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

Abstract 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 i...

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Main Authors: Karolina Ruraż, Sebastian Wojciech Przemieniecki, Magdalena Błaszak, Sylwia Dagmara Czarnomska, Ireneusz Ochmian, Renata Piwowarczyk
Format: Article
Language:English
Published: BMC 2023-10-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-023-04488-1
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author Karolina Ruraż
Sebastian Wojciech Przemieniecki
Magdalena Błaszak
Sylwia Dagmara Czarnomska
Ireneusz Ochmian
Renata Piwowarczyk
author_facet Karolina Ruraż
Sebastian Wojciech Przemieniecki
Magdalena Błaszak
Sylwia Dagmara Czarnomska
Ireneusz Ochmian
Renata Piwowarczyk
author_sort Karolina Ruraż
collection DOAJ
description Abstract 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.
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spelling doaj.art-81b5a6b679d1425aa67fe9a54400b68a2023-11-26T12:46:45ZengBMCBMC Plant Biology1471-22292023-10-0123112210.1186/s12870-023-04488-1Stigmas of holoparasitic Phelipanche arenaria (Orobanchaceae) – a suitable ephemeric flower habitat for development unique microbiomeKarolina Ruraż0Sebastian Wojciech Przemieniecki1Magdalena Błaszak2Sylwia Dagmara Czarnomska3Ireneusz Ochmian4Renata Piwowarczyk5Center for Research and Conservation of Biodiversity, Department of Environmental Biology, Institute of Biology, Jan Kochanowski UniversityDepartment of Entomology, Phytopathology and Molecular Diagnostics, University of Warmia and Mazury in OlsztynDepartment of Bioengineering, West Pomeranian University of Technology in SzczecinMuseum and Institute of Zoology, Polish Academy of SciencesDepartment of Horticulture, West Pomeranian University of Technology in SzczecinCenter for Research and Conservation of Biodiversity, Department of Environmental Biology, Institute of Biology, Jan Kochanowski UniversityAbstract 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.https://doi.org/10.1186/s12870-023-04488-1Flower microbiomeParasitic plantsEnvironment16S rRNA geneInternal transcribed spacer (ITS)Next-generation sequencing
spellingShingle Karolina Ruraż
Sebastian Wojciech Przemieniecki
Magdalena Błaszak
Sylwia Dagmara Czarnomska
Ireneusz Ochmian
Renata Piwowarczyk
Stigmas of holoparasitic Phelipanche arenaria (Orobanchaceae) – a suitable ephemeric flower habitat for development unique microbiome
BMC Plant Biology
Flower microbiome
Parasitic plants
Environment
16S rRNA gene
Internal transcribed spacer (ITS)
Next-generation sequencing
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 Flower microbiome
Parasitic plants
Environment
16S rRNA gene
Internal transcribed spacer (ITS)
Next-generation sequencing
url https://doi.org/10.1186/s12870-023-04488-1
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