title: The mutualistic fungus Piriformospora indica colonizes Arabidopsis roots by inducing an endoplasmic reticulum stress-triggered caspase-dependent cell death.
abstract: In Arabidopsis thaliana roots, the mutualistic fungus Piriformospora indica initially colonizes living cells, which die as the colonization proceeds. We aimed to clarify the molecular basis of this colonization-associated cell death. Our cytological analyses revealed endoplasmic reticulum (ER) swelling and vacuolar collapse in invaded cells, indicative of ER stress and cell death during root colonization. Consistent with this, P. indica-colonized plants were hypersensitive to the ER stress inducer tunicamycin. By clear contrast, ER stress sensors bZIP60 and bZIP28 as well as canonical markers for the ER stress response pathway, termed the unfolded protein response (UPR), were suppressed at the same time. Arabidopsis mutants compromised in caspase 1-like activity, mediated by cell death-regulating vacuolar processing enzymes (VPEs), showed reduced colonization and decreased cell death incidence. We propose a previously unreported microbial invasion strategy during which P. indica induces ER stress but inhibits the adaptive UPR. This disturbance results in a VPE/caspase 1-like-mediated cell death, which is required for the establishment of the symbiosis. Our results suggest the presence of an at least partially conserved ER stress-induced caspase-dependent cell death pathway in plants as has been reported for metazoans.
authors.affiliation: Research Centre for Biosystems, Land Use, and Nutrition, Justus Liebig University, 35392 Giessen, Germany.
authors.forename: Xiaoyu
authors.initials: X
authors.lastname: Qiang
authors.forename: Bernd
authors.initials: B
authors.lastname: Zechmann
authors.forename: Marco U
authors.initials: MU
authors.lastname: Reitz
authors.forename: Karl-Heinz
authors.initials: KH
authors.lastname: Kogel
authors.forename: Patrick
authors.initials: P
authors.lastname: Schäfer
mesh_terms: D017360:Arabidopsis / Q000166:cytology* / Q000235:genetics / Q000382:microbiology; D029681:Arabidopsis Proteins / Q000378:metabolism; D050976:Basic-Leucine Zipper Transcription Factors / Q000378:metabolism; D001487:Basidiomycota / Q000502:physiology*; D020169:Caspases / Q000378:metabolism; D016923:Cell Death; D004721:Endoplasmic Reticulum / Q000382:microbiology; D059865:Endoplasmic Reticulum Stress; D018506:Gene Expression Regulation, Plant; D008969:Molecular Sequence Data; D018517:Plant Roots / Q000382:microbiology*; D013559:Symbiosis; D014415:Tunicamycin / Q000494:pharmacology; D056811:Unfolded Protein Response; D014617:Vacuoles / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; D050976:Basic-Leucine Zipper Transcription Factors; C530495:bZIP28 protein, Arabidopsis; C533092:bZIP60 protein, Arabidopsis; D014415:Tunicamycin; D020169:Caspases