Integrative multi-omics analysis reveals the translational landscape of the plant-parasitic nematode Meloidogyne incognita

Abstract Root-knot nematodes (RKNs) of the genus Meloidogyne pose the most significant threats to global food security due to their destructive nature as plant-parasitic nematodes. Although significant attention has been devoted to investigating the gene transcription profiling of RKNs, our understa...

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Main Authors: Zhaolu Zhu, Dexin Bo, Chuanshuai Xie, Dadong Dai, Donghai Peng, Ming Sun, Jinshui Zheng
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-025-07533-x
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author Zhaolu Zhu
Dexin Bo
Chuanshuai Xie
Dadong Dai
Donghai Peng
Ming Sun
Jinshui Zheng
author_facet Zhaolu Zhu
Dexin Bo
Chuanshuai Xie
Dadong Dai
Donghai Peng
Ming Sun
Jinshui Zheng
author_sort Zhaolu Zhu
collection DOAJ
description Abstract Root-knot nematodes (RKNs) of the genus Meloidogyne pose the most significant threats to global food security due to their destructive nature as plant-parasitic nematodes. Although significant attention has been devoted to investigating the gene transcription profiling of RKNs, our understanding of the translational landscape of RKNs remains limited. In this study, we elucidated the translational landscape of Meloidogyne incognita through the integration of translatome, transcriptome and quantitative proteome analyses. Our findings revealed numerous previously unannotated translation events and refined the genome annotation. By investigating the genome-wide translational dynamics of M. incognita during parasitism, we revealed that the genes of M. incognita undergo parasitic stage-specific regulation at the translational level. Interestingly, we identified 470 micropeptides (containing fewer than 100 amino acids) with the potential to function as effectors. Additionally, we observed that the effector-coding genes in M. incognita exhibit higher translation efficiency (TE). Further analysis suggests that M. incognita has the potential to regulate the TE of effector-coding genes without simultaneous alterations in their transcript abundance, facilitating effector synthesis. Collectively, our study provides comprehensive datasets and explores the genome-wide translational landscape of M. incognita, shedding light on the contributions of translational regulation during parasitism.
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issn 2399-3642
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spelling doaj-art-90cdeee476f94610a8acd2cbf7dcbf272025-02-02T12:37:25ZengNature PortfolioCommunications Biology2399-36422025-01-018111210.1038/s42003-025-07533-xIntegrative multi-omics analysis reveals the translational landscape of the plant-parasitic nematode Meloidogyne incognitaZhaolu Zhu0Dexin Bo1Chuanshuai Xie2Dadong Dai3Donghai Peng4Ming Sun5Jinshui Zheng6National Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityAbstract Root-knot nematodes (RKNs) of the genus Meloidogyne pose the most significant threats to global food security due to their destructive nature as plant-parasitic nematodes. Although significant attention has been devoted to investigating the gene transcription profiling of RKNs, our understanding of the translational landscape of RKNs remains limited. In this study, we elucidated the translational landscape of Meloidogyne incognita through the integration of translatome, transcriptome and quantitative proteome analyses. Our findings revealed numerous previously unannotated translation events and refined the genome annotation. By investigating the genome-wide translational dynamics of M. incognita during parasitism, we revealed that the genes of M. incognita undergo parasitic stage-specific regulation at the translational level. Interestingly, we identified 470 micropeptides (containing fewer than 100 amino acids) with the potential to function as effectors. Additionally, we observed that the effector-coding genes in M. incognita exhibit higher translation efficiency (TE). Further analysis suggests that M. incognita has the potential to regulate the TE of effector-coding genes without simultaneous alterations in their transcript abundance, facilitating effector synthesis. Collectively, our study provides comprehensive datasets and explores the genome-wide translational landscape of M. incognita, shedding light on the contributions of translational regulation during parasitism.https://doi.org/10.1038/s42003-025-07533-x
spellingShingle Zhaolu Zhu
Dexin Bo
Chuanshuai Xie
Dadong Dai
Donghai Peng
Ming Sun
Jinshui Zheng
Integrative multi-omics analysis reveals the translational landscape of the plant-parasitic nematode Meloidogyne incognita
Communications Biology
title Integrative multi-omics analysis reveals the translational landscape of the plant-parasitic nematode Meloidogyne incognita
title_full Integrative multi-omics analysis reveals the translational landscape of the plant-parasitic nematode Meloidogyne incognita
title_fullStr Integrative multi-omics analysis reveals the translational landscape of the plant-parasitic nematode Meloidogyne incognita
title_full_unstemmed Integrative multi-omics analysis reveals the translational landscape of the plant-parasitic nematode Meloidogyne incognita
title_short Integrative multi-omics analysis reveals the translational landscape of the plant-parasitic nematode Meloidogyne incognita
title_sort integrative multi omics analysis reveals the translational landscape of the plant parasitic nematode meloidogyne incognita
url https://doi.org/10.1038/s42003-025-07533-x
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