasovsky M, Zent E, Wittinghofer A (2009) GTP-induced conformational changes in septins and implications for function. Proc Natl Acad Sci U S A 106:16592–16597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Versele M, Thorner J (2004) Septin collar formation in budding yeast requires GTP binding and direct phosphorylation by the PAK, Cla4. J Cell Biol 164:701–715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Sirajuddin M, Farkasovsky M, Hauer F, Kuhlmann D, Macara IG, Weyand M, Stark H, Wittinghofer A (2007) Structural insight into filament formation by mammalian septins. Nature 449:311–315

    Article  CAS  PubMed  Google Scholar 

  91. Dulal N, Rogers A, Wang Y, Egan M (2020) Dynamic assembly of a higher-order septin structure during appressorium morphogenesis by the rice blast fungus. Fungal Genet Biol 140:103385

    Article  CAS  PubMed  Google Scholar 

  92. Galhano R, Illana A, Ryder LS, Rodriguez-Romero J, Demuez M, Badaruddin M, Martinez-Rocha AL, Soanes DM, Studholme DJ, Talbot NJ, Sesma A (2017) Tpc1 is an important Zn(II)2Cys6 transcriptional regulator required for polarized growth and virulence in the rice blast fungus. PLoS Pathog 13:e1006516

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Kershaw MJ, Basiewicz M, Soanes DM, Yan X, Ryder LS, Csukai M, Oses-Ruiz M, Valent B, Talbot NJ (2019) Conidial morphogenesis and Septin-mediated plant infection require Smo1, a Ras GTPase-activating protein in Magnaporthe oryzae. Genetics 211:151–167

    Article  CAS  PubMed  Google Scholar 

  94. 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. Proc Natl Acad Sci U S A 95:12713–12718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Park G, Xue C, Zheng L, Lam S, Xu JR (2002) MST12 regulates infectious growth but not appressorium formation in the rice blast fungus Magnaporthe grisea. Mol Plant-Microbe Interact 15:183–192

    Article  CAS  PubMed  Google Scholar 

  96. Liu C, Li Z, Xing J, Yang J, Wang Z, Zhang H, Chen D, Peng YL, Chen XL (2018) Global analysis of sumoylation function reveals novel insights into development and appressorium-mediated infection of the rice blast fungus. New Phytol 219:1031–1047

    Article  CAS  PubMed  Google Scholar 

  97. Gupta YK, Dagdas YF, Martinez-Rocha A-L, Kershaw MJ, Littlejohn GR, Ryder LS, Sklenar J, Menke F, Talbot NJ (2015) Septin-dependent assembly of the exocyst is essential for plant infection by Magnaporthe oryzae. Plant Cell 27:3277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Armijo G, Schlechter R, Agurto M, Muñoz D, Nuñez C, Arce-Johnson P (2016) Grapevine pathogenic microorganisms: understanding infection strategies and host response scenarios. Front Plant Sci 7:382

    Article  PubMed  PubMed Central  Google Scholar 

  99. Fernandez J, Orth K (2018) Rise of a cereal killer: the biology of Magnaporthe oryzae biotrophic growth. Trends Microbiol 26:582–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Yi M, Valent B (2013) Communication between filamentous pathogens and plants at the biotrophic interface. Annu Rev Phytopathol 51:587–611

    Article  CAS  PubMed  Google Scholar 

  101. Kankanala P, Czymmek K, Valent B (2007) Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. Plant Cell 19:706–724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Giraldo MC, Dagdas YF, Gupta YK, Mentlak TA, Yi M, Martinez-Rocha AL, Saitoh H, Terauchi R, Talbot NJ, Valent B (2013) Two distinct secretion systems facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae. Nat Commun 4:1996

    Article  PubMed  CAS  Google Scholar 

  103. Khang CH, Berruyer R, Giraldo MC, Kankanala P, Park SY, Czymmek K, Kang S, Valent B (2010) Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22:1388–1403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Mosquera G, Giraldo MC, Khang CH, Coughlan S, Valent B (2009) Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1-4 as biotrophy-associated secreted proteins in rice blast disease. Plant Cell 21:1273–1290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Patkar RN, Benke PI, Qu Z, Chen YY, Yang F, Swarup S, Naqvi NI (2015) A fungal monooxygenase-derived jasmonate attenuates host innate immunity. Nat Chem Biol 11:733–740

    Article  CAS  PubMed  Google Scholar 

  106. Marroquin-Guzman M, Hartline D, Wright JD, Elowsky C, Bourret TJ, Wilson RA (2017) The Magnaporthe oryzae nitrooxidative stress response suppresses rice innate immunity during blast disease. Nat Microbiol 2:17054

