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

Appressorium Autophagy Cell cycle Fungus MAP kinase Pathogenesis Plasmodesmata Pyricularia Rice Septins Virulence Wheat

Journal

Methods in molecular biology (Clifton, N.J.)
ISSN: 1940-6029
Titre abrégé: Methods Mol Biol
Pays: United States
ID NLM: 9214969

Informations de publication

Date de publication:
2021
Historique:
entrez: 8 7 2021
pubmed: 9 7 2021
medline: 13 1 2022
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 34236674
doi: 10.1007/978-1-0716-1613-0_2
doi:

Substances chimiques

Fungal Proteins 0
Septins EC 3.6.1.-

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

19-40

Références

Wilson RA, Talbot NJ (2009) Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat Rev Microbiol 7:185–195
pubmed: 19219052 doi: 10.1038/nrmicro2032 pmcid: 19219052
Hamer JE, Howard RJ, Chumley FG, Valent B (1988) A mechanism for surface attachment in spores of a plant pathogenic fungus. Science 239:288
pubmed: 17769992 doi: 10.1126/science.239.4837.288
Bourett TM, Howard RJ (1990) In vitro development of penetration structures in the rice blast fungus Magnaporthe grisea. Can J Bot 68:329–342
doi: 10.1139/b90-044
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
pubmed: 19717456 pmcid: 2747227 doi: 10.1073/pnas.0901477106
de Jong JC, McCormack BJ, Smirnoff N, Talbot NJ (1997) Glycerol generates turgor in rice blast. Nature 389:244–244
doi: 10.1038/38418
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
pubmed: 28165657 doi: 10.1111/1462-2920.13688
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
pubmed: 22267486 pmcid: 3289562 doi: 10.1105/tpc.111.092957
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
pubmed: 27816794 doi: 10.1016/j.mib.2016.10.001 pmcid: 27816794
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
pubmed: 26703899 doi: 10.1016/j.fgb.2015.12.009
Talbot NJ (2003) On the trail of a cereal killer: exploring the biology of Magnaporthe grisea. Ann Rev Microbiol 57:177–202
doi: 10.1146/annurev.micro.57.030502.090957
Wang X, Valent B (2009) Advances in genetics, genomics and control of rice blast disease. Springer Science & Business Media, Berlin/Heidelberg
doi: 10.1007/978-1-4020-9500-9
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
pubmed: 21283781 pmcid: 3024261 doi: 10.1371/journal.ppat.1001261
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
pubmed: 8312740 pmcid: 160387
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
pubmed: 27142249 pmcid: 4855151 doi: 10.1038/srep25288
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
pubmed: 15774025 pmcid: 1088943 doi: 10.1186/gb-2005-6-3-r24
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
pubmed: 10521529 pmcid: 144101 doi: 10.1105/tpc.11.10.2013
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
pubmed: 9390422 doi: 10.1094/MPMI.1997.10.9.1075 pmcid: 9390422
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
pubmed: 17255942 pmcid: 1794393 doi: 10.1038/sj.emboj.7601536
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
pubmed: 11059488 doi: 10.1094/MPMI.2000.13.11.1214 pmcid: 11059488
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
pubmed: 22927898 pmcid: 3426613 doi: 10.1371/journal.pone.0041084
Bölker M (1998) Sex and crime: heterotrimeric G proteins in fungal mating and pathogenesis. Fungal Genet Biol 25:143–156
pubmed: 9917369 doi: 10.1006/fgbi.1998.1102 pmcid: 9917369
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
doi: 10.1111/j.1574-6968.1999.tb13403.x
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
pubmed: 8946911 doi: 10.1101/gad.10.21.2696 pmcid: 8946911
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
pubmed: 9707535 pmcid: 144070 doi: 10.1105/tpc.10.8.1361
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
pubmed: 15846337 doi: 10.1038/nature03449 pmcid: 15846337
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
pubmed: 9401122 pmcid: 157051
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
doi: 10.1006/pmpp.1996.0027
Douglas LM, Alvarez FJ, McCreary C, Konopka JB (2005) Septin function in yeast model systems and pathogenic fungi. Eukaryot Cell 4:1503–1512
