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Stigmas of holoparasitic Phelipanche arenaria (Orobanchaceae) – a suitable ephemeric flower habitat for development unique microbiome

BACKGROUND: Microbial communities have occasionally been observed in part of the ephemeric reproductive structure of floral stigmas, but their prevalence, phylogenetic diversity and ecological roles are understudied. This report describes the first study of bacterial and fungal communities in immatu...

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Autores principales: Ruraż, Karolina, Przemieniecki, Sebastian Wojciech, Błaszak, Magdalena, Czarnomska, Sylwia Dagmara, Ochmian, Ireneusz, Piwowarczyk, Renata
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10566107/
https://www.ncbi.nlm.nih.gov/pubmed/37821804
http://dx.doi.org/10.1186/s12870-023-04488-1
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author Ruraż, Karolina
Przemieniecki, Sebastian Wojciech
Błaszak, Magdalena
Czarnomska, Sylwia Dagmara
Ochmian, Ireneusz
Piwowarczyk, Renata
author_facet Ruraż, Karolina
Przemieniecki, Sebastian Wojciech
Błaszak, Magdalena
Czarnomska, Sylwia Dagmara
Ochmian, Ireneusz
Piwowarczyk, Renata
author_sort Ruraż, Karolina
collection PubMed
description BACKGROUND: Microbial communities have occasionally been observed in part of the ephemeric reproductive structure of floral stigmas, but their prevalence, phylogenetic diversity and ecological roles are understudied. This report describes the first study of bacterial and fungal communities in immature and mature stigma tissue of the endangered holoparasitic plant Phelipanche arenaria. Culture-dependent methods coupled with next-generation sequencing indicated that a small surface of the flower stigma was an unexpectedly rich and diverse microhabitat for colonization of microbial. We also compared the enzymatic activity of the bacterial communities between immature and mature stigmas samples. RESULTS: Using high-throughput sequencing methods, we identified and classified 39 to over 51 OTUs per sample for bacterial OTUs represented by Pantoea agglomerans and P. ananatis, comprising 50.6%, followed by Pseudomonas, Luteibacter spp., Sphingomonas spp. with 17% of total frequency. The bacterial profile of immature stigmas of P. arenaria contained unique microorganisms (21 of the most numerous OTUs) that were not confirmed in mature stigmas. However, the enzymatic activity of bacteria in mature stigmas of P. arenaria showed more activity than observed in immature stigmas. In the fungal profile, we recorded even 80 OTUs in mature stigmas, consisting of Capnodiales 45.03% of the total abundance with 28.27% of frequency was created by Alternaria eichhorniae (10.55%), Mycosphaerella tassiana (9.69%), and Aureobasidium pullulans (8.03%). Additionally, numerous putative plant growth-promoting bacteria, fungal pathogens and pathogen-antagonistic yeasts were also detected. CONCLUSIONS: Our study uncovered that P. arenaria stigmas host diverse bacterial and fungal communities. These microorganisms are well known and have been described as beneficial for biotechnological and environmental applications (e.g., production of different enzymes and antimicrobial compounds). This research provided valuable insight into the parasitic plant–microbe interactions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04488-1.
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spelling pubmed-105661072023-10-12 Stigmas of holoparasitic Phelipanche arenaria (Orobanchaceae) – a suitable ephemeric flower habitat for development unique microbiome Ruraż, Karolina Przemieniecki, Sebastian Wojciech Błaszak, Magdalena Czarnomska, Sylwia Dagmara Ochmian, Ireneusz Piwowarczyk, Renata BMC Plant Biol Research BACKGROUND: Microbial communities have occasionally been observed in part of the ephemeric reproductive structure of floral stigmas, but their prevalence, phylogenetic diversity and ecological roles are understudied. This report describes the first study of bacterial and fungal communities in immature and mature stigma tissue of the endangered holoparasitic plant Phelipanche arenaria. Culture-dependent methods coupled with next-generation sequencing indicated that a small surface of the flower stigma was an unexpectedly rich and diverse microhabitat for colonization of microbial. We also compared the enzymatic activity of the bacterial communities between immature and mature stigmas samples. RESULTS: Using high-throughput sequencing methods, we identified and classified 39 to over 51 OTUs per sample for bacterial OTUs represented by Pantoea agglomerans and P. ananatis, comprising 50.6%, followed by Pseudomonas, Luteibacter spp., Sphingomonas spp. with 17% of total frequency. The bacterial profile of immature stigmas of P. arenaria contained unique microorganisms (21 of the most numerous OTUs) that were not confirmed in mature stigmas. However, the enzymatic activity of bacteria in mature stigmas of P. arenaria showed more activity than observed in immature stigmas. In the fungal profile, we recorded even 80 OTUs in mature stigmas, consisting of Capnodiales 45.03% of the total abundance with 28.27% of frequency was created by Alternaria eichhorniae (10.55%), Mycosphaerella tassiana (9.69%), and Aureobasidium pullulans (8.03%). Additionally, numerous putative plant growth-promoting bacteria, fungal pathogens and pathogen-antagonistic yeasts were also detected. CONCLUSIONS: Our study uncovered that P. arenaria stigmas host diverse bacterial and fungal communities. These microorganisms are well known and have been described as beneficial for biotechnological and environmental applications (e.g., production of different enzymes and antimicrobial compounds). This research provided valuable insight into the parasitic plant–microbe interactions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04488-1. BioMed Central 2023-10-11 /pmc/articles/PMC10566107/ /pubmed/37821804 http://dx.doi.org/10.1186/s12870-023-04488-1 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Ruraż, Karolina
Przemieniecki, Sebastian Wojciech
Błaszak, Magdalena
Czarnomska, Sylwia Dagmara
Ochmian, Ireneusz
Piwowarczyk, Renata
Stigmas of holoparasitic Phelipanche arenaria (Orobanchaceae) – a suitable ephemeric flower habitat for development unique microbiome
title Stigmas of holoparasitic Phelipanche arenaria (Orobanchaceae) – a suitable ephemeric flower habitat for development unique microbiome
title_full Stigmas of holoparasitic Phelipanche arenaria (Orobanchaceae) – a suitable ephemeric flower habitat for development unique microbiome
title_fullStr Stigmas of holoparasitic Phelipanche arenaria (Orobanchaceae) – a suitable ephemeric flower habitat for development unique microbiome
title_full_unstemmed Stigmas of holoparasitic Phelipanche arenaria (Orobanchaceae) – a suitable ephemeric flower habitat for development unique microbiome
title_short Stigmas of holoparasitic Phelipanche arenaria (Orobanchaceae) – a suitable ephemeric flower habitat for development unique microbiome
title_sort stigmas of holoparasitic phelipanche arenaria (orobanchaceae) – a suitable ephemeric flower habitat for development unique microbiome
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10566107/
https://www.ncbi.nlm.nih.gov/pubmed/37821804
http://dx.doi.org/10.1186/s12870-023-04488-1
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