Skip to main content

13 The Biotrophy–Necrotrophy Switch in Fungal Pathogenesis

  • Chapter
  • First Online:
Agricultural Applications

Part of the book series: The Mycota ((MYCOTA,volume 11))

Abstract

In recent years, increasing numbers of plant pathogenic fungi have been identified as hemibiotrophs, i.e., pathogens sequentially differentiating biotrophic and necrotrophic hyphae in the host tissue. Interestingly, these pathogens make it possible to analyze biotrophic and necrotrophic lifestyles at the molecular level in the same genetic background. Biotrophic development strictly depends on prevention of initiation of plant defense responses, either by masking pathogen-associated molecular patterns or by secretion of effectors which efficiently interfere with recognition of the invading pathogen and/or signal transduction. After establishment of biotrophic hyphae, hemibiotrophs switch to necrotrophic development. The signal(s) leading to switching of hyphal morphology and lifestyles is/are so far unknown, but fundamental physiological changes are associated with these changes. For example, the carbon sources available during biotrophic growth in the interfacial matrix are probably strikingly different from those available during growth on killed host tissue, and, accordingly, different sets of sugar transporters differing in their substrate specificity are activated. Furthermore, associated with changing lifestyle, dramatic changes in fungal secondary metabolism occur, and these changes probably pave the necrotrophic pathway.

This review provides an overview of recent development and understanding of fungal hemibiotrophy.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 299.99
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

  • Barber MS, Bertram RE, Ride JP (1989) Chitin oligosaccharides elicit lignification in wounded wheat leaves. Physiol Mol Plant Pathol 34(1):3–12

    Article  CAS  Google Scholar 

  • Baron-Epel O, Gharyal PK, Schindler M (1988) Pectins as mediators of wall porosity in soybean cells. Planta 175:389–395

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bolton MD, Van Esse HP, Vossen JH, De Jonge R, Stergiopoulos I, Stulemeijer IJE, Van Den Berg G, Borráás‐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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • de Jonge R, Thomma BPHJ (2009) Fungal LysM effectors: extinguishers of host immunity? Trends Microbiol 17:151–157

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Divon HH, Fluhr R (2007) Nutrition acquisition strategies during fungal infection of plants. FEMS Microbiol Lett 26:65–74

    Article  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Fliegmann J, Mithöfer A, Wanner G, Ebel J (2004) An ancient enzyme domain hidden in the putative beta-glucan 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hass H, Taylor TN, Remy W (1994) Fungi from the Lower Devonian Rhynie Chert: mycoparasitism. Am J Bot 81:29–37

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Horbach R, Graf A, Weihmann F, Antelo L, Mathea S, Liermann JC, Opatz T, Thines E, Aguirre J, Deising HB (2009) Sfp-type 4′-phosphopantetheinyl transferase is indispensable for fungal pathogenicity. Plant Cell 21:3379–3396

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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-β-D-glucan synthase. Biol Pharm Bull 28:2138–2141

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Lingner U, Muench S, Deising HB, Sauer N (2011a) Hexose transporters of a hemibiotrophic plant pathogen: functional variations and regulatory differences at different stages of infection. J Biol Chem 286:20913–20922

    Article  PubMed  CAS  Google Scholar 

  • Lingner U, Münch S, Sode B, Deising HB, Sauer N (2011b) Functional characterization of a eukaryotic melibiose transporter. Plant Physiol 156:1565–1576

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Maor R, Shirasu K (2005) The arms race continues: battle strategies between plants and fungal pathogens. Curr Opinion Microbiol 8(4):399–404

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Mendgen K, Deising H (1993) Infection structures of fungal plant pathogens – a cytological and physiological evaluation. New Phytol 124:193–213

    Article  Google Scholar 

  • Mendgen K, Hahn M (2002) Plant infection and establishment of fungal biotrophy. Trends Plant Sci 7(8):352–356

    Article  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Pain NA, Green JR, Gammie F, O’Connell RJ (1994a) Immunomagnetic isolation of viable intracellular hyphae of Colletotrichum lindemuthianum from infected bean leaves using a monoclonal antibody. New Phytol 127:223–232

    Article  Google Scholar 

  • Pain NA, O’Connell RJ, Mendgen K, Green JR (1994b) Identification of glycoproteins specific to biotrophic intracellular hyphae formed in the Colletotrichum–bean interaction. New Phytol 127:233–242

    Article  CAS  Google Scholar 

  • Patrick JW (1989) Solute efflux at plant/micro-organism interfaces. Aust J Plant Physiol 16:53–68

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Postel S, Kemmerling B (2009) Plant systems for recognition of pathogen-associated molecular patterns. Semin Cell Dev Biol 20:1025–1031

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Schüßler A, Martin H, Cohen D, Fitz M, Wipf D (2006) Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi. Nature 444:933–936

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Shrestha B, Vertes A (2009) In situ metabolic profiling of single cells by laser ablation electrospray ionization mass spectrometry. Anal Chem 81:8265–8271

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sonnewald U (2011) SWEETS – The missing sugar efflux carriers. Front Plant Sci 2, article 7

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Taylor TN, Remy W, Hass H (1992) Parasitism in a 400-million-year-old green alga. Nature 357:493–494

    Article  Google Scholar 

  • Taylor TN, Remy W, Hass H, Kerp H (1995) Fossil arbuscular-mycorrhiza from the Early Devonian. Mycologia 87:560–573

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Walton JD (1994) Deconstructing the cell wall. Plant Physiol 104:1113–1118

    PubMed  CAS  Google Scholar 

  • Walton JD (1996) Host-selective toxins: agents of compatibility. Plant Cell 8:1723–1733

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Weiergang I, Dunkle LD, Wood KV, Nicholson RL (1996) Morphogenic regulation of pathotoxin synthesis in Cochliobolus carbonum. Fungal Genet Biol 20:74–78

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Wessels JGH (1996) Fungal hydrophobins: proteins that function at an interface. Trends Plant Sci 1:9–15

    Article  Google Scholar 

  • Wharton PS, Julian AM, O’Connell RJ (2001) Ultrastructure of the infection of Sorghum bicolor by Colletotrichum sublineolum. Phytopathology 91:148–158

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors acknowledge support by Deutsche Forschungsgemeinschaft (DFG), FOR666 project A1; project HO4600/1-1 and project HO4600/2-1, and by Interdisciplinary Center for Crop Plant Research (IZN).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ralf Horbach .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Horbach, R., Deising, H.B. (2013). 13 The Biotrophy–Necrotrophy Switch in Fungal Pathogenesis. In: Kempken, F. (eds) Agricultural Applications. The Mycota, vol 11. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-36821-9_13

Download citation

Publish with us

Policies and ethics