The Meloidogyne incognita Nuclear Effector MiEFF1 Interacts With Arabidopsis Cytosolic Glyceraldehyde-3-Phosphate Dehydrogenases to Promote Parasitism

Root-knot nematodes are obligate endoparasites that maintain a biotrophic relationship with their hosts over a period of several weeks. They induce the differentiation of root cells into specialized multinucleate hypertrophied feeding cells known as giant cells. Nematode effectors synthesized in the...

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Main Authors: Nhat My Truong, Yongpan Chen, Joffrey Mejias, Salomé Soulé, Karine Mulet, Maëlle Jaouannet, Stéphanie Jaubert-Possamai, Shinichiro Sawa, Pierre Abad, Bruno Favery, Michaël Quentin
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-04-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.641480/full
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author Nhat My Truong
Nhat My Truong
Yongpan Chen
Yongpan Chen
Joffrey Mejias
Salomé Soulé
Karine Mulet
Maëlle Jaouannet
Stéphanie Jaubert-Possamai
Shinichiro Sawa
Pierre Abad
Bruno Favery
Michaël Quentin
author_facet Nhat My Truong
Nhat My Truong
Yongpan Chen
Yongpan Chen
Joffrey Mejias
Salomé Soulé
Karine Mulet
Maëlle Jaouannet
Stéphanie Jaubert-Possamai
Shinichiro Sawa
Pierre Abad
Bruno Favery
Michaël Quentin
author_sort Nhat My Truong
collection DOAJ
description Root-knot nematodes are obligate endoparasites that maintain a biotrophic relationship with their hosts over a period of several weeks. They induce the differentiation of root cells into specialized multinucleate hypertrophied feeding cells known as giant cells. Nematode effectors synthesized in the esophageal glands and injected into the plant tissue through the syringe-like stylet play a key role in giant cell ontogenesis. The Meloidogyne incognita MiEFF1 is one of the rare effectors of phytopathogenic nematodes to have been located in vivo in feeding cells. This effector specifically targets the giant cell nuclei. We investigated the Arabidopsis functions modulated by this effector, by using a yeast two-hybrid approach to identify its host targets. We characterized a universal stress protein (USP) and cytosolic glyceraldehyde-3-phosphate dehydrogenases (GAPCs) as the targets of MiEFF1. We validated the interaction of MiEFF1 with these host targets in the plant cell nucleus, by bimolecular fluorescence complementation (BiFC). A functional analysis with Arabidopsis GUS reporter lines and knockout mutant lines showed that GAPCs were induced in giant cells and that their non-metabolic functions were required for root-knot nematode infection. These susceptibility factors are potentially interesting targets for the development of new root-knot nematode control strategies.
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spelling doaj.art-5b4cc3a82d5b4c82b3b343e2816be11f2022-12-21T22:53:41ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-04-011210.3389/fpls.2021.641480641480The Meloidogyne incognita Nuclear Effector MiEFF1 Interacts With Arabidopsis Cytosolic Glyceraldehyde-3-Phosphate Dehydrogenases to Promote ParasitismNhat My Truong0Nhat My Truong1Yongpan Chen2Yongpan Chen3Joffrey Mejias4Salomé Soulé5Karine Mulet6Maëlle Jaouannet7Stéphanie Jaubert-Possamai8Shinichiro Sawa9Pierre Abad10Bruno Favery11Michaël Quentin12Institut Sophia Agrobiotech, INRAE, CNRS, Université Côte d’Azur, Sophia Antipolis, FranceGraduate School of Science and Technology, Kumamoto University, Kumamoto, JapanInstitut Sophia Agrobiotech, INRAE, CNRS, Université Côte d’Azur, Sophia Antipolis, FranceDepartment of Plant Pathology and Key Laboratory of Pest Monitoring and Green Management of the Ministry of Agriculture, China Agricultural University, Beijing, ChinaInstitut Sophia Agrobiotech, INRAE, CNRS, Université Côte d’Azur, Sophia Antipolis, FranceInstitut Sophia Agrobiotech, INRAE, CNRS, Université Côte d’Azur, Sophia Antipolis, FranceInstitut Sophia