Apoplastic venom allergen-like proteins of plant-parasitic nematodes modulate the activation of plant innate immunity by cell surface receptors

J.L. Lozano Torres, R.H.P. Wilbers, S. Warmerdam, K. Varossieau, J. Willig, C.C. van Schaik, Oluwatoyin A. Asojo, Rabih Darwiche, Roger Schneiter, Claire Drurey, Rick M. Maizels, A. Goverse, A. Schots, G. Smant

Research output: Contribution to conferenceAbstractAcademic

Abstract

Despite causing considerable damage to host tissue during parasitism, nematodes establish persistent infections in both animals and plants. An elaborate repertoire of nematode effectors modulates damage-triggered immune responses of the host. However, the nature and mode of action of most of nematode immunomodulatory compounds is not well understood. We discovered that the nematode effectors named the venom allergen-like proteins (VAPs) selectively suppress host immunity during the onset of parasitism in plants. VAPs are uniquely conserved in secretions of all animal- and plant-parasitic nematodes, but their role in parasitism has remained elusive. Knocking-down the expression of Gr-VAP1 hampered the infectivity of the potato cyst nematode Globodera rostochiensis. By contrast, heterologous expression of Gr-VAP1 and VAPs from the beet cyst nematode Heterodera schachtii, in Arabidopsis, resulted in the loss of basal immunity to multiple pathogens. Surprisingly, VAPs only affect the defence responses mediated by surface-localised immune receptors. The modulation of basal immunity by ectopic expression of VAPs involves extracellular protease-based host defences and jasmonic acid responses. Crystal structures of VAPs revealed lipid binding motifs. In these cavities VAPs can bind palmitate and sterol both in vitro and in vivo. The delivery of VAPs into host tissue coincides with large modifications in the extracellular matrix by migratory nematodes. We, therefore, conclude that parasitic nematodes most likely utilise VAPs to suppress the activation of defences by immunogenic breakdown products in damaged host tissue.
Original languageEnglish
Publication statusPublished - 13 Sep 2018
EventESN Conference 2018 - Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium
Duration: 9 Sep 201813 Sep 2018

Conference

ConferenceESN Conference 2018
CountryBelgium
CityGhent
Period9/09/1813/09/18

Fingerprint

venoms
plant parasitic nematodes
allergens
receptors
Nematoda
proteins
cells
parasitism
cyst nematodes
immunity
Heterodera schachtii
animal parasitic nematodes
innate immunity
Globodera rostochiensis
palmitates
beets
jasmonic acid
crystal structure
extracellular matrix
sterols

Cite this

@conference{7b9ee8fa9f884376b27cbddf0495c5a2,
title = "Apoplastic venom allergen-like proteins of plant-parasitic nematodes modulate the activation of plant innate immunity by cell surface receptors",
abstract = "Despite causing considerable damage to host tissue during parasitism, nematodes establish persistent infections in both animals and plants. An elaborate repertoire of nematode effectors modulates damage-triggered immune responses of the host. However, the nature and mode of action of most of nematode immunomodulatory compounds is not well understood. We discovered that the nematode effectors named the venom allergen-like proteins (VAPs) selectively suppress host immunity during the onset of parasitism in plants. VAPs are uniquely conserved in secretions of all animal- and plant-parasitic nematodes, but their role in parasitism has remained elusive. Knocking-down the expression of Gr-VAP1 hampered the infectivity of the potato cyst nematode Globodera rostochiensis. By contrast, heterologous expression of Gr-VAP1 and VAPs from the beet cyst nematode Heterodera schachtii, in Arabidopsis, resulted in the loss of basal immunity to multiple pathogens. Surprisingly, VAPs only affect the defence responses mediated by surface-localised immune receptors. The modulation of basal immunity by ectopic expression of VAPs involves extracellular protease-based host defences and jasmonic acid responses. Crystal structures of VAPs revealed lipid binding motifs. In these cavities VAPs can bind palmitate and sterol both in vitro and in vivo. The delivery of VAPs into host tissue coincides with large modifications in the extracellular matrix by migratory nematodes. We, therefore, conclude that parasitic nematodes most likely utilise VAPs to suppress the activation of defences by immunogenic breakdown products in damaged host tissue.",
author = "{Lozano Torres}, J.L. and R.H.P. Wilbers and S. Warmerdam and K. Varossieau and J. Willig and {van Schaik}, C.C. and Asojo, {Oluwatoyin A.} and Rabih Darwiche and Roger Schneiter and Claire Drurey and Maizels, {Rick M.} and A. Goverse and A. Schots and G. Smant",
year = "2018",
month = "9",
day = "13",
language = "English",
note = "ESN Conference 2018 ; Conference date: 09-09-2018 Through 13-09-2018",

}

Apoplastic venom allergen-like proteins of plant-parasitic nematodes modulate the activation of plant innate immunity by cell surface receptors. / Lozano Torres, J.L.; Wilbers, R.H.P.; Warmerdam, S.; Varossieau, K.; Willig, J.; van Schaik, C.C.; Asojo, Oluwatoyin A.; Darwiche, Rabih; Schneiter, Roger; Drurey, Claire; Maizels, Rick M.; Goverse, A.; Schots, A.; Smant, G.

2018. Abstract from ESN Conference 2018, Ghent, Belgium.

Research output: Contribution to conferenceAbstractAcademic

TY - CONF

T1 - Apoplastic venom allergen-like proteins of plant-parasitic nematodes modulate the activation of plant innate immunity by cell surface receptors

AU - Lozano Torres, J.L.

AU - Wilbers, R.H.P.

AU - Warmerdam, S.

AU - Varossieau, K.

AU - Willig, J.

AU - van Schaik, C.C.

AU - Asojo, Oluwatoyin A.

AU - Darwiche, Rabih

AU - Schneiter, Roger

AU - Drurey, Claire

AU - Maizels, Rick M.

AU - Goverse, A.

AU - Schots, A.

AU - Smant, G.

PY - 2018/9/13

Y1 - 2018/9/13

N2 - Despite causing considerable damage to host tissue during parasitism, nematodes establish persistent infections in both animals and plants. An elaborate repertoire of nematode effectors modulates damage-triggered immune responses of the host. However, the nature and mode of action of most of nematode immunomodulatory compounds is not well understood. We discovered that the nematode effectors named the venom allergen-like proteins (VAPs) selectively suppress host immunity during the onset of parasitism in plants. VAPs are uniquely conserved in secretions of all animal- and plant-parasitic nematodes, but their role in parasitism has remained elusive. Knocking-down the expression of Gr-VAP1 hampered the infectivity of the potato cyst nematode Globodera rostochiensis. By contrast, heterologous expression of Gr-VAP1 and VAPs from the beet cyst nematode Heterodera schachtii, in Arabidopsis, resulted in the loss of basal immunity to multiple pathogens. Surprisingly, VAPs only affect the defence responses mediated by surface-localised immune receptors. The modulation of basal immunity by ectopic expression of VAPs involves extracellular protease-based host defences and jasmonic acid responses. Crystal structures of VAPs revealed lipid binding motifs. In these cavities VAPs can bind palmitate and sterol both in vitro and in vivo. The delivery of VAPs into host tissue coincides with large modifications in the extracellular matrix by migratory nematodes. We, therefore, conclude that parasitic nematodes most likely utilise VAPs to suppress the activation of defences by immunogenic breakdown products in damaged host tissue.

AB - Despite causing considerable damage to host tissue during parasitism, nematodes establish persistent infections in both animals and plants. An elaborate repertoire of nematode effectors modulates damage-triggered immune responses of the host. However, the nature and mode of action of most of nematode immunomodulatory compounds is not well understood. We discovered that the nematode effectors named the venom allergen-like proteins (VAPs) selectively suppress host immunity during the onset of parasitism in plants. VAPs are uniquely conserved in secretions of all animal- and plant-parasitic nematodes, but their role in parasitism has remained elusive. Knocking-down the expression of Gr-VAP1 hampered the infectivity of the potato cyst nematode Globodera rostochiensis. By contrast, heterologous expression of Gr-VAP1 and VAPs from the beet cyst nematode Heterodera schachtii, in Arabidopsis, resulted in the loss of basal immunity to multiple pathogens. Surprisingly, VAPs only affect the defence responses mediated by surface-localised immune receptors. The modulation of basal immunity by ectopic expression of VAPs involves extracellular protease-based host defences and jasmonic acid responses. Crystal structures of VAPs revealed lipid binding motifs. In these cavities VAPs can bind palmitate and sterol both in vitro and in vivo. The delivery of VAPs into host tissue coincides with large modifications in the extracellular matrix by migratory nematodes. We, therefore, conclude that parasitic nematodes most likely utilise VAPs to suppress the activation of defences by immunogenic breakdown products in damaged host tissue.

M3 - Abstract

ER -