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Plants and Associated Soil Microbiota Cooperatively Suppress Plant-Parasitic Nematodes

Disease suppressive soils with specific suppression of soil-borne pathogens and parasites have been long studied and are most often of microbiological origin. As for the plant-parasitic nematodes (PPN), which represent a huge threat to agricultural crops and which successfully defy many conventional...

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Autores principales: Topalović, Olivera, Hussain, Muzammil, Heuer, Holger
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7058703/
https://www.ncbi.nlm.nih.gov/pubmed/32184773
http://dx.doi.org/10.3389/fmicb.2020.00313
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author Topalović, Olivera
Hussain, Muzammil
Heuer, Holger
author_facet Topalović, Olivera
Hussain, Muzammil
Heuer, Holger
author_sort Topalović, Olivera
collection PubMed
description Disease suppressive soils with specific suppression of soil-borne pathogens and parasites have been long studied and are most often of microbiological origin. As for the plant-parasitic nematodes (PPN), which represent a huge threat to agricultural crops and which successfully defy many conventional control methods, soil progression from conducive to suppressive state is accompanied by the enrichment of specific antagonistic microbial consortia. However, a few microbial groups have come to the fore in diminishing PPN in disease suppressive soils using culture-dependent methods. Studies with cultured strains resulted in understanding the mechanisms by which nematodes are antagonized by microorganisms. Recent culture-independent studies on the microbiome associated with soil, plant roots, and PPN contributed to a better understanding of the functional potential of disease suppressive microbial cohort. Plant root exudation is an important pathway determining host-microbe communication and plays a key role in selection and enrichment of a specific set of microbial antagonists in the rhizosphere as first line of defense against crop pathogens or parasites. Root exudates comprising primary metabolites such as amino acids, sugars, organic acids, and secondary metabolites can also cause modifications in the nematode surface and subsequently affect microbial attachment. A positive interaction between hosts and their beneficial root microbiota is correlated with a low nematode performance on the host. In this review, we first summarized the historical records of nematode-suppressive soils and then focused on more recent studies in this aspect, emphasizing the advances in studying nematode-microbe interactions over time. We highlighted nematode biocontrol mechanisms, especially parasitism, induced systemic resistance, and volatile organic compounds using microbial consortia, or bacterial strains of the genera Pasteuria, Bacillus, Pseudomonas, Rhizobium, Streptomyces, Arthrobacter, and Variovorax, or fungal isolates of Pochonia, Dactylella, Nematophthora, Purpureocillium, Trichoderma, Hirsutella, Arthrobotrys, and Mortierella. We discussed the importance of root exudates in plant communication with PPN and soil microorganisms, emphasizing their role in microbial attachment to the nematode surface and subsequent events of nematode parasitism. Comprehensive understanding of the plant-beneficial microbial consortia and the mechanisms underlying disease suppression may help to develop synthetic microbial communities for biocontrol of PPN, thereby reducing nematicides and fertilizers inputs.
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spelling pubmed-70587032020-03-17 Plants and Associated Soil Microbiota Cooperatively Suppress Plant-Parasitic Nematodes Topalović, Olivera Hussain, Muzammil Heuer, Holger Front Microbiol Microbiology Disease suppressive soils with specific suppression of soil-borne pathogens and parasites have been long studied and are most often of microbiological origin. As for the plant-parasitic nematodes (PPN), which represent a huge threat to agricultural crops and which successfully defy many conventional control methods, soil progression from conducive to suppressive state is accompanied by the enrichment of specific antagonistic microbial consortia. However, a few microbial groups have come to the fore in diminishing PPN in disease suppressive soils using culture-dependent methods. Studies with cultured strains resulted in understanding the mechanisms by which nematodes are antagonized by microorganisms. Recent culture-independent studies on the microbiome associated with soil, plant roots, and PPN contributed to a better understanding of the functional potential of disease suppressive microbial cohort. Plant root exudation is an important pathway determining host-microbe communication and plays a key role in selection and enrichment of a specific set of microbial antagonists in the rhizosphere as first line of defense against crop pathogens or parasites. Root exudates comprising primary metabolites such as amino acids, sugars, organic acids, and secondary metabolites can also cause modifications in the nematode surface and subsequently affect microbial attachment. A positive interaction between hosts and their beneficial root microbiota is correlated with a low nematode performance on the host. In this review, we first summarized the historical records of nematode-suppressive soils and then focused on more recent studies in this aspect, emphasizing the advances in studying nematode-microbe interactions over time. We highlighted nematode biocontrol mechanisms, especially parasitism, induced systemic resistance, and volatile organic compounds using microbial consortia, or bacterial strains of the genera Pasteuria, Bacillus, Pseudomonas, Rhizobium, Streptomyces, Arthrobacter, and Variovorax, or fungal isolates of Pochonia, Dactylella, Nematophthora, Purpureocillium, Trichoderma, Hirsutella, Arthrobotrys, and Mortierella. We discussed the importance of root exudates in plant communication with PPN and soil microorganisms, emphasizing their role in microbial attachment to the nematode surface and subsequent events of nematode parasitism. Comprehensive understanding of the plant-beneficial microbial consortia and the mechanisms underlying disease suppression may help to develop synthetic microbial communities for biocontrol of PPN, thereby reducing nematicides and fertilizers inputs. Frontiers Media S.A. 2020-02-28 /pmc/articles/PMC7058703/ /pubmed/32184773 http://dx.doi.org/10.3389/fmicb.2020.00313 Text en Copyright © 2020 Topalović, Hussain and Heuer. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Topalović, Olivera
Hussain, Muzammil
Heuer, Holger
Plants and Associated Soil Microbiota Cooperatively Suppress Plant-Parasitic Nematodes
title Plants and Associated Soil Microbiota Cooperatively Suppress Plant-Parasitic Nematodes
title_full Plants and Associated Soil Microbiota Cooperatively Suppress Plant-Parasitic Nematodes
title_fullStr Plants and Associated Soil Microbiota Cooperatively Suppress Plant-Parasitic Nematodes
title_full_unstemmed Plants and Associated Soil Microbiota Cooperatively Suppress Plant-Parasitic Nematodes
title_short Plants and Associated Soil Microbiota Cooperatively Suppress Plant-Parasitic Nematodes
title_sort plants and associated soil microbiota cooperatively suppress plant-parasitic nematodes
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7058703/
https://www.ncbi.nlm.nih.gov/pubmed/32184773
http://dx.doi.org/10.3389/fmicb.2020.00313
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