    Article  CAS  PubMed  Google Scholar 

  107. Valent B, Khang CH (2010) Recent advances in rice blast effector research. Curr Opin Plant Biol 13:434–441

    Article  CAS  PubMed  Google Scholar 

  108. Nishimura T, Mochizuki S, Ishii-Minami N, Fujisawa Y, Kawahara Y, Yoshida Y, Okada K, Ando S, Matsumura H, Terauchi R, Minami E, Nishizawa Y (2016) Magnaporthe oryzae glycine-rich secretion protein, Rbf1 critically participates in pathogenicity through the focal formation of the biotrophic interfacial complex. PLoS Pathog 12:e1005921

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  109. Fujikawa T, Kuga Y, Yano S, Yoshimi A, Tachiki T, Abe K, Nishimura M (2009) Dynamics of cell wall components of Magnaporthe grisea during infectious structure development. Mol Microbiol 73:553–570

    Article  CAS  PubMed  Google Scholar 

  110. Mehrabi R, Ding S, Xu J-R (2008) MADS-box transcription factor Mig1 is required for infectious growth in Magnaporthe grisea. Eukaryot Cell 7:791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Qi Z, Wang QI, Dou X, Wang WEI, Zhao Q, Lv R, Zhang H, Zheng X, Wang P, Zhang Z (2012) MoSwi6, an APSES family transcription factor, interacts with MoMps1 and is required for hyphal and conidial morphogenesis, appressorial function and pathogenicity of Magnaporthe oryzae. Mol Plant Pathol 13:677–689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Fernandez J, Wilson RA (2012) Why no feeding frenzy? Mechanisms of nutrient acquisition and utilization during infection by the rice blast fungus Magnaporthe oryzae. Mol Plant-Microbe Interact 25:1286–1293

    Article  CAS  PubMed  Google Scholar 

  113. Fernandez J, Marroquin-Guzman M, Wilson RA (2014) Mechanisms of nutrient acquisition and utilization during fungal infections of leaves. Annu Rev Phytopathol 52:155–174

    Article  CAS  PubMed  Google Scholar 

  114. Fernandez J, Marroquin-Guzman M, Wilson RA (2014) Evidence for a transketolase-mediated metabolic checkpoint governing biotrophic growth in rice cells by the blast fungus Magnaporthe oryzae. PLoS Pathog 10:e1004354

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  115. Sun G, Elowsky C, Li G, Wilson RA (2018) TOR-autophagy branch signaling via Imp1 dictates plant-microbe biotrophic interface longevity. PLoS Genet 14:e1007814

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  116. Molloy S (2010) Fungal biology: Magnaporthe effectors on the move. Nat Rev Microbiol 8:466–467

    Article  CAS  PubMed  Google Scholar 

  117. Kamoun S (2006) A catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev Phytopathol 44:41–60

    Article  CAS  PubMed  Google Scholar 

  118. Govers F, Bouwmeester K (2008) Effector trafficking: RXLR-dEER as extra gear for delivery into plant cells. Plant Cell 20:1728–1730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Saitoh H, Fujisawa S, Mitsuoka C, Ito A, Hirabuchi A, Ikeda K, Irieda H, Yoshino K, Yoshida K, Matsumura H, Tosa Y, Win J, Kamoun S, Takano Y, Terauchi R (2012) Large-scale gene disruption in Magnaporthe oryzae identifies MC69, a secreted protein required for infection by monocot and dicot fungal pathogens. PLoS Pathog 8:e1002711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Park SY, Choi J, Lim SE, Lee GW, Park J, Kim Y, Kong S, Kim SR, Rho HS, Jeon J, Chi MH, Kim S, Khang CH, Kang S, Lee YH (2013) Global expression profiling of transcription factor genes provides new insights into pathogenicity and stress responses in the rice blast fungus. PLoS Pathog 9:e1003350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. van der Hoorn RA, Kamoun S (2008) From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20:2009–2017

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  122. Hogenhout SA, Van der Hoorn RA, Terauchi R, Kamoun S (2009) Emerging concepts in effector biology of plant-associated organisms. Mol Plant-Microbe Interact 22:115–122

    Article  CAS  PubMed  Google Scholar 

  123. Birch PR, Rehmany AP, Pritchard L, Kamoun S, Beynon JL (2006) Trafficking arms: oomycete effectors enter host plant cells. Trends Microbiol 14:8–11

    Article  CAS  PubMed  Google Scholar 

  124. Win J, Chaparro-Garcia A, Belhaj K, Saunders DG, Yoshida K, Dong S, Schornack S, Zipfel C, Robatzek S, Hogenhout SA, Kamoun S (2012) Effector biology of plant-associated organisms: concepts and perspectives. Cold Spring Harb Symp Quant Biol 77:235–247

