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Cited by 43Plant-Microbe Interactions and ImmunityPlant pathogens and resistance mechanismsPlant Pathogens and Fungal Diseases

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Botrytis hypersensitive response inducing protein 1 triggers noncanonical PTI to induce plant cell death

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Jeblick, Tanja, Leisen, Thomas, Steidele, Christina E, Albert, Isabell, Müller, Jonas, Kaiser, Sabrina, Mahler, Florian, Sommer, Frederik, Keller, Sandro, Hückelhoven, Ralph, Hahn, Matthias, Scheuring, David·2023·Plant Physiology
DOI 10.1093/plphys/kiac476PMC PMC9806589

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Abstract

According to their lifestyle, plant pathogens are divided into biotrophic and necrotrophic organisms. Biotrophic pathogens exclusively nourish living host cells, whereas necrotrophic pathogens rapidly kill host cells and nourish cell walls and cell contents. To this end, the necrotrophic fungus Botrytis cinerea secretes large amounts of phytotoxic proteins and cell wall-degrading enzymes. However, the precise role of these proteins during infection is unknown. Here, we report on the identification and characterization of the previously unknown toxic protein hypersensitive response-inducing protein 1 (Hip1), which induces plant cell death. We found the adoption of a structurally conserved folded Alternaria alternata Alt a 1 protein structure to be a prerequisite for Hip1 to exert its necrosis-inducing activity in a host-specific manner. Localization and the induction of typical plant defense responses by Hip1 indicate recognition as a pathogen-associated molecular pattern at the plant plasma membrane. In contrast to other secreted toxic Botrytis proteins, the activity of Hip1 does not depend on the presence of the receptor-associated kinases BRI1-associated kinase 1 and suppressor of BIR1-1. Our results demonstrate that recognition of Hip1, even in the absence of obvious enzymatic or pore-forming activity, induces strong plant defense reactions eventually leading to plant cell death. Botrytis hip1 overexpression strains generated by CRISPR/Cas9 displayed enhanced infection, indicating the virulence-promoting potential of Hip1. Taken together, Hip1 induces a noncanonical defense response which might be a common feature of structurally conserved fungal proteins from the Alt a 1 family.

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Metadata

Authors
Jeblick, T., Leisen, T., Steidele, C. E., Albert, I., Müller, J., Kaiser, S., Mahler, F., Sommer, F., Keller, S., Hückelhoven, R., Hahn, M., & Scheuring, D.
Affiliations
  • University of Kaiserslautern (DE)
  • Technical University of Munich (DE)
  • Friedrich-Alexander-Universität Erlangen-Nürnberg (DE)
Corresponding author
Scheuring, David
ORCID
Venue
Plant Physiology
Publisher
Oxford University Press (OUP)
Published
2022-10-12
Volume
191
Issue
1
Pages
125-141
ISSN
  • 0032-0889 (ISSN-L)
  • 1532-2548
DOI
10.1093/plphys/kiac476
PMC
PMC9806589
OpenAlex
W4304758064
Cited by
43
References
3
Citations by year
2026: 7 · 2025: 12 · 2024: 12 · 2023: 10
FWCI
4.68
Type
journal article
Language
en
Open access
Licence
Locations
  • PLANT PHYSIOLOGY (publishedVersion, cc-by-nc-nd)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • mediaTUM – the media and publications repository of the Technical University Munich (Technical University Munich) (submittedVersion)
  • mediaTUM – the media and publications repository of the Technical University Munich (Technical University Munich) (submittedVersion, other-oa)
Funders
  • University of Kaiserslautern
  • DFG (SCHE 1836/4-1, SCHE 1836/5-1)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant pathogens and resistance mechanisms
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Pathogens and Fungal Diseases
Keywords
Botrytis cinerea, HIP1, plant cell death, necrotrophic fungal pathogen, plant defense response, fungal virulence
MeSH terms
Cell Membrane, Plant Diseases, Virulence, Cell Death, Gene Expression Regulation, Plant, Botrytis, Plant Cells

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