Contrasting microbial communities on male and female flowers of a dioecious plant, Mallotus japonicus (Euphorbiaceae)

Abstract Flowers play a central role in plant reproduction by dispersing and receiving pollen grains delivered by animal vectors or air. They are rich in various nutrients, and therefore, provide an ideal habitat for many microbes. Recent studies have revealed that flower microbial communities can b...

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Main Authors: Maxime Marre, Masayuki Ushio, Shoko Sakai
Format: Article
Language:English
Published: Wiley 2022-05-01
Series:Environmental DNA
Subjects:
Online Access:https://doi.org/10.1002/edn3.271
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author Maxime Marre
Masayuki Ushio
Shoko Sakai
author_facet Maxime Marre
Masayuki Ushio
Shoko Sakai
author_sort Maxime Marre
collection DOAJ
description Abstract Flowers play a central role in plant reproduction by dispersing and receiving pollen grains delivered by animal vectors or air. They are rich in various nutrients, and therefore, provide an ideal habitat for many microbes. Recent studies have revealed that flower microbial communities can be highly variable among species, individuals, or even floral parts. However, sexual differences in flower microbial communities have rarely been investigated. In this study, we analyzed the flower prokaryotic communities of a dioecious plant (male and female flowers are produced on different individuals), Mallotus japonicus, in its natural habitat in Otsu, Japan. Using 16S rRNA amplicon sequencing, we found a differentiation in microbial communities between male and female flowers. Procaryotes on male flowers were relatively diverse, and included several dominant amplicon sequence variants (ASVs), mainly from the Gammaproteobacteria. These ASVs were also found on the body surface of flower visitor insects, suggesting that the visitors dispersed these microbes when they visited the flowers. On the other hand, female flower samples were overwhelmingly dominated by a single bacterial sequence from the Alphaproteobacteria, which showed a peak of relative abundance at the middle of the flowering season. The bacterium had already been present at anthesis, and its relative abundance on flower visitors was low. Flower visitors may have little effect on the microbial composition on female flowers. The lower diversity of microbes on female flowers than on male flowers suggests that the female flowers function as a stronger filter, possibly related to a strong defense against antagonists. These differences may be associated with different reproductive strategies of male and female flowers. This study indicates that dioecious plants provide unique opportunities to study roles of microbes in the evolution of floral traits that have mostly been overlooked in pollination ecology.
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spelling doaj.art-7bdef441b16848b18fe03ebe125b23d22022-12-22T00:22:29ZengWileyEnvironmental DNA2637-49432022-05-014356557910.1002/edn3.271Contrasting microbial communities on male and female flowers of a dioecious plant, Mallotus japonicus (Euphorbiaceae)Maxime Marre0Masayuki Ushio1Shoko Sakai2Center for Ecological Research Kyoto University Otsu JapanCenter for Ecological Research Kyoto University Otsu JapanCenter for Ecological Research Kyoto University Otsu JapanAbstract Flowers play a central role in plant reproduction by dispersing and receiving pollen grains delivered by animal vectors or air. They are rich in various nutrients, and therefore, provide an ideal habitat for many microbes. Recent studies have revealed that flower microbial communities can be highly variable among species, individuals, or even floral parts. However, sexual differences in flower microbial communities have rarely been investigated. In this study, we analyzed the flower prokaryotic communities of a dioecious plant (male and female flowers are produced on different individuals), Mallotus japonicus, in its natural habitat in Otsu, Japan. Using 16S rRNA amplicon sequencing, we found a differentiation in microbial communities between male and female flowers. Procaryotes on male flowers were relatively diverse, and included several dominant amplicon sequence variants (ASVs), mainly from the Gammaproteobacteria. These ASVs were also found on the body surface of flower visitor insects, suggesting that the visitors dispersed these microbes when they visited the flowers. On the other hand, female flower samples were overwhelmingly dominated by a single bacterial sequence from the Alphaproteobacteria, which showed a peak of relative abundance at the middle of the flowering season. The bacterium had already been present at anthesis, and its relative abundance on flower visitors was low. Flower visitors may have little effect on the microbial composition on female flowers. The lower diversity of microbes on female flowers than on male flowers suggests that the female flowers function as a stronger filter, possibly related to a strong defense against antagonists. These differences may be associated with different reproductive strategies of male and female flowers. This study indicates that dioecious plants provide unique opportunities to study roles of microbes in the evolution of floral traits that have mostly been overlooked in pollination ecology.https://doi.org/10.1002/edn3.271dioecyflower microbial communityMallotus japonicuspollinationsexual difference
spellingShingle Maxime Marre
Masayuki Ushio
Shoko Sakai
Contrasting microbial communities on male and female flowers of a dioