title: Sequential delivery of host-induced virulence effectors by appressoria and intracellular hyphae of the phytopathogen Colletotrichum higginsianum.
abstract: Phytopathogens secrete effector proteins to manipulate their hosts for effective colonization. Hemibiotrophic fungi must maintain host viability during initial biotrophic growth and elicit host death for subsequent necrotrophic growth. To identify effectors mediating these opposing processes, we deeply sequenced the transcriptome of Colletotrichum higginsianum infecting Arabidopsis. Most effector genes are host-induced and expressed in consecutive waves associated with pathogenic transitions, indicating distinct effector suites are deployed at each stage. Using fluorescent protein tagging and transmission electron microscopy-immunogold labelling, we found effectors localised to stage-specific compartments at the host-pathogen interface. In particular, we show effectors are focally secreted from appressorial penetration pores before host invasion, revealing new levels of functional complexity for this fungal organ. Furthermore, we demonstrate that antagonistic effectors either induce or suppress plant cell death. Based on these results we conclude that hemibiotrophy in Colletotrichum is orchestrated through the coordinated expression of antagonistic effectors supporting either cell viability or cell death.
authors.affiliation: Department of Plant-Microbe Interactions, Max-Planck-Institute for Plant Breeding Research, Cologne, Germany.
authors.forename: Jochen
authors.initials: J
authors.lastname: Kleemann
authors.forename: Linda J
authors.initials: LJ
authors.lastname: Rincon-Rivera
authors.forename: Hiroyuki
authors.initials: H
authors.lastname: Takahara
authors.forename: Ulla
authors.initials: U
authors.lastname: Neumann
authors.forename: E
authors.initials: E
authors.lastname: Ver Loren van Themaat
authors.forename: Emiel Ver Loren
authors.initials: EV
authors.lastname: van Themaat
authors.forename: H Charlotte
authors.initials: HC
authors.lastname: van der Does
authors.forename: Stéphane
authors.initials: S
authors.lastname: Hacquard
authors.forename: Kurt
authors.initials: K
authors.lastname: Stüber
authors.forename: Isa
authors.initials: I
authors.lastname: Will
authors.forename: Wolfgang
authors.initials: W
authors.lastname: Schmalenbach
authors.forename: Elmon
authors.initials: E
authors.lastname: Schmelzer
authors.forename: Richard J
authors.initials: RJ
authors.lastname: O'Connell
mesh_terms: D017360:Arabidopsis / Q000378:metabolism / Q000382:microbiology* / Q000648:ultrastructure; D020231:Colletotrichum / Q000378:metabolism* / Q000472:pathogenicity* / Q000648:ultrastructure; D015966:Gene Expression Regulation, Fungal / Q000502:physiology; D025301:Hyphae / Q000378:metabolism* / Q000472:pathogenicity* / Q000648:ultrastructure; D010935:Plant Diseases / Q000382:microbiology*; D059467:Transcriptome / Q000502:physiology; D037521:Virulence Factors / Q000096:biosynthesis*
chemical_list: D037521:Virulence Factors