An oomycete NLP cytolysin forms transient small pores in lipid membranes

Author:

Pirc Katja1ORCID,Clifton Luke A.2ORCID,Yilmaz Neval3,Saltalamacchia Andrea4,Mally Mojca5ORCID,Snoj Tina1,Žnidaršič Nada6,Srnko Marija1ORCID,Borišek Jure7ORCID,Parkkila Petteri89ORCID,Albert Isabell1011ORCID,Podobnik Marjetka1ORCID,Numata Keiji3ORCID,Nürnberger Thorsten1012,Viitala Tapani813ORCID,Derganc Jure514,Magistrato Alessandra415ORCID,Lakey Jeremy H.16ORCID,Anderluh Gregor1ORCID

Affiliation:

1. Department of Molecular Biology and Nanobiotechnology, National Institute of Chemistry, 1000 Ljubljana, Slovenia.

2. ISIS Pulsed Neutron and Muon Source, Science and Technology Facilities Council, Rutherford Appleton Laboratory, Harwell Science and Innovation Campus, Didcot, Oxfordshire, Oxford OX11 OQX, UK.

3. Biomacromolecules Research Team, RIKEN Center for Sustainable Resource Science, Wako, Saitama 351-0198, Japan.

4. International School for Advanced Studies (SISSA/ISAS), 34136 Trieste, Italy.

5. Institute of Biophysics, Faculty of Medicine, University of Ljubljana, 1000 Ljubljana, Slovenia.

6. Department of Biology, Biotechnical Faculty, University of Ljubljana, 1000 Ljubljana, Slovenia.

7. Theory Department, National Institute of Chemistry, 1000 Ljubljana, Slovenia.

8. Drug Research Program, Division of Pharmaceutical Biosciences, Faculty of Pharmacy, University of Helsinki, 00014 Helsinki, Finland.

9. Department of Physics, Chalmers University of Technology, SE-412 96 Gothenburg, Sweden.

10. Center of Plant Molecular Biology (ZMBP), Eberhard-Karls-University Tübingen, Tübingen, Germany.

11. Molecular Plant Physiology, FAU Erlangen-Nuremberg, 91058 Erlangen, Germany.

12. Department of Biochemistry, University of Johannesburg, Auckland Park, Johannesburg, South Africa.

13. Drug Research Program, Division of Pharmaceutical Chemistry and Technology, Faculty of Pharmacy, University of Helsinki, 00014 Helsinki, Finland.

14. Chair of Microprocess Engineering and Technology—COMPETE, University of Ljubljana, 1000 Ljubljana, Slovenia.

15. National Research Council Institute of Material (CNR-IOM), 34136 Trieste, Italy.

16. Biosciences Institute, Newcastle University, Newcastle upon Tyne NE2 4HH, UK.

Abstract

Microbial plant pathogens secrete a range of effector proteins that damage host plants and consequently constrain global food production. Necrosis and ethylene-inducing peptide 1–like proteins (NLPs) are produced by numerous phytopathogenic microbes that cause important crop diseases. Many NLPs are cytolytic, causing cell death and tissue necrosis by disrupting the plant plasma membrane. Here, we reveal the unique molecular mechanism underlying the membrane damage induced by the cytotoxic model NLP. This membrane disruption is a multistep process that includes electrostatic-driven, plant-specific lipid recognition, shallow membrane binding, protein aggregation, and transient pore formation. The NLP-induced damage is not caused by membrane reorganization or large-scale defects but by small membrane ruptures. This distinct mechanism of lipid membrane disruption is highly adapted to effectively damage plant cells.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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