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The Cultured Microbiome of Pollinated Maize Silks Shifts after Infection with Fusarium graminearum and Varies by Distance from the Site of Pathogen Inoculation

Styles transmit pollen-derived sperm nuclei from pollen to ovules, but also transmit environmental pathogens. The microbiomes of styles are likely important for reproduction/disease, yet few studies exist. Whether style microbiome compositions are spatially responsive to pathogens is unknown. The ma...

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Autores principales: Thompson, Michelle E. H., Shrestha, Anuja, Rinne, Jeffrey, Limay-Rios, Victor, Reid, Lana, Raizada, Manish N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10675081/
https://www.ncbi.nlm.nih.gov/pubmed/38003787
http://dx.doi.org/10.3390/pathogens12111322
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author Thompson, Michelle E. H.
Shrestha, Anuja
Rinne, Jeffrey
Limay-Rios, Victor
Reid, Lana
Raizada, Manish N.
author_facet Thompson, Michelle E. H.
Shrestha, Anuja
Rinne, Jeffrey
Limay-Rios, Victor
Reid, Lana
Raizada, Manish N.
author_sort Thompson, Michelle E. H.
collection PubMed
description Styles transmit pollen-derived sperm nuclei from pollen to ovules, but also transmit environmental pathogens. The microbiomes of styles are likely important for reproduction/disease, yet few studies exist. Whether style microbiome compositions are spatially responsive to pathogens is unknown. The maize pathogen Fusarium graminearum enters developing grain through the style (silk). We hypothesized that F. graminearum treatment shifts the cultured transmitting silk microbiome (TSM) compared to healthy silks in a distance-dependent manner. Another objective of the study was to culture microbes for future application. Bacteria were cultured from husk-covered silks of 14 F. graminearum-treated diverse maize genotypes, proximal (tip) and distal (base) to the F. graminearum inoculation site. Long-read 16S sequences from 398 isolates spanned 35 genera, 71 species, and 238 OTUs. More bacteria were cultured from F. graminearum-inoculated tips (271 isolates) versus base (127 isolates); healthy silks were balanced. F. graminearum caused a collapse in diversity of ~20–25% across multiple taxonomic levels. Some species were cultured exclusively or, more often, from F. graminearum-treated silks (e.g., Delftia acidovorans, Klebsiella aerogenes, K. grimontii, Pantoea ananatis, Stenotrophomonas pavanii). Overall, the results suggest that F. graminearum alters the TSM in a distance-dependent manner. Many isolates matched taxa that were previously identified using V4-MiSeq (core and F. graminearum-induced), but long-read sequencing clarified the taxonomy and uncovered greater diversity than was initially predicted (e.g., within Pantoea). These isolates represent the first comprehensive cultured collection from pathogen-treated maize silks to facilitate biocontrol efforts and microbial marker-assisted breeding.
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spelling pubmed-106750812023-11-06 The Cultured Microbiome of Pollinated Maize Silks Shifts after Infection with Fusarium graminearum and Varies by Distance from the Site of Pathogen Inoculation Thompson, Michelle E. H. Shrestha, Anuja Rinne, Jeffrey Limay-Rios, Victor Reid, Lana Raizada, Manish N. Pathogens Article Styles transmit pollen-derived sperm nuclei from pollen to ovules, but also transmit environmental pathogens. The microbiomes of styles are likely important for reproduction/disease, yet few studies exist. Whether style microbiome compositions are spatially responsive to pathogens is unknown. The maize pathogen Fusarium graminearum enters developing grain through the style (silk). We hypothesized that F. graminearum treatment shifts the cultured transmitting silk microbiome (TSM) compared to healthy silks in a distance-dependent manner. Another objective of the study was to culture microbes for future application. Bacteria were cultured from husk-covered silks of 14 F. graminearum-treated diverse maize genotypes, proximal (tip) and distal (base) to the F. graminearum inoculation site. Long-read 16S sequences from 398 isolates spanned 35 genera, 71 species, and 238 OTUs. More bacteria were cultured from F. graminearum-inoculated tips (271 isolates) versus base (127 isolates); healthy silks were balanced. F. graminearum caused a collapse in diversity of ~20–25% across multiple taxonomic levels. Some species were cultured exclusively or, more often, from F. graminearum-treated silks (e.g., Delftia acidovorans, Klebsiella aerogenes, K. grimontii, Pantoea ananatis, Stenotrophomonas pavanii). Overall, the results suggest that F. graminearum alters the TSM in a distance-dependent manner. Many isolates matched taxa that were previously identified using V4-MiSeq (core and F. graminearum-induced), but long-read sequencing clarified the taxonomy and uncovered greater diversity than was initially predicted (e.g., within Pantoea). These isolates represent the first comprehensive cultured collection from pathogen-treated maize silks to facilitate biocontrol efforts and microbial marker-assisted breeding. MDPI 2023-11-06 /pmc/articles/PMC10675081/ /pubmed/38003787 http://dx.doi.org/10.3390/pathogens12111322 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Thompson, Michelle E. H.
Shrestha, Anuja
Rinne, Jeffrey
Limay-Rios, Victor
Reid, Lana
Raizada, Manish N.
The Cultured Microbiome of Pollinated Maize Silks Shifts after Infection with Fusarium graminearum and Varies by Distance from the Site of Pathogen Inoculation
title The Cultured Microbiome of Pollinated Maize Silks Shifts after Infection with Fusarium graminearum and Varies by Distance from the Site of Pathogen Inoculation
title_full The Cultured Microbiome of Pollinated Maize Silks Shifts after Infection with Fusarium graminearum and Varies by Distance from the Site of Pathogen Inoculation
title_fullStr The Cultured Microbiome of Pollinated Maize Silks Shifts after Infection with Fusarium graminearum and Varies by Distance from the Site of Pathogen Inoculation
title_full_unstemmed The Cultured Microbiome of Pollinated Maize Silks Shifts after Infection with Fusarium graminearum and Varies by Distance from the Site of Pathogen Inoculation
title_short The Cultured Microbiome of Pollinated Maize Silks Shifts after Infection with Fusarium graminearum and Varies by Distance from the Site of Pathogen Inoculation
title_sort cultured microbiome of pollinated maize silks shifts after infection with fusarium graminearum and varies by distance from the site of pathogen inoculation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10675081/
https://www.ncbi.nlm.nih.gov/pubmed/38003787
http://dx.doi.org/10.3390/pathogens12111322
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