    Article  CAS  PubMed  Google Scholar 

  125. Bozkurt TO, Schornack S, Banfield MJ, Kamoun S (2012) Oomycetes, effectors, and all that jazz. Curr Opin Plant Biol 15:483–492

    Article  PubMed  Google Scholar 

  126. Xin X-F, Nomura K, Aung K, Velásquez AC, Yao J, Boutrot F, Chang JH, Zipfel C, He SY (2016) Bacteria establish an aqueous living space in plants crucial for virulence. Nature 539:524–529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Liu W, Liu J, Ning Y, Ding B, Wang X, Wang Z, Wang GL (2013) Recent progress in understanding PAMP- and effector-triggered immunity against the rice blast fungus Magnaporthe oryzae. Mol Plant 6:605–620. https://doi.org/10.1093/mp/sst015

    Article  CAS  PubMed  Google Scholar 

  128. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    Article  CAS  PubMed  Google Scholar 

  129. Banfield MJ (2015) Perturbation of host ubiquitin systems by plant pathogen/pest effector proteins. Cell Microbiol 17:18–25

    Article  CAS  PubMed  Google Scholar 

  130. Oliveira-Garcia E, Valent B (2015) How eukaryotic filamentous pathogens evade plant recognition. Curr Opin Microbiol 26:92–101

    Article  CAS  PubMed  Google Scholar 

  131. Azizi P, Rafii MY, Abdullah SN, Nejat N, Maziah M, Hanafi MM, Latif MA, Sahebi M (2016) Toward understanding of rice innate immunity against Magnaporthe oryzae. Crit Rev Biotechnol 36:165–174

    Article  CAS  PubMed  Google Scholar 

  132. Bentham A, Burdett H, Anderson PA, Williams SJ, Kobe B (2016) Animal NLRs provide structural insights into plant NLR function. Ann Bot 119(5):827–702

    Google Scholar 

  133. Stein JC, Yu Y, Copetti D, Zwickl DJ, Zhang L, Zhang C, Chougule K, Gao D, Iwata A, Goicoechea JL, Wei S, Wang J, Liao Y, Wang M, Jacquemin J, Becker C, Kudrna D, Zhang J, Londono CEM, Song X, Lee S, Sanchez P, Zuccolo A, Ammiraju JSS, Talag J, Danowitz A, Rivera LF, Gschwend AR, Noutsos C, Wu C-c, S-m K, J-w Z, F-j W, Zhao Q, Feng Q, El Baidouri M, Carpentier M-C, Lasserre E, Cooke R, da Rosa Farias D, da Maia LC, dos Santos RS, Nyberg KG, McNally KL, Mauleon R, Alexandrov N, Schmutz J, Flowers D, Fan C, Weigel D, Jena KK, Wicker T, Chen M, Han B, Henry R, Hsing Y-iC, Kurata N, de Oliveira AC, Panaud O, Jackson SA, Machado CA, Sanderson MJ, Long M, Ware D, Wing RA (2018) Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza. Nat Genet 50:285–296

    Article  CAS  PubMed  Google Scholar 

  134. Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B (2000) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19:4004–4014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Kanzaki H, Yoshida K, Saitoh H, Fujisaki K, Hirabuchi A, Alaux L, Fournier E, Tharreau D, Terauchi R (2012) Arms race co-evolution of Magnaporthe oryzae AVR-Pik and rice Pik genes driven by their physical interactions. Plant J 72:894–907

    Article  CAS  PubMed  Google Scholar 

  136. Yoshida K, Saitoh H, Fujisawa S, Kanzaki H, Matsumura H, Yoshida K, Tosa Y, Chuma I, Takano Y, Win J, Kamoun S, Terauchi R (2009) Association genetics reveals three novel avirulence genes from the Rice blast fungal pathogen Magnaporthe oryzae. Plant Cell 21:1573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Chuma I, Isobe C, Hotta Y, Ibaragi K, Futamata N, Kusaba M, Yoshida K, Terauchi R, Fujita Y, Nakayashiki H, Valent B, Tosa Y (2011) Multiple translocation of the AVR-Pita effector gene among chromosomes of the rice blast fungus Magnaporthe oryzae and related species. PLoS Pathog 7:e1002147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Zhang S, Wang L, Wu W, He L, Yang X, Pan Q (2015) Function and evolution of Magnaporthe oryzae avirulence gene AvrPib responding to the rice blast resistance gene Pib. Sci Rep 5:11642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Inoue Y, Vy TTP, Yoshida K, Asano H, Mitsuoka C, Asuke S, Anh VL, Cumagun CJR, Chuma I, Terauchi R, Kato K, Mitchell T, Valent B, Farman M, Tosa Y (2017) Evolution of the wheat blast fungus through functional losses in a host specificity determinant. Science 357:80