pubmed: 16151244 pmcid: 1214204 doi: 10.1128/EC.4.9.1503-1512.2005
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
pubmed: 6638784 pmcid: 6638784 doi: 10.1111/j.1364-3703.2011.00783.x
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
pubmed: 25901357 pmcid: 4406744 doi: 10.1371/journal.ppat.1004851
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
pubmed: 21115813 pmcid: 3003025 doi: 10.1073/pnas.1006839107
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
pubmed: 22570632 pmcid: 3342947 doi: 10.1371/journal.pgen.1002673
Jiang C, Zhang X, Liu H, Xu J-R (2018) Mitogen-activated protein kinase signaling in plant pathogenic fungi. PLoS Pathog 14:e1006875
pubmed: 29543901 pmcid: 5854419 doi: 10.1371/journal.ppat.1006875
Turrà D, Segorbe D, Di Pietro A (2014) Protein kinases in plant-pathogenic fungi: conserved regulators of infection. Annu Rev Phytopathol 52:267–288
pubmed: 25090477 doi: 10.1146/annurev-phyto-102313-050143
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
pubmed: 29567712 doi: 10.1126/science.aaq0892
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
pubmed: 15590826 pmcid: 539019 doi: 10.1128/EC.3.6.1525-1532.2004
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
doi: 10.1105/tpc.104.029116
Li G, Zhou X, Xu J-R (2012) Genetic control of infection-related development in Magnaporthe oryzae. Curr Opin Microbiol 15:678–684
pubmed: 23085322 doi: 10.1016/j.mib.2012.09.004
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
pubmed: 17214742 doi: 10.1111/j.1365-2958.2006.05548.x pmcid: 17214742
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
pubmed: 27059015 doi: 10.1111/1462-2920.13315
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
pubmed: 26057388 doi: 10.1094/MPMI-12-14-0391-R
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
pubmed: 24835254 doi: 10.1094/MPMI-02-14-0052-R
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
pubmed: 28244240 doi: 10.1111/1462-2920.13710
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
pubmed: 17056708 pmcid: 1626611 doi: 10.1105/tpc.105.038422
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
pubmed: 14507377 doi: 10.1046/j.1365-2958.2003.03676.x
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
pubmed: 27898176 doi: 10.1111/nph.14347
Ryder LS, Talbot NJ (2015) Regulation of appressorium development in pathogenic fungi. Curr Opin Plant Biol 26:8–13
pubmed: 26043436 pmcid: 4781897 doi: 10.1016/j.pbi.2015.05.013
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
pubmed: 21642506 pmcid: 3165448 doi: 10.1128/EC.00007-11
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
pubmed: 19997500 pmcid: 2779367 doi: 10.1371/journal.pgen.1000757
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
pubmed: 26441322 doi: 10.1094/MPMI-09-15-0201-R
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
pubmed: 22346750 pmcid: 3276559 doi: 10.1371/journal.ppat.1002514
Saunders DG, Aves SJ, Talbot NJ (2010) Cell cycle-mediated regulation of plant infection by the rice blast fungus. Plant Cell 22:497–507
pubmed: 20190078 pmcid: 2845407 doi: 10.1105/tpc.109.072447
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
pubmed: 29259729 pmcid: 5731507 doi: 10.1080/19420889.2017.1372067
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
pubmed: 28028232 doi: 10.1073/pnas.1611307114
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
pubmed: 20639448 pmcid: 2929119 doi: 10.1105/tpc.110.074492
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
pubmed: 1868838 pmcid: 452969 doi: 10.1002/j.1460-2075.1991.tb07810.x
Rhind N, Russell P (1998) Mitotic DNA damage and replication checkpoints in yeast. Curr Opin Cell Biol 10:749–758
pubmed: 9914174 pmcid: 2864141 doi: 10.1016/S0955-0674(98)80118-X
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
pubmed: 16645096 doi: 10.1126/science.1124550
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
pubmed: 17416896 pmcid: 1951528 doi: 10.1128/EC.00011-07
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
pubmed: 32367535 doi: 10.1111/nph.16636
Armentrout V, Downer A (1987) Infection cushion development by Rhizoctonia solani on cotton. Phytopathology 77:619–623
