Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential.

The root knot nematode, Meloidogyne incognita, is an obligate parasite that causes significant damage to a broad range of host plants. Infection is associated with secretion of proteins surrounded by proliferating cells. Many parasites are known to secrete effectors that interfere with plant innate...

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Main Authors: Stéphane Bellafiore, Zhouxin Shen, Marie-Noelle Rosso, Pierre Abad, Patrick Shih, Steven P Briggs
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2008-10-01
Series:PLoS Pathogens
Online Access:http://europepmc.org/articles/PMC2568823?pdf=render
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spelling doaj-119422b576114aa780205168d40767102020-11-24T23:58:44ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742008-10-01410e100019210.1371/journal.ppat.1000192Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential.Stéphane BellafioreZhouxin ShenMarie-Noelle RossoPierre AbadPatrick ShihSteven P BriggsThe root knot nematode, Meloidogyne incognita, is an obligate parasite that causes significant damage to a broad range of host plants. Infection is associated with secretion of proteins surrounded by proliferating cells. Many parasites are known to secrete effectors that interfere with plant innate immunity, enabling infection to occur; they can also release pathogen-associated molecular patterns (PAMPs, e.g., flagellin) that trigger basal immunity through the nematode stylet into the plant cell. This leads to suppression of innate immunity and reprogramming of plant cells to form a feeding structure containing multinucleate giant cells. Effectors have generally been discovered using genetics or bioinformatics, but M. incognita is non-sexual and its genome sequence has not yet been reported. To partially overcome these limitations, we have used mass spectrometry to directly identify 486 proteins secreted by M. incognita. These proteins contain at least segmental sequence identity to those found in our 3 reference databases (published nematode proteins; unpublished M. incognita ESTs; published plant proteins). Several secreted proteins are homologous to plant proteins, which they may mimic, and they contain domains that suggest known effector functions (e.g., regulating the plant cell cycle or growth). Others have regulatory domains that could reprogram cells. Using in situ hybridization we observed that most secreted proteins were produced by the subventral glands, but we found that phasmids also secreted proteins. We annotated the functions of the secreted proteins and classified them according to roles they may play in the development of root knot disease. Our results show that parasite secretomes can be partially characterized without cognate genomic DNA sequence. We observed that the M. incognita secretome overlaps the reported secretome of mammalian parasitic nematodes (e.g., Brugia malayi), suggesting a common parasitic behavior and a possible conservation of function between metazoan parasites of plants and animals.http://europepmc.org/articles/PMC2568823?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Stéphane Bellafiore
Zhouxin Shen
Marie-Noelle Rosso
Pierre Abad
Patrick Shih
Steven P Briggs
spellingShingle Stéphane Bellafiore
Zhouxin Shen
Marie-Noelle Rosso
Pierre Abad
Patrick Shih
Steven P Briggs
Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential.
PLoS Pathogens
author_facet Stéphane Bellafiore
Zhouxin Shen
Marie-Noelle Rosso
Pierre Abad
Patrick Shih
Steven P Briggs
author_sort Stéphane Bellafiore
title Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential.
title_short Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential.
title_full Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential.
title_fullStr Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential.
title_full_unstemmed Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential.
title_sort direct identification of the meloidogyne incognita secretome reveals proteins with host cell reprogramming potential.
publisher Public Library of Science (PLoS)
series PLoS Pathogens
issn 1553-7366
1553-7374
publishDate 2008-10-01
description The root knot nematode, Meloidogyne incognita, is an obligate parasite that causes significant damage to a broad range of host plants. Infection is associated with secretion of proteins surrounded by proliferating cells. Many parasites are known to secrete effectors that interfere with plant innate immunity, enabling infection to occur; they can also release pathogen-associated molecular patterns (PAMPs, e.g., flagellin) that trigger basal immunity through the nematode stylet into the plant cell. This leads to suppression of innate immunity and reprogramming of plant cells to form a feeding structure containing multinucleate giant cells. Effectors have generally been discovered using genetics or bioinformatics, but M. incognita is non-sexual and its genome sequence has not yet been reported. To partially overcome these limitations, we have used mass spectrometry to directly identify 486 proteins secreted by M. incognita. These proteins contain at least segmental sequence identity to those found in our 3 reference databases (published nematode proteins; unpublished M. incognita ESTs; published plant proteins). Several secreted proteins are homologous to plant proteins, which they may mimic, and they contain domains that suggest known effector functions (e.g., regulating the plant cell cycle or growth). Others have regulatory domains that could reprogram cells. Using in situ hybridization we observed that most secreted proteins were produced by the subventral glands, but we found that phasmids also secreted proteins. We annotated the functions of the secreted proteins and classified them according to roles they may play in the development of root knot disease. Our results show that parasite secretomes can be partially characterized without cognate genomic DNA sequence. We observed that the M. incognita secretome overlaps the reported secretome of mammalian parasitic nematodes (e.g., Brugia malayi), suggesting a common parasitic behavior and a possible conservation of function between metazoan parasites of plants and animals.
url http://europepmc.org/articles/PMC2568823?pdf=render
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