An oomycete NLP cytolysin forms transient small pores in lipid membranes

Katja Pirc; Luke A. Clifton; Neval Yilmaz; Andrea Saltalamacchia; Mojca Mally; Tina Snoj; Nada Žnidaršič; Marija Srnko; Jure Borišek; Petteri Parkkila; Isabell Albert; Marjetka Podobnik; Keiji Numata; Thorsten Nürnberger; Tapani Viitala; Jure Derganc; Alessandra Magistrato; Jeremy H. Lakey; Gregor Anderluh

doi:10.1126/sciadv.abj9406

An oomycete NLP cytolysin forms transient small pores in lipid membranes

Katja Pirc, Luke A. Clifton, Neval Yilmaz, Andrea Saltalamacchia, Mojca Mally, Tina Snoj, Nada Žnidaršič, Marija Srnko, Jure Borišek, Petteri Parkkila, Isabell Albert, Marjetka Podobnik, Keiji Numata, Thorsten Nürnberger, Tapani Viitala, Jure Derganc, Alessandra Magistrato, Jeremy H. Lakey, Gregor Anderluh^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Scientific › peer-review

13 Citations (Scopus)

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.

Original language	English
Article number	eabj9406
Journal	Science Advances
Volume	8
Issue number	10
DOIs	https://doi.org/10.1126/sciadv.abj9406
Publication status	Published - Mar 2022
Externally published	Yes
MoE publication type	A1 Journal article-refereed

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Pirc, K., Clifton, L. A., Yilmaz, N., Saltalamacchia, A., Mally, M., Snoj, T., Žnidaršič, N., Srnko, M., Borišek, J., Parkkila, P., Albert, I., Podobnik, M., Numata, K., Nürnberger, T., Viitala, T., Derganc, J., Magistrato, A., Lakey, J. H., & Anderluh, G. (2022). An oomycete NLP cytolysin forms transient small pores in lipid membranes. Science Advances, 8(10), Article eabj9406. https://doi.org/10.1126/sciadv.abj9406

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title = "An oomycete NLP cytolysin forms transient small pores in lipid membranes",

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.",

author = "Katja Pirc and Clifton, {Luke A.} and Neval Yilmaz and Andrea Saltalamacchia and Mojca Mally and Tina Snoj and Nada {\v Z}nidar{\v s}i{\v c} and Marija Srnko and Jure Bori{\v s}ek and Petteri Parkkila and Isabell Albert and Marjetka Podobnik and Keiji Numata and Thorsten N{\"u}rnberger and Tapani Viitala and Jure Derganc and Alessandra Magistrato and Lakey, {Jeremy H.} and Gregor Anderluh",

note = "Publisher Copyright: Copyright {\textcopyright} 2022 The Authors,",

year = "2022",

month = mar,

doi = "10.1126/sciadv.abj9406",

language = "English",

volume = "8",

journal = "Science Advances",

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Pirc, K, Clifton, LA, Yilmaz, N, Saltalamacchia, A, Mally, M, Snoj, T, Žnidaršič, N, Srnko, M, Borišek, J, Parkkila, P, Albert, I, Podobnik, M, Numata, K, Nürnberger, T, Viitala, T, Derganc, J, Magistrato, A, Lakey, JH & Anderluh, G 2022, 'An oomycete NLP cytolysin forms transient small pores in lipid membranes', Science Advances, vol. 8, no. 10, eabj9406. https://doi.org/10.1126/sciadv.abj9406

TY - JOUR

T1 - An oomycete NLP cytolysin forms transient small pores in lipid membranes

AU - Pirc, Katja

AU - Clifton, Luke A.

AU - Yilmaz, Neval

AU - Saltalamacchia, Andrea

AU - Mally, Mojca

AU - Snoj, Tina

AU - Žnidaršič, Nada

AU - Srnko, Marija

AU - Borišek, Jure

AU - Parkkila, Petteri

AU - Albert, Isabell

AU - Podobnik, Marjetka

AU - Numata, Keiji

AU - Nürnberger, Thorsten

AU - Viitala, Tapani

AU - Derganc, Jure

AU - Magistrato, Alessandra

AU - Lakey, Jeremy H.

AU - Anderluh, Gregor

PY - 2022/3

Y1 - 2022/3

N2 - 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.

AB - 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.

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DO - 10.1126/sciadv.abj9406

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C2 - 35275729

AN - SCOPUS:85126389855

SN - 2375-2548

VL - 8

JO - Science Advances

JF - Science Advances

IS - 10

M1 - eabj9406

ER -

An oomycete NLP cytolysin forms transient small pores in lipid membranes

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