title: Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments.
abstract: Many fungal parasites enter plant cells by penetrating the host cell wall and, thereafter, differentiate specialized intracellular feeding structures, called haustoria, by invagination of the plant's plasma membrane. Arabidopsis PEN gene products are known to act at the cell periphery and function in the execution of apoplastic immune responses to limit fungal entry. This response underneath fungal contact sites is tightly linked with the deposition of plant cell wall polymers, including PMR4/GSL5-dependent callose, in the paramural space, thereby producing localized wall thickenings called papillae. We show that powdery mildew fungi specifically induce the extracellular transport and entrapment of the fusion protein GFP-PEN1 syntaxin and its interacting partner monomeric yellow fluorescent protein (mYFP)-SNAP33 within the papillary matrix. Remarkably, PMR4/GSL5 callose, GFP-PEN1, mYFP-SNAP33, and the ABC transporter GFP-PEN3 are selectively incorporated into extracellular encasements surrounding haustoria of the powdery mildew Golovinomyces orontii, suggesting that the same secretory defense responses become activated during the formation of papillae and haustorial encasements. This is consistent with a time-course analysis of the encasement process, indicating that these extracellular structures are generated through the extension of papillae. We show that PMR4/GSL5 callose accumulation in papillae and haustorial encasements occurs independently of PEN1 syntaxin. We propose a model in which exosome biogenesis/release serves as a common transport mechanism by which the proteins PEN1 and PEN3, otherwise resident in the plasma membrane, together with membrane lipids, become stably incorporated into both pathogen-induced cell wall compartments.
authors.affiliation: Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research-Cologne, Carl-von-Linné-Weg 10, Köln, Germany.
authors.forename: Dorit
authors.initials: D
authors.lastname: Meyer
authors.forename: Simone
authors.initials: S
authors.lastname: Pajonk
authors.forename: Cristina
authors.initials: C
authors.lastname: Micali
authors.forename: Richard
authors.initials: R
authors.lastname: O'Connell
authors.forename: Paul
authors.initials: P
authors.lastname: Schulze-Lefert
mesh_terms: D017360:Arabidopsis / Q000378:metabolism* / Q000382:microbiology; D029681:Arabidopsis Proteins / Q000378:metabolism*; D001203:Ascomycota / Q000502:physiology*; D002473:Cell Wall / Q000378:metabolism* / Q000382:microbiology; D005936:Glucans / Q000378:metabolism; D005964:Glucosyltransferases / Q000378:metabolism; D018613:Microscopy, Confocal; D019441:Plant Epidermis / Q000166:cytology / Q000382:microbiology; D021381:Protein Transport; D050765:Qa-SNARE Proteins / Q000378:metabolism*; D050766:Qb-SNARE Proteins / Q000378:metabolism; D050767:Qc-SNARE Proteins / Q000378:metabolism; D022161:Transport Vesicles / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; D005936:Glucans; C479425:PEN1 protein, Arabidopsis; D050765:Qa-SNARE Proteins; D050766:Qb-SNARE Proteins; D050767:Qc-SNARE Proteins; C439366:SNAP33 protein, Arabidopsis; C048306:callose; D005964:Glucosyltransferases; C020570:1,3-beta-glucan synthase