Agrobiotech, INRAE, CNRS, Université Côte d’Azur, Sophia Antipolis, FranceInstitut Sophia Agrobiotech, INRAE, CNRS, Université Côte d’Azur, Sophia Antipolis, FranceInstitut Sophia Agrobiotech, INRAE, CNRS, Université Côte d’Azur, Sophia Antipolis, FranceGraduate School of Science and Technology, Kumamoto University, Kumamoto, JapanInstitut Sophia Agrobiotech, INRAE, CNRS, Université Côte d’Azur, Sophia Antipolis, FranceInstitut Sophia Agrobiotech, INRAE, CNRS, Université Côte d’Azur, Sophia Antipolis, FranceInstitut Sophia Agrobiotech, INRAE, CNRS, Université Côte d’Azur, Sophia Antipolis, FranceRoot-knot nematodes are obligate endoparasites that maintain a biotrophic relationship with their hosts over a period of several weeks. They induce the differentiation of root cells into specialized multinucleate hypertrophied feeding cells known as giant cells. Nematode effectors synthesized in the esophageal glands and injected into the plant tissue through the syringe-like stylet play a key role in giant cell ontogenesis. The Meloidogyne incognita MiEFF1 is one of the rare effectors of phytopathogenic nematodes to have been located in vivo in feeding cells. This effector specifically targets the giant cell nuclei. We investigated the Arabidopsis functions modulated by this effector, by using a yeast two-hybrid approach to identify its host targets. We characterized a universal stress protein (USP) and cytosolic glyceraldehyde-3-phosphate dehydrogenases (GAPCs) as the targets of MiEFF1. We validated the interaction of MiEFF1 with these host targets in the plant cell nucleus, by bimolecular fluorescence complementation (BiFC). A functional analysis with Arabidopsis GUS reporter lines and knockout mutant lines showed that GAPCs were induced in giant cells and that their non-metabolic functions were required for root-knot nematode infection. These susceptibility factors are potentially interesting targets for the development of new root-knot nematode control strategies.https://www.frontiersin.org/articles/10.3389/fpls.2021.641480/fullroot-knot nematode (Meloidogyne incognita)effectorgiant cellcytosolic glyceraldehyde-3-phosphate dehydrogenasessusceptibility gene
spellingShingle Nhat My Truong
Nhat My Truong
Yongpan Chen
Yongpan Chen
Joffrey Mejias
Salomé Soulé
Karine Mulet
Maëlle Jaouannet
Stéphanie Jaubert-Possamai
Shinichiro Sawa
Pierre Abad
Bruno Favery
Michaël Quentin
The Meloidogyne incognita Nuclear Effector MiEFF1 Interacts With Arabidopsis Cytosolic Glyceraldehyde-3-Phosphate Dehydrogenases to Promote Parasitism
Frontiers in Plant Science
root-knot nematode (Meloidogyne incognita)
effector
giant cell
cytosolic glyceraldehyde-3-phosphate dehydrogenases
susceptibility gene
title The Meloidogyne incognita Nuclear Effector MiEFF1 Interacts With Arabidopsis Cytosolic Glyceraldehyde-3-Phosphate Dehydrogenases to Promote Parasitism
title_full The Meloidogyne incognita Nuclear Effector MiEFF1 Interacts With Arabidopsis Cytosolic Glyceraldehyde-3-Phosphate Dehydrogenases to Promote Parasitism
title_fullStr The Meloidogyne incognita Nuclear Effector MiEFF1 Interacts With Arabidopsis Cytosolic Glyceraldehyde-3-Phosphate Dehydrogenases to Promote Parasitism
title_full_unstemmed The Meloidogyne incognita Nuclear Effector MiEFF1 Interacts With Arabidopsis Cytosolic Glyceraldehyde-3-Phosphate Dehydrogenases to Promote Parasitism
title_short The Meloidogyne incognita Nuclear Effector MiEFF1 Interacts With Arabidopsis Cytosolic Glyceraldehyde-3-Phosphate Dehydrogenases to Promote Parasitism
title_sort meloidogyne incognita nuclear effector mieff1 interacts with arabidopsis cytosolic glyceraldehyde 3 phosphate dehydrogenases to promote parasitism
topic root-knot nematode (Meloidogyne incognita)
effector
giant cell
cytosolic glyceraldehyde-3-phosphate dehydrogenases
susceptibility gene
url https://www.frontiersin.org/articles/10.3389/fpls.2021.641480/full
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