doi: 10.1094/Phyto-77-619
Mendgen K, Hahn M, Deising H (1996) Morphogenesis and mechanisms of penetration by plant pathogenic fungi. Annu Rev Phytopathol 34:367–386
pubmed: 15012548 doi: 10.1146/annurev.phyto.34.1.367
Talbot NJ (2019) Appressoria. Curr Biol 29:R144–r146
pubmed: 30836078 doi: 10.1016/j.cub.2018.12.050
Skamnioti P, Gurr SJ (2007) Magnaporthe grisea Cutinase2 mediates appressorium differentiation and host penetration and is required for full virulence. Plant Cell 19:2674
pubmed: 17704215 pmcid: 2002628 doi: 10.1105/tpc.107.051219
Chang HX, Miller LA, Hartman GL (2014) Melanin-independent accumulation of turgor pressure in appressoria of Phakopsora pachyrhizi. Phytopathology 104:977–984
pubmed: 24779353 doi: 10.1094/PHYTO-12-13-0335-R
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
pubmed: 24725259 doi: 10.1111/nph.12784
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
doi: 10.1094/MPMI-09-13-0267-R
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
pubmed: 10521531 pmcid: 144108 doi: 10.1105/tpc.11.10.2045
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
pubmed: 31597961 doi: 10.1038/s41586-019-1637-x
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
pubmed: 9867851 doi: 10.1074/jbc.274.1.360
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
pubmed: 20848286 doi: 10.1007/s00294-010-0319-x
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
pubmed: 23382235 pmcid: 3581893 doi: 10.1073/pnas.1217470110
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
pubmed: 22723425 doi: 10.1126/science.1222934
Bourett TM, Howard RJ (1992) Actin in penetration pegs of the fungal rice blast pathogen, Magnaporthe grisea. Protoplasma 168:20–26
doi: 10.1007/BF01332647
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
pubmed: 20302965 doi: 10.1016/j.fgb.2010.03.004
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
pubmed: 24800890 pmcid: 4011870 doi: 10.1371/journal.pone.0096744
Upadhyay S, Shaw BD (2008) The role of actin, fimbrin and endocytosis in growth of hyphae in aspergillus nidulans. Mol Microbiol 68:690–705
pubmed: 18331474 doi: 10.1111/j.1365-2958.2008.06178.x
Berepiki A, Lichius A, Shoji JY, Tilsner J, Read ND (2010) F-actin dynamics in Neurospora crassa. Eukaryot Cell 9:547–557
pubmed: 20139238 pmcid: 2863416 doi: 10.1128/EC.00253-09
Roberson RW (1992) The actin cytoskeleton in hyphal cells of Sclerotium rolfsii. Mycologia 84:41–51
doi: 10.1080/00275514.1992.12026102
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
pubmed: 18216285 pmcid: 2291424 doi: 10.1091/mbc.e07-05-0464
Berepiki A, Lichius A, Read ND (2011) Actin organization and dynamics in filamentous fungi. Nat Rev Microbiol 9:876–887
pubmed: 22048737 doi: 10.1038/nrmicro2666
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
pubmed: 18536722 pmcid: 2814344 doi: 10.1038/nmeth.1220
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
doi: 10.1002/cm.20461
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
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
pubmed: 4950437 doi: 10.1016/0014-4827(71)90223-0
Spiliotis ET, Nelson WJ (2006) Here come the septins: novel polymers that coordinate intracellular functions and organization. J Cell Sci 119:4–10
pubmed: 16371649 doi: 10.1242/jcs.02746
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
pubmed: 16353550 doi: 10.1094/MPMI-18-1148
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
pubmed: 19805342 pmcid: 2757862 doi: 10.1073/pnas.0902858106
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
pubmed: 14993234 pmcid: 2172161 doi: 10.1083/jcb.200312070
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
pubmed: 17637674 doi: 10.1038/nature06052 pmcid: 17637674
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
pubmed: 32305452 doi: 10.1016/j.fgb.2020.103385 pmcid: 32305452
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
pubmed: 28742127 pmcid: 5542705 doi: 10.1371/journal.ppat.1006516
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
pubmed: 30446520 doi: 10.1534/genetics.118.301490 pmcid: 30446520
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