    Article  CAS  PubMed  Google Scholar 

  140. De Wit PJ, Mehrabi R, Van den Burg HA, Stergiopoulos I (2009) Fungal effector proteins: past, present and future. Mol Plant Pathol 10:735–747

    Article  PubMed  Google Scholar 

  141. Wang B-H, Ebbole DJ, Wang Z-h (2017) The arms race between Magnaporthe oryzae and rice: diversity and interaction of Avr and R genes. J Integr Agric 16:2746–2760

    Article  Google Scholar 

  142. Orbach MJ, Farrall L, Sweigard JA, Chumley FG, Valent B (2000) A telomeric avirulence gene determines efficacy for the rice blast resistance gene pi-ta. Plant Cell 12:2019–2032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Bohnert HU, Fudal I, Dioh W, Tharreau D, Notteghem JL, Lebrun MH (2004) A putative polyketide synthase/peptide synthetase from Magnaporthe grisea signals pathogen attack to resistant rice. Plant Cell 16:2499–2513

    Article  PubMed  PubMed Central  Google Scholar 

  144. Wolpert TJ, Dunkle LD, Ciuffetti LM (2002) Host-selective toxins and avirulence determinants: what's in a name? Annu Rev Phytopathol 40:251–285

    Article  CAS  PubMed  Google Scholar 

  145. Berruyer R, Adreit H, Milazzo J, Gaillard S, Berger A, Dioh W, Lebrun MH, Tharreau D (2003) Identification and fine mapping of Pi33, the rice resistance gene corresponding to the Magnaporthe grisea avirulence gene ACE1. Theor Appl Genet 107:1139–1147

    Article  CAS  PubMed  Google Scholar 

  146. Wu CH, Abd-El-Haliem A, Bozkurt TO, Belhaj K, Terauchi R, Vossen JH, Kamoun S (2017) NLR network mediates immunity to diverse plant pathogens. Proc Natl Acad Sci U S A 114:8113–8118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Cesari S, Kanzaki H, Fujiwara T, Bernoux M, Chalvon V, Kawano Y, Shimamoto K, Dodds P, Terauchi R, Kroj T (2014) The NB-LRR proteins RGA4 and RGA5 interact functionally and physically to confer disease resistance. EMBO J 33:1941–1959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Cesari S, Thilliez G, Ribot C, Chalvon V, Michel C, Jauneau A, Rivas S, Alaux L, Kanzaki H, Okuyama Y, Morel JB, Fournier E, Tharreau D, Terauchi R, Kroj T (2013) The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-pia and AVR1-CO39 by direct binding. Plant Cell 25:1463–1481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Maqbool A, Saitoh H, Franceschetti M, Stevenson CEM, Uemura A, Kanzaki H, Kamoun S, Terauchi R, Banfield MJ (2015) Structural basis of pathogen recognition by an integrated HMA domain in a plant NLR immune receptor. elife 4:e08709

    Article  PubMed Central  Google Scholar 

  150. De la Concepcion JC, Franceschetti M, Maqbool A, Saitoh H, Terauchi R, Kamoun S, Banfield MJ (2018) Polymorphic residues in rice NLRs expand binding and response to effectors of the blast pathogen. Nat Plants 4:576–585

    Article  PubMed  CAS  Google Scholar 

  151. De la Concepcion JC, Franceschetti M, MacLean D, Terauchi R, Kamoun S, Banfield MJ (2019) Protein engineering expands the effector recognition profile of a rice NLR immune receptor. elife 8:e47713

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. The Sainsbury Laboratory, University of East Anglia, Norwich, UK

    Neftaly Cruz-Mireles, Iris Eisermann, Marisela Garduño-Rosales, Camilla Molinari, Lauren S. Ryder, Bozeng Tang, Xia Yan & Nicholas J. Talbot

  2. Department of Microbiology, Center for Scientific Research and Higher Education of Ensenada (CICESE), Ensenada, Mexico

    Marisela Garduño-Rosales

Authors
  1. Neftaly Cruz-Mireles
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Iris Eisermann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marisela Garduño-Rosales
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Camilla Molinari
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lauren S. Ryder
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bozeng Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xia Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Nicholas J. Talbot
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nicholas J. Talbot .

Editor information

Editors and Affiliations

  1. Institute of Biotechnology and Drug Research gGmbH (IBWF), Mainz, Rheinland-Pfalz, Germany

    Stefan Jacob

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Cruz-Mireles, N. et al. (2021). The Biology of Invasive Growth by the Rice Blast Fungus Magnaporthe oryzae . In: Jacob, S. (eds) Magnaporthe oryzae. Methods in Molecular Biology, vol 2356. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-1613-0_2

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-1613-0_2

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-1612-3

  • Online ISBN: 978-1-0716-1613-0

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation