The biotrophy-necrotrophy switch in fungal pathogenesis

Agricultural Applications, 2nd Edition

Volumn 11, Issue , 2013, Pages 343-360

  Horbach, Ralf ^a   Deising, Holger B ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; TISSUE;

GENETIC BACKGROUNDS; MOLECULAR LEVELS; PATHOGEN-ASSOCIATED MOLECULAR PATTERNS; PLANT DEFENSE RESPONSE; PLANT PATHOGENIC FUNGUS; SECONDARY METABOLISM; SUBSTRATE SPECIFICITY; SUGAR TRANSPORTERS;

PATHOGENS;

EID: 84897950821     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-642-36821-9_13     Document Type: Chapter

References (95)

1. Barber MS, Bertram RE, Ride JP.(1989) Chitin oligosaccharides elicit lignification in wounded wheat leaves. Physiol Mol Plant Pathol.34(1):3-12
2. Baron-Epel O, Gharyal PK, Schindler M.(1988) Pectins as mediators of wall porosity in soybean cells. Planta.175:389-395
3. Behr M, Humbeck K, Hause G, Deising HB, Wirsel SGR.(2010) The hemibiotroph Colletotrichum graminicola locally induces photosynthetically active green islands but globally accelerates senescence on aging maize leaves. Mol Plant Microbe Interact.23:879-892
4. Behr M, Motyka V, Weihmann F, Malbeck J, Deising HB, Wirsel SGR.(2012) Remodeling of cytokinin metabolism at infection sites of Colletotrichum graminicola on maize leaves. Mol Plant Microbe Interact.25(8):1073-1082
5. Bhadauria V, Banniza S, Vandenberg A, Selvaraj G, Wei Y.(2011) EST mining identifies proteins putatively secreted by the anthracnose pathogen Colletotrichum truncatum. BMC Genomics.12:327
6. Bolton MD, Van Esse HP, Vossen JH, De Jonge R, Stergiopoulos I, Stulemeijer IJE, Van Den Berg G, Borrás-Hidalgo O, Dekker HL, De Koster CG, De Wit PJGM, Joosten MHAJ, Thomma BPHJ.(2008) The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologs in other fungal species. Mol Microbiol.69:119-136
7. Bonas U, Van den Ackerveken G, Büttner D, Hahn K, Marois E, Nennstiel D, Noël L, Rossier O, Szurek B.(2000) How the bacterial plant pathogen Xanthomonas campestris pv. vesicatoria conquers the host. Mol Plant Pathol.1:73-76
8. Bowling AJ, Vaughn KC, Hoagland RE, Stetina K, Douglas Boyette C.(2010) Immunohistochemical investigation of the necrotrophic phase of the fungus Colletotrichum gloeosporioides in the biocontrol of hemp sesbania (Sesbania exaltata; Papilionaceae). Am J Bot.97:1915-1925
9. Brouta F, Descamps F, Monod M, Vermout S, Losson B, Mignon B.(2002) Secreted metalloprotease gene family of Microsporum canis. Infect Immun.70:5676-5683
10. Catanzariti AM, Dodds PN, Lawrence GJ, Ayliffe MA, Ellis JG.(2006) Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell.18:243-256
11. Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, Qu XQ, Guo WJ, Kim JG, Underwood W, Chaudhuri B, Chermak D, Antony G, White FF, Somerville SC, Mudgett MB, Frommer WB.(2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature.468:527-532
12. de Jonge R, Thomma BPHJ.(2009) Fungal LysM effectors:extinguishers of host immunity?.Trends Microbiol.17:151-157
13. de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y, Bours R, van der Krol S, Shibuya N, Joosten MH, Thomma BP.(2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science.329:953-955
14. Deising H, Rauscher M, Haug M, Heiler S.(1995) Differentiation and cell wall-degrading enzymes in the obligately biotrophic rust fungus Uromyces viciae-fabae. Can J Bot.73:624-631
15. Divon HH, Ziv C, Davydov O, Yarden O, Fluhr R.(2006) The global nitrogen regulator, FNR1, regulates fungal nutrition-genes and fitness during Fusarium oxysporum pathogenesis. Mol Plant Pathol.7:485-497
16. Divon HH, Fluhr R.(2007) Nutrition acquisition strategies during fungal infection of plants. FEMS Microbiol Lett.26:65-74
17. Dufresne M, Perfect S, Pellier AL, Bailey JA, Langin T.(2000) A GAL4-like protein is involved in the switch between biotrophic and necrotrophic phases of the infection process of Colletotrichum lindemuthianum on common bean. Plant Cell.12:1579-1590
18. El Gueddari NE, Rauchhaus U, Moerschbacher BM, Deising HB.(2002) Developmentally regulated conversion of surface-exposed chitin to chitosan in cell walls of plant pathogenic fungi. New Phytol.156:103-112
19. Fang W, St. Leger RJ.(2010) Mrt, a gene unique to fungi, encodes an oligosaccharide transporter and facilitates rhizosphere competency in Metarhizium robertsii. Plant Physiol.154:1549e-1557e
20. Felix G, Regenass M, Boller T.(1993) Specific perception of subnanomolar concentrations of chitin fragments by tomato cells: induction of extracellular alkalinization, changes in protein phosphorylation, and establishment of a refractory state. Plant J.4:307-316
21. Fliegmann J, Mithöfer A, Wanner G, Ebel J.(2004) An ancient enzyme domain hidden in the putative betaglucan elicitor receptor of soybean may play an active part in the perception of pathogen-associated molecular patterns during broad host resistance. J Biol Chem.279(2):1132-1140
22. Georgopapadakou NH.(2001) Update on antifungals targeted to the cell wall: focus on beta-1,3-glucan synthase inhibitors. Expert Opin Investig Drugs.10:269-280
23. Haas BJ, Kamoun S, Zody MC, Jiang RHY, Handsaker RE.(2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature.461:393-398
24. Hahn M, Mendgen K.(1992) Isolation by ConA binding of haustoria from different rust fungi and comparison of their surface qualities. Protoplasma.170:95-103
25. Hass H, Taylor TN, Remy W.(1994) Fungi from the Lower Devonian Rhynie Chert: mycoparasitism. Am J Bot.81:29-37
26. Heath MC, Valent B, Howard RJ, Chumley FG.(1990) Interactions of two strains of Magnaporthe grisea with rice, goosegrass, and weeping lovegrass. Can J Bot.68:1627-1637
27. Herbert C, O’ Connell R, Gaqulin E, Salesses V, Esquerre-Tugaye MT, Dumas B.(2004) Production of a cell wall-associated endopolygalacturonase during bean infection. Fungal Genet Biol.41:140-147
28. Horbach R, Graf A, Weihmann F, Antelo L, Mathea S, Liermann JC, Opatz T, Thines E, Aguirre J, Deising HB.(2009) Sfp-type 40-phosphopantetheinyl transferase is indispensable for fungal pathogenicity. Plant Cell.21:3379-3396
29. Horbach R, Navarro-Quesada AR, Knogge W, Deising HB.(2011) When and how to kill a plant cell:infection strategies of plant pathogenic fungi. J Plant Physiol.168:51-62
30. Huser A, Takahara H, Schmalenbach W, O’Connell R.(2009) Discovery of pathogenicity genes in the crucifer anthracnose fungus Colletotrichum higginsianum, using random insertional mutagenesis. Mol Plant Microbe Interact.22:143-156
31. Jousson O, Léchenne B, Bontems O, Capoccia S, Mignon B, Barblan J, Quadroni M, Monod M.(2004) Multiplication of an ancestral gene encoding secreted fungalysin preceded species differentiation in the dermatophytes Trichophyton and Microsporum. Microbiol.150:301-310
32. Kamoun S.(2006) A catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev Phytopathol.44:41-60
33. Kamoun S.(2009) The secretome of plant-associated fungi and oomycetes. In: Deising H (ed) Plant relationships, vol V, 2nd edn, The Mycota. Springer, Berlin/Heidelberg
34. Kämper J, Kahmann R, Bölker M, Ma LJ, Brefort T, Saville BJ et al.(2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature.444:97-101
35. 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
36. Klarzynski O, Plesse B, Joubert JM, Yvin JC, Kopp M, Kloareg B, Fritig B.(2000) Linear beta-1,3 glucans are elicitors of defense responses in tobacco. Plant Physiol.124(3):1027-1038