pubmed: 9770551 pmcid: 22896 doi: 10.1073/pnas.95.21.12713
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
pubmed: 11952120 doi: 10.1094/MPMI.2002.15.3.183 pmcid: 11952120
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
pubmed: 29663402 doi: 10.1111/nph.15141 pmcid: 29663402
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
pubmed: 26566920 pmcid: 4682301 doi: 10.1105/tpc.15.00552
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
pubmed: 27066032 pmcid: 4811896 doi: 10.3389/fpls.2016.00382
Fernandez J, Orth K (2018) Rise of a cereal killer: the biology of Magnaporthe oryzae biotrophic growth. Trends Microbiol 26:582–597
pubmed: 29395728 pmcid: 6003838 doi: 10.1016/j.tim.2017.12.007
Yi M, Valent B (2013) Communication between filamentous pathogens and plants at the biotrophic interface. Annu Rev Phytopathol 51:587–611
pubmed: 23750888 doi: 10.1146/annurev-phyto-081211-172916 pmcid: 23750888
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
pubmed: 17322409 pmcid: 1867340 doi: 10.1105/tpc.106.046300
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
pubmed: 23774898 doi: 10.1038/ncomms2996 pmcid: 23774898
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
pubmed: 20435900 pmcid: 2879738 doi: 10.1105/tpc.109.069666
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
pubmed: 19357089 pmcid: 2685627 doi: 10.1105/tpc.107.055228
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
pubmed: 26258762 doi: 10.1038/nchembio.1885 pmcid: 26258762
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
pubmed: 28418377 doi: 10.1038/nmicrobiol.2017.54 pmcid: 28418377
Valent B, Khang CH (2010) Recent advances in rice blast effector research. Curr Opin Plant Biol 13:434–441
pubmed: 20627803 doi: 10.1016/j.pbi.2010.04.012 pmcid: 20627803
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
pubmed: 27711180 pmcid: 5053420 doi: 10.1371/journal.ppat.1005921
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
pubmed: 19602150 doi: 10.1111/j.1365-2958.2009.06786.x pmcid: 19602150
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
pubmed: 18344407 pmcid: 2394974 doi: 10.1128/EC.00009-08
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
pubmed: 22321443 pmcid: 3355222 doi: 10.1111/j.1364-3703.2011.00779.x
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
pubmed: 22947213 doi: 10.1094/MPMI-12-11-0326
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
pubmed: 24848414 doi: 10.1146/annurev-phyto-102313-050135
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
pubmed: 25188286 pmcid: 4154871 doi: 10.1371/journal.ppat.1004354
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
pubmed: 30462633 pmcid: 6281275 doi: 10.1371/journal.pgen.1007814
Molloy S (2010) Fungal biology: Magnaporthe effectors on the move. Nat Rev Microbiol 8:466–467
pubmed: 21394961 doi: 10.1038/nrmicro2389
Kamoun S (2006) A catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev Phytopathol 44:41–60
pubmed: 16448329 doi: 10.1146/annurev.phyto.44.070505.143436
Govers F, Bouwmeester K (2008) Effector trafficking: RXLR-dEER as extra gear for delivery into plant cells. Plant Cell 20:1728–1730
pubmed: 18647825 pmcid: 2518235 doi: 10.1105/tpc.108.062075
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
pubmed: 22589729 pmcid: 3349759 doi: 10.1371/journal.ppat.1002711
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
pubmed: 23762023 pmcid: 3675110 doi: 10.1371/journal.ppat.1003350
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
pubmed: 18723576 pmcid: 2553620 doi: 10.1105/tpc.108.060194
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
pubmed: 19132864 doi: 10.1094/MPMI-22-2-0115
Birch PR, Rehmany AP, Pritchard L, Kamoun S, Beynon JL (2006) Trafficking arms: oomycete effectors enter host plant cells. Trends Microbiol 14:8–11
pubmed: 16356717 doi: 10.1016/j.tim.2005.11.007
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
pubmed: 23223409 doi: 10.1101/sqb.2012.77.015933
Bozkurt TO, Schornack S, Banfield MJ, Kamoun S (2012) Oomycetes, effectors, and all that jazz. Curr Opin Plant Biol 15:483–492
pubmed: 22483402 doi: 10.1016/j.pbi.2012.03.008
