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Fatty Acid-and Retinol-Binding Protein, Mj-FAR-1 Induces Tomato Host Susceptibility to Root-Knot Nematodes

Plant-parasitic nematodes produce at least one structurally unique class of small helix-rich retinol- and fatty-acid-binding proteins that have no counterparts in their plant hosts. Herein we describe a protein of the plant-parasitic root-knot nematode Meloidogyne javanica, which is a member of the...

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Autores principales: Iberkleid, Ionit, Vieira, Paulo, de Almeida Engler, Janice, Firester, Kalia, Spiegel, Yitzhak, Horowitz, Sigal Brown
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3661543/
https://www.ncbi.nlm.nih.gov/pubmed/23717636
http://dx.doi.org/10.1371/journal.pone.0064586
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author Iberkleid, Ionit
Vieira, Paulo
de Almeida Engler, Janice
Firester, Kalia
Spiegel, Yitzhak
Horowitz, Sigal Brown
author_facet Iberkleid, Ionit
Vieira, Paulo
de Almeida Engler, Janice
Firester, Kalia
Spiegel, Yitzhak
Horowitz, Sigal Brown
author_sort Iberkleid, Ionit
collection PubMed
description Plant-parasitic nematodes produce at least one structurally unique class of small helix-rich retinol- and fatty-acid-binding proteins that have no counterparts in their plant hosts. Herein we describe a protein of the plant-parasitic root-knot nematode Meloidogyne javanica, which is a member of the nematode-specific fatty-acid- and retinol-binding (Mj-FAR-1) family of proteins. The mj-far-1 mRNA was detected through M. javanica pre-parasitic J2s, migratory and sedentary parasitic stages by quantitative reverse transcriptase polymerase chain reaction (qRT-PCR). Immunolocalization assays demonstrate that the FAR protein of Meloidogyne is secreted during sedentary stages, as evidenced by the accumulation of FAR at the nematode cuticle surface and along the adjacent host root tissues. Tomato roots constitutively expressing mj-far-1 demonstrated an increased susceptibility to root-knot nematodes infection as observed by accelerated gall induction and expansion, accompanied by a higher percentage of nematodes developing into mature females compared to control roots. RNA interference assays that expressed double-stranded RNA complementary to mj-far-1 in transgenic tomato lines specifically reduced nematode infection levels. Histological analysis of nematode-infested roots indicated that in roots overexpressing mj-far-1, galls contained larger feeding cells and might support a faster nematode development and maturation. Roots overexpressing mj-far-1 suppressed jasmonic acid responsive genes such as the proteinase inhibitor (Pin2) and γ-thionin, illustrating the possible role of Mj-FAR-1 in manipulating the lipid based signaling in planta. This data, suggests that Meloidogyne FAR might have a strategic function during the interaction of the nematode with its plant host. Our study present the first demonstration of an in planta functional characterization and localization of FAR proteins secreted by plant-parasitic nematodes. It provides evidence that Mj-FAR-1 facilitates infection most likely via the manipulation of host lipid-based defenses, as critical components for a successful parasitism by plant-parasitic nematodes.
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spelling pubmed-36615432013-05-28 Fatty Acid-and Retinol-Binding Protein, Mj-FAR-1 Induces Tomato Host Susceptibility to Root-Knot Nematodes Iberkleid, Ionit Vieira, Paulo de Almeida Engler, Janice Firester, Kalia Spiegel, Yitzhak Horowitz, Sigal Brown PLoS One Research Article Plant-parasitic nematodes produce at least one structurally unique class of small helix-rich retinol- and fatty-acid-binding proteins that have no counterparts in their plant hosts. Herein we describe a protein of the plant-parasitic root-knot nematode Meloidogyne javanica, which is a member of the nematode-specific fatty-acid- and retinol-binding (Mj-FAR-1) family of proteins. The mj-far-1 mRNA was detected through M. javanica pre-parasitic J2s, migratory and sedentary parasitic stages by quantitative reverse transcriptase polymerase chain reaction (qRT-PCR). Immunolocalization assays demonstrate that the FAR protein of Meloidogyne is secreted during sedentary stages, as evidenced by the accumulation of FAR at the nematode cuticle surface and along the adjacent host root tissues. Tomato roots constitutively expressing mj-far-1 demonstrated an increased susceptibility to root-knot nematodes infection as observed by accelerated gall induction and expansion, accompanied by a higher percentage of nematodes developing into mature females compared to control roots. RNA interference assays that expressed double-stranded RNA complementary to mj-far-1 in transgenic tomato lines specifically reduced nematode infection levels. Histological analysis of nematode-infested roots indicated that in roots overexpressing mj-far-1, galls contained larger feeding cells and might support a faster nematode development and maturation. Roots overexpressing mj-far-1 suppressed jasmonic acid responsive genes such as the proteinase inhibitor (Pin2) and γ-thionin, illustrating the possible role of Mj-FAR-1 in manipulating the lipid based signaling in planta. This data, suggests that Meloidogyne FAR might have a strategic function during the interaction of the nematode with its plant host. Our study present the first demonstration of an in planta functional characterization and localization of FAR proteins secreted by plant-parasitic nematodes. It provides evidence that Mj-FAR-1 facilitates infection most likely via the manipulation of host lipid-based defenses, as critical components for a successful parasitism by plant-parasitic nematodes. Public Library of Science 2013-05-22 /pmc/articles/PMC3661543/ /pubmed/23717636 http://dx.doi.org/10.1371/journal.pone.0064586 Text en © 2013 Iberkleid et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Iberkleid, Ionit
Vieira, Paulo
de Almeida Engler, Janice
Firester, Kalia
Spiegel, Yitzhak
Horowitz, Sigal Brown
Fatty Acid-and Retinol-Binding Protein, Mj-FAR-1 Induces Tomato Host Susceptibility to Root-Knot Nematodes
title Fatty Acid-and Retinol-Binding Protein, Mj-FAR-1 Induces Tomato Host Susceptibility to Root-Knot Nematodes
title_full Fatty Acid-and Retinol-Binding Protein, Mj-FAR-1 Induces Tomato Host Susceptibility to Root-Knot Nematodes
title_fullStr Fatty Acid-and Retinol-Binding Protein, Mj-FAR-1 Induces Tomato Host Susceptibility to Root-Knot Nematodes
title_full_unstemmed Fatty Acid-and Retinol-Binding Protein, Mj-FAR-1 Induces Tomato Host Susceptibility to Root-Knot Nematodes
title_short Fatty Acid-and Retinol-Binding Protein, Mj-FAR-1 Induces Tomato Host Susceptibility to Root-Knot Nematodes
title_sort fatty acid-and retinol-binding protein, mj-far-1 induces tomato host susceptibility to root-knot nematodes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3661543/
https://www.ncbi.nlm.nih.gov/pubmed/23717636
http://dx.doi.org/10.1371/journal.pone.0064586
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