37. Kleemann J, Rincon-Rivera LJ, Takahara H, Neumann U, van Themaat EVL, van der Does HC, Hacquard S, Stüber K, Will I, Schmalenbach W, Schmelzer E, O’Connell RJ.(2012) Sequential delivery of host-induced virulence effectors by Appressoria and intracellular hyphae of the phytopathogen Colletotrichum higginsianum. PLoS Pathog.8(4):e1002643
38. Kondoh O, Inagaki Y, Fukuda H, Mizuguchi E, Ohya Y, Arisawa M, Nobuo Shimma N, Aoki Y, Sakaitani M, Watanabe T.(2005) Piperazine propanol derivative as a novel antifungal targeting 1,3-b-D-glucan synthase. Biol Pharm Bull.28:2138-2141
39. Krijger J-J, Horbach R, Behr M, Schweizer P, Deising HB, Wirsel SGR.(2008) The yeast signal sequence trap identifies secreted proteins of the hemibiotrophic corn pathogen Colletotrichum graminicola. Mol Plant Microbe Interact.21:1325-1336
40. Latunde-Dada AO, O’Connell RJ, Nash C, Pring RJ, Lucas JA, Bailey JA.(1996) Infection process and identity of the hemibiotrophic anthracnose fungus (Colletotrichum destructivum O’Gara) from cowpea (Vigna unguiculata (L.) Walp.). Mycol Res.100:1133-1141
41. Lingner U.(2012) Stoffaustausch bei der Interaktion zwischen Pflanze und Pilz: Identifizierung von Zuckertransportern und deren Charakterisierung. In: Naturwissenschaftliche Fakultät. Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen-Nuremberg, p 131
42. Lingner U, Muench S, Deising HB, Sauer N.(2011 a) Hexose transporters of a hemibiotrophic plant pathogen: functional variations and regulatory differences at different stages of infection. J Biol Chem.286:20913-20922
43. Lingner U, Münch S, Sode B, Deising HB, Sauer N.(2011 b) Functional characterization of a eukaryotic melibiose transporter.Plant Physiol.156:1565-1576
44. López-Berges MS, Rispail N, Prados-Rosales RC, Di Pietro A.(2010) A nitrogen response pathway regulates virulence functions in Fusarium oxysporum via the protein kinase TOR and the bZIP protein MeaB. Plant Cell.22:2459-2475
45. Maor R, Shirasu K.(2005) The arms race continues: battle strategies between plants and fungal pathogens. Curr Opinion Microbiol.8(4):399-404
46. Mathy A, Baldo A, Schoofs L, Cambier L, Defaweux V, Tabart J, Maréchal F, Symoens F, Mignon B.(2010) Fungalysin and dipeptidyl-peptidase gene transcription in Microsporum canis strains isolated from symptomatic and asymptomatic cats. Vet Microbiol.146:179-182
47. Mendgen K, Deising H.(1993) Infection structures of fungal plant pathogens - a cytological and physiological evaluation. New Phytol.124:193-213
48. Mendgen K, Hahn M.(2002) Plant infection and establishment of fungal biotrophy. Trends Plant Sci.7(8):352-356
49. 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
50. Mims CW, Rodriguez-Lother C, Richardson EA.(2002) Ultrastructure of the host-pathogen interface in daylily leaves infected by the rust fungus Puccinia hemerocallidis. Protoplasma.219(3-4):221-226
51. Nürnberger T, Brunner F, Kemmerling B, Piater L.(2004) Innate immunity in plants and animals:striking similarities and obvious differences. Immunol Rev.198:249-266
52. O’Connell RJ, Uronu AB, Waksman G, Nash C, Keon JPR, Bailey JA.(1993) Hemibiotrophic infection of Pisum sativum by Colletotrichum truncatum. Plant Pathol.42:774-783
53. O’Connell RJ, Thon MR, Hacquard S et al.(2012) Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nature Genet.44:1060-1065
54. Oliver RP, Ipcho SV.(2004) Arabidopsis pathology breathes new life into the necrotrophs-vs.-biotrophs classification of fungal pathogens. Mol Plant Pathol.5(4):347-352
55. Pain NA, Green JR, Gammie F, O’Connell RJ.(1994 a) Immunomagnetic isolation of viable intracellular hyphae of Colletotrichum lindemuthianum from infected bean leaves using a monoclonal antibody.New Phytol.127:223-232
56. Pain NA, O’Connell RJ, Mendgen K, Green JR.(1994 b) Identification of glycoproteins specific to biotrophic intracellular hyphae formed in the Colletotrichum-bean interaction.New Phytol.127:233-242
57. Patrick JW.(1989) Solute efflux at plant/microorganism interfaces. Aust J Plant Physiol.16:53-68
58. Pellier AL, Lauge R, Veneault-Fourrey C, Langin T.(2003) CLNR1, the AREA/NIT2-like global nitrogen regulator of the plant fungal pathogen Colletotrichum lindemuthianum is required for the infection cycle. Mol Microbiol.48:639-655
59. Perfect SE, Green JR, O’Connell RJ.(2001) Surface characteristics of necrotrophic secondary hyphae produced by the bean anthracnose fungus, Colletotrichum lindemuthianum. Eur J Plant Pathol.107:813-819
60. Postel S, Kemmerling B.(2009) Plant systems for recognition of pathogen-associated molecular patterns. Semin Cell Dev Biol.20:1025-1031
61. Prusky D, McEvoy JL, Leverentz B, Conway WS.(2001) Local modulation of host pH by Colletotrichum species as a mechanism to increase virulence. Mol Plant Microbe Interact.14:1105-1113
62. Remy E, Meyer M, Blaise F, Simon UK, Kuhn D, Balesdent MH, Rouxel T.(2009) A key enzyme of the Leloir pathway is involved in pathogenicity of Leptosphaeria maculans towards oilseed rape. Mol Plant Microbe Interact.22:725-736
63. Rosenblum EB, Stajich JE, Maddox N, Eisen MB.(2008) Global gene expression profiles for life stages of the deadly amphibian pathogen Batrachochytrium dendrobatidis. Proc Natl Acad Sci USA.105:17034-17039
64. Schüßler A, Martin H, Cohen D, Fitz M, Wipf D.(2006) Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi. Nature.444:933-936
65. Serfling A, Wohlrab J, Deising H.(2007) Treatment of a clinically relevant plant-pathogenic fungus with an agricultural azole causes cross-resistance to medical azoles and potentiates caspofungin efficacy. Antimicrob Agents Chemother.51(10):' 3672-3676
66. Shetty NP, Jensen JD, Knudsen A, Finnie C, Geshi N, Blennow A, Collinge DB, Jørgensen HJ.(2009) Effects of beta-1,3-glucan from Septoria tritici on structural defence responses in wheat. J Exp Bot.60(15):4287-4300
67. Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H, Shibuya N.(2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J.64:204-214
68. Shrestha B, Vertes A.(2009) In situ metabolic profiling of single cells by laser ablation electrospray ionization mass spectrometry. Anal Chem.81:8265-8271
69. Snoeijers SS, Pérez-García A, Joosten MHAJ, de Wit PJGM.(2000) The effect of nitrogen on disease development and gene expression in bacterial and fungal plant pathogens. Eur J Plant Pathol.106:493-506
70. Sonnewald U.(2011) SWEETS - The missing sugar efflux carriers. Front Plant Sci 2, article 7
71. Takahara H, Dolf A, Endl E, O’Connell R.(2009) Flow cytometric purification of Colletotrichum higginsianum biotrophic hyphae from Arabidopsis leaves for stage-specific transcriptome analysis. Plant J.59:672-683
72. Tang W, Coughlan S, Crane E, Beatty M, Duvick J.(2006) The application of laser microdissection to in planta gene expression profiling of the maize anthracnose stalk rot fungus Colletotrichum graminicola. Mol Plant Microbe Interact.19:1240-1250
73. Taylor TN, Remy W, Hass H.(1992) Parasitism in a 400-million-year-old green alga.Nature.357:493-494
74. Taylor TN, Remy W, Hass H, Kerp H.(1995) Fossil arbuscular-mycorrhiza from the Early Devonian. Mycologia.87:560-573
75. Thomma BPHJ, Bolton MD, Clergeot PH, de Wit PJGM.(2006) Nitrogen controls in planta expression of Cladosporium fulvum Avr9 but no other effector genes. Mol Plant Pathol.7:125-130
76. Thon MR, Nuckles EM, Takach JE, Vaillancourt LJ.(2002) CPR1: a gene encoding a putative signal peptidase that functions in pathogenicity of Colletotrichum graminicola to maize. Mol Plant Microbe Interact.15:120-128
77. van den Ackerveken GFJM, Dunn RM, Cozijnsen AJ, Vossen JPMJ, Van Den Broek HWJ, de Wit PJGM.(1994) Nitrogen limitation induces expression of the avirulence gene Avr9 in the tomato pathogen Cladosporium fulvum. Mol Gen Genet.243:277-285
78. Vander P, Varum KM, Domard A, El-Gueddari NE, Moerschbacher BM.(1998) Comparison of the ability of partially Nacetylated chitosans and chitooligosaccharides to elicit resistance reactions in wheat leaves. Plant Physiol.118:1353-1359
79. Vargas WA, Sanz Martín JM, Rech GE, Rivera LP, Benito EP, Díaz-Mínguez JM, Thon MR, Sukno SA.(2012) Plant defense mechanisms are activated during biotrophic and necrotrophic development of Colletotricum graminicola in maize. Plant Physiol.158:1342-1358
80. Vleeshouwers VG, Raffaele S, Vossen JH, Champouret N, Oliva R, Segretin ME, Rietman H, Cano LM, Lokossou A, Kessel G, Pel MA, Kamoun S.(2011) Understanding and exploiting late blight resistance in the age of effectors. Annu Rev Phytopathol.49:507-531
81. Voegele RT, Struck C, Hahn M, Mendgen K.(2001) The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proc Natl Acad Sci USA.98:8133-8138
82. Voll LM, Horst RJ, Voitsik A-M, Zajic D, Samans B, Pons-Kühnemann J, Doehlemann G, Münch S, Wahl R, Molitor A, Hofmann J, Schmiedl A, Waller F, Deising HB, Kahmann R, Kämper J, Kogel K-H, Sonnewald U.(2011) Common motifs in the response of cereal primary metabolism to fungal pathogens are not based on similar transcriptional reprogramming. Front Plant Sci.2:39
83. Wahl R, Wippel K, Goos S, Kämper J, Sauer N.(2010) A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol.8(2):e1000303
84. Walton JD.(1994) Deconstructing the cell wall. Plant Physiol.104:1113-1118
85. Walton JD.(1996) Host-selective toxins: agents of compatibility. Plant Cell.8:1723-1733
86. Wattad C, Dinoor A, Prusky D.(1994) Purification of pectate lyase produced by Colletotrichum gloeosporioides and its inhibition by epicatechin:a possible factor involved in the resistance of unripe avocado fruits to anthracnose. Mol Plant Microbe Interact.7:293-297
87. Wei Y, Shen W, Dauk M, Wang F, Selvaraj G, Zou J.(2004) Targeted gene disruption of glycerol-3- phosphate dehydrogenase in Colletotrichum gloeosporioides reveals evidence that glycerol is a significant transferred nutrient from host plant to fungal pathogen. J Biol Chem.279:429-435
88. Weiergang I, Dunkle LD, Wood KV, Nicholson RL.(1996) Morphogenic regulation of pathotoxin synthesis in Cochliobolus carbonum. Fungal Genet Biol.20:74-78
89. Werner S, Sugui JA, Steinberg G, Deising HB.(2007) A chitin synthase with a myosin-like motor domain is essential for hyphal growth, appressorium differentiation and pathogenicity of the maize anthracnose fungus Colletotrichum graminicola. Mol Plant Microbe Interact.20:1555-1567
90. Wessels JGH.(1996) Fungal hydrophobins: proteins that function at an interface. Trends Plant Sci.1:9-15
91. Wharton PS, Julian AM, O’Connell RJ.(2001) Ultrastructure of the infection of Sorghum bicolor by Colletotrichum sublineolum. Phytopathology.91:148-158
92. Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, Gilroy EM, Armstrong MR, Grouffaud S, van West P, Chapman S et al.(2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature.450:115-118
93. Yaeno T, Li H, Chaparro-Garcia A, Schornack S, Koshiba S, Watanabe S et al.(2011) Phosphatidylinositol monophosphate-binding interface in the oomycete RXLR effector AVR3a is required for its stability in host cells to modulate plant immunity. Proc Natl Acad Sci USA.108:14682-14687
94. Yakoby N, Kobiler I, Dinoor A, Prusky D.(2000) pH regulation of pectate lyase secretion modulates the attack of Colletotrichum gloeosporioides on avocado fruits. Appl Environ Microbiol.66:1026-1030
95. Yakoby N, Beno-Moualem D, Keen NT, Dinoor A, Pines O, Prusky D.(2001) Colletotrichum gloeosporioides pelB is an important virulence factor in avocado fruit-fungus interaction. Mol Plant Microbe Interact.14:988-995