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
pubmed: 27882964 pmcid: 5135018 doi: 10.1038/nature20166
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
doi: 10.1093/mp/sst015 pubmed: 23340743
Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814
pubmed: 16497589 doi: 10.1016/j.cell.2006.02.008
Banfield MJ (2015) Perturbation of host ubiquitin systems by plant pathogen/pest effector proteins. Cell Microbiol 17:18–25
pubmed: 25339602 doi: 10.1111/cmi.12385
Oliveira-Garcia E, Valent B (2015) How eukaryotic filamentous pathogens evade plant recognition. Curr Opin Microbiol 26:92–101
pubmed: 26162502 doi: 10.1016/j.mib.2015.06.012 pmcid: 26162502
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
pubmed: 25198435 doi: 10.3109/07388551.2014.946883
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
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
pubmed: 29358651 doi: 10.1038/s41588-018-0040-0
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
pubmed: 10921881 pmcid: 306585 doi: 10.1093/emboj/19.15.4004
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
pubmed: 22805093 doi: 10.1111/j.1365-313X.2012.05110.x
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
pubmed: 19454732 pmcid: 2700537 doi: 10.1105/tpc.109.066324
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
pubmed: 21829350 pmcid: 3145791 doi: 10.1371/journal.ppat.1002147
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
pubmed: 26109439 pmcid: 5387869 doi: 10.1038/srep11642
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
pubmed: 28684523 doi: 10.1126/science.aam9654 pmcid: 28684523
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
pubmed: 19849781 doi: 10.1111/j.1364-3703.2009.00591.x
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
doi: 10.1016/S2095-3119(17)61746-5
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
pubmed: 11090206 pmcid: 152363 doi: 10.1105/tpc.12.11.2019
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
pubmed: 15319478 pmcid: 520948 doi: 10.1105/tpc.104.022715
Wolpert TJ, Dunkle LD, Ciuffetti LM (2002) Host-selective toxins and avirulence determinants: what's in a name? Annu Rev Phytopathol 40:251–285
pubmed: 12147761 doi: 10.1146/annurev.phyto.40.011402.114210
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
pubmed: 12838393 doi: 10.1007/s00122-003-1349-2
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
pubmed: 28698366 pmcid: 5544293 doi: 10.1073/pnas.1702041114
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
pubmed: 25024433 pmcid: 4195788 doi: 10.15252/embj.201487923
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
pubmed: 23548743 pmcid: 3663280 doi: 10.1105/tpc.112.107201
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
pmcid: 4547098 doi: 10.7554/eLife.08709 pubmed: 4547098
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
pubmed: 29988155 doi: 10.1038/s41477-018-0194-x
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
pubmed: 31535976 pmcid: 6768660 doi: 10.7554/eLife.47713

Auteurs

Neftaly Cruz-Mireles (N)

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

Iris Eisermann (I)

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

Marisela Garduño-Rosales (M)

The Sainsbury Laboratory, University of East Anglia, Norwich, UK.
Department of Microbiology, Center for Scientific Research and Higher Education of Ensenada (CICESE), Ensenada, Mexico.

Camilla Molinari (C)

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

Lauren S Ryder (LS)

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

Bozeng Tang (B)

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

Xia Yan (X)

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

Nicholas J Talbot (NJ)

The Sainsbury Laboratory, University of East Anglia, Norwich, UK. Nick.Talbot@tsl.ac.uk.

Articles similaires

Genome, Viral Ralstonia Composting Solanum lycopersicum Bacteriophages
Biological Evolution History, 20th Century Selection, Genetic History, 19th Century Biology
Capsicum Disease Resistance Plant Diseases Polymorphism, Single Nucleotide Ralstonia solanacearum
Biofilms Candida albicans Quorum Sensing Candida glabrata Menthol

Classifications MeSH