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Herbivory Protection via Volatile Organic Compounds Is Influenced by Maize Genotype, Not Bacillus altitudinis-Enriched Bacterial Communities

Belowground, plants interact with beneficial soil microbes such as plant growth-promoting rhizobacteria (PGPR). PGPR are rhizosphere bacteria that colonize roots and elicit beneficial effects in plants such as improved plant growth, pathogen resistance, abiotic stress tolerance, and herbivore protec...

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Autores principales: Raglin, Sierra S., Kent, Angela D., Ngumbi, Esther N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9108721/
https://www.ncbi.nlm.nih.gov/pubmed/35586862
http://dx.doi.org/10.3389/fmicb.2022.826635
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author Raglin, Sierra S.
Kent, Angela D.
Ngumbi, Esther N.
author_facet Raglin, Sierra S.
Kent, Angela D.
Ngumbi, Esther N.
author_sort Raglin, Sierra S.
collection PubMed
description Belowground, plants interact with beneficial soil microbes such as plant growth-promoting rhizobacteria (PGPR). PGPR are rhizosphere bacteria that colonize roots and elicit beneficial effects in plants such as improved plant growth, pathogen resistance, abiotic stress tolerance, and herbivore protection. Treatment of plants with PGPR has been shown to trigger the emission of volatile organic compounds (VOCs). Volatile emissions can also be triggered by herbivory, termed herbivore-induced plant volatiles (HIPV), with important ramifications for chemical-mediated plant and insect interactions. Much of our current understanding of PGPR and herbivore-induced volatiles is based on studies using one plant genotype, yet domestication and modern breeding has led to the development of diverse germplasm with altered phenotypes and chemistry. In this study, we investigated if volatile emissions triggered by PGPR colonization and herbivory varies by maize genotype and microbial community assemblages. Six maize genotypes representing three decades of crop breeding and two heterotic groups were used, with four microbiome treatments: live or sterilized soil, with or without a Bacillus inoculant. Soil sterilization was used to delay microbiome establishment, resulting in low-diversity treatments. At planting, maize seeds were inoculated with PGPR Bacillus altitudinis AP-283 and grown under greenhouse conditions. Four weeks post planting, plants were subjected to feeding by third instar Helicoverpa zea (Lepidoptera: Noctuidae) larvae. Volatiles were collected using solid phase microextraction and analyzed with gas chromatography-mass spectrometry. Illumina NovaSeq 16S rRNA amplicon sequencing was carried out to characterize the rhizosphere microbiome. Maize genotype significantly influenced total volatile emissions, and relative abundance of volatile classes. We did not document a strong influence of microbe treatment on plant VOC emissions. However, inoculating plants with PGPR improved plant growth under sterile conditions. Taken together, our results suggest that genotypic variation is the dominant driver in HIPV composition and individual HIPV abundances, and any bacterial-mediated benefit is genotype and HIPV-specific. Therefore, understanding the interplay of these factors is necessary to fully harness microbially-mediated benefits and improve agricultural sustainability.
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spelling pubmed-91087212022-05-17 Herbivory Protection via Volatile Organic Compounds Is Influenced by Maize Genotype, Not Bacillus altitudinis-Enriched Bacterial Communities Raglin, Sierra S. Kent, Angela D. Ngumbi, Esther N. Front Microbiol Microbiology Belowground, plants interact with beneficial soil microbes such as plant growth-promoting rhizobacteria (PGPR). PGPR are rhizosphere bacteria that colonize roots and elicit beneficial effects in plants such as improved plant growth, pathogen resistance, abiotic stress tolerance, and herbivore protection. Treatment of plants with PGPR has been shown to trigger the emission of volatile organic compounds (VOCs). Volatile emissions can also be triggered by herbivory, termed herbivore-induced plant volatiles (HIPV), with important ramifications for chemical-mediated plant and insect interactions. Much of our current understanding of PGPR and herbivore-induced volatiles is based on studies using one plant genotype, yet domestication and modern breeding has led to the development of diverse germplasm with altered phenotypes and chemistry. In this study, we investigated if volatile emissions triggered by PGPR colonization and herbivory varies by maize genotype and microbial community assemblages. Six maize genotypes representing three decades of crop breeding and two heterotic groups were used, with four microbiome treatments: live or sterilized soil, with or without a Bacillus inoculant. Soil sterilization was used to delay microbiome establishment, resulting in low-diversity treatments. At planting, maize seeds were inoculated with PGPR Bacillus altitudinis AP-283 and grown under greenhouse conditions. Four weeks post planting, plants were subjected to feeding by third instar Helicoverpa zea (Lepidoptera: Noctuidae) larvae. Volatiles were collected using solid phase microextraction and analyzed with gas chromatography-mass spectrometry. Illumina NovaSeq 16S rRNA amplicon sequencing was carried out to characterize the rhizosphere microbiome. Maize genotype significantly influenced total volatile emissions, and relative abundance of volatile classes. We did not document a strong influence of microbe treatment on plant VOC emissions. However, inoculating plants with PGPR improved plant growth under sterile conditions. Taken together, our results suggest that genotypic variation is the dominant driver in HIPV composition and individual HIPV abundances, and any bacterial-mediated benefit is genotype and HIPV-specific. Therefore, understanding the interplay of these factors is necessary to fully harness microbially-mediated benefits and improve agricultural sustainability. Frontiers Media S.A. 2022-05-02 /pmc/articles/PMC9108721/ /pubmed/35586862 http://dx.doi.org/10.3389/fmicb.2022.826635 Text en Copyright © 2022 Raglin, Kent and Ngumbi. https://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
Raglin, Sierra S.
Kent, Angela D.
Ngumbi, Esther N.
Herbivory Protection via Volatile Organic Compounds Is Influenced by Maize Genotype, Not Bacillus altitudinis-Enriched Bacterial Communities
title Herbivory Protection via Volatile Organic Compounds Is Influenced by Maize Genotype, Not Bacillus altitudinis-Enriched Bacterial Communities
title_full Herbivory Protection via Volatile Organic Compounds Is Influenced by Maize Genotype, Not Bacillus altitudinis-Enriched Bacterial Communities
title_fullStr Herbivory Protection via Volatile Organic Compounds Is Influenced by Maize Genotype, Not Bacillus altitudinis-Enriched Bacterial Communities
title_full_unstemmed Herbivory Protection via Volatile Organic Compounds Is Influenced by Maize Genotype, Not Bacillus altitudinis-Enriched Bacterial Communities
title_short Herbivory Protection via Volatile Organic Compounds Is Influenced by Maize Genotype, Not Bacillus altitudinis-Enriched Bacterial Communities
title_sort herbivory protection via volatile organic compounds is influenced by maize genotype, not bacillus altitudinis-enriched bacterial communities
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9108721/
https://www.ncbi.nlm.nih.gov/pubmed/35586862
http://dx.doi.org/10.3389/fmicb.2022.826635
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