A root-knot nematode effector manipulates the rhizosphere microbiome for establishing parasitism relationship with hosts

IntroductionRoot-knot nematode (RKN; Meloidogyne spp.) is one of the most infamous soilborne plant diseases, causing severe crop losses every year. Effector proteins secreted by RKNs play crucial roles during plant-nematode interaction. However, less is known about whether RKN effector proteins can...

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Main Authors: Rui Liu, Mengfei Chen, Boliang Liu, Kaiwei Huang, Zhenchuan Mao, Huixia Li, Jianlong Zhao
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1217863/full
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author Rui Liu
Mengfei Chen
Boliang Liu
Kaiwei Huang
Zhenchuan Mao
Huixia Li
Jianlong Zhao
author_facet Rui Liu
Mengfei Chen
Boliang Liu
Kaiwei Huang
Zhenchuan Mao
Huixia Li
Jianlong Zhao
author_sort Rui Liu
collection DOAJ
description IntroductionRoot-knot nematode (RKN; Meloidogyne spp.) is one of the most infamous soilborne plant diseases, causing severe crop losses every year. Effector proteins secreted by RKNs play crucial roles during plant-nematode interaction. However, less is known about whether RKN effector proteins can impact the rhizosphere microbial environment.MethodsIn this study, we investigated the rhizosphere microbiome community of MiMIF-2 (a plant immunity-modulating effector) transgenic Arabidopsis thaliana with or without nematode infection using the Illumina high-throughput sequencing analysis.Results and discussionThe results showed that the bacterial species richness index increased, while the fungi species richness index decreased in M. incognita-infected MiMIF-2 transgenic A. thaliana plants. The relative abundance of genera such as Clitopilus, Komagataeibacter, Lactobacillus, Prevotella, Moritella, Vibrio, Escherichia-Shigella, and Pseudomonas was reduced in MiMIF-2 transgenic A. thaliana plants compared to wild type, but was significantly increased after inoculation with M. incognita. The Cluster of Orthologous Genes (COG) function classification analysis revealed a decrease in the relative abundance of defense mechanisms, secondary metabolite biosynthesis, transport, and nematode infection catabolism-related functions in MiMIF-2 lines compared to the wild type. These differences may be the reason for the increased susceptibility of MiMIF-2 transgenic A. thaliana to nematode infection. Our results provide a new insight into RKN effector proteins and their association with the microbial community, host, and plant pathogens, which will lead to the exploration of new innovative ideas for future biological control of RKNs.
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spelling doaj.art-20af014308294c14a7168a09ccdc86912023-07-19T08:28:44ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-07-011410.3389/fmicb.2023.12178631217863A root-knot nematode effector manipulates the rhizosphere microbiome for establishing parasitism relationship with hostsRui Liu0Mengfei Chen1Boliang Liu2Kaiwei Huang3Zhenchuan Mao4Huixia Li5Jianlong Zhao6College of Plant Protection, Gansu Agricultural University/Biocontrol Engineering Laboratory of Crop Diseases and Pests of Gansu Province, Lanzhou, Gansu, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, ChinaSchool of Life Sciences, Sun Yat-Sen University, Guangzhou, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, ChinaCollege of Plant Protection, Gansu Agricultural University/Biocontrol Engineering Laboratory of Crop Diseases and Pests of Gansu Province, Lanzhou, Gansu, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, ChinaIntroductionRoot-knot nematode (RKN; Meloidogyne spp.) is one of the most infamous soilborne plant diseases, causing severe crop losses every year. Effector proteins secreted by RKNs play crucial roles during plant-nematode interaction. However, less is known about whether RKN effector proteins can impact the rhizosphere microbial environment.MethodsIn this study, we investigated the rhizosphere microbiome community of MiMIF-2 (a plant immunity-modulating effector) transgenic Arabidopsis thaliana with or without nematode infection using the Illumina high-throughput sequencing analysis.Results and discussionThe results showed that the bacterial species richness index increased, while the fungi species richness index decreased in M. incognita-infected MiMIF-2 transgenic A. thaliana plants. The relative abundance of genera such as Clitopilus, Komagataeibacter, Lactobacillus, Prevotella, Moritella, Vibrio, Escherichia-Shigella, and Pseudomonas was reduced in MiMIF-2 transgenic A. thaliana plants compared to wild type, but was significantly increased after inoculation with M. incognita. The Cluster of Orthologous Genes (COG) function classification analysis revealed a decrease in the relative abundance of defense mechanisms, secondary metabolite biosynthesis, transport, and nematode infection catabolism-related functions in MiMIF-2 lines compared to the wild type. These differences may be the reason for the increased susceptibility of MiMIF-2 transgenic A. thaliana to nematode infection. Our results provide a new insight into RKN effector proteins and their association with the microbial community, host, and plant pathogens, which will lead to the exploration of new innovative ideas for future biological control of RKNs.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1217863/fullrhizosphere microbiomeMeloidogyne incognitaArabidopsis thalianaMiMIF-2 effector proteinparasitism
spellingShingle Rui Liu
Mengfei Chen
Boliang Liu
Kaiwei Huang
Zhenchuan Mao
Huixia Li
Jianlong Zhao
A root-knot nematode effector manipulates the rhizosphere microbiome for establishing parasitism relationship with hosts
Frontiers in Microbiology
rhizosphere microbiome
Meloidogyne incognita
Arabidopsis thaliana
MiMIF-2 effector protein
parasitism
title A root-knot nematode effector manipulates the rhizosphere microbiome for establishing parasitism relationship with hosts
title_full A root-knot nematode effector manipulates the rhizosphere microbiome for establishing parasitism relationship with hosts
title_fullStr A root-knot nematode effector manipulates the rhizosphere microbiome for establishing parasitism relationship with hosts
title_full_unstemmed A root-knot nematode effector manipulates the rhizosphere microbiome for establishing parasitism relationship with hosts
title_short A root-knot nematode effector manipulates the rhizosphere microbiome for establishing parasitism relationship with hosts
title_sort root knot nematode effector manipulates the rhizosphere microbiome for establishing parasitism relationship with hosts
topic rhizosphere microbiome
Meloidogyne incognita
Arabidopsis thaliana
MiMIF-2 effector protein
parasitism
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1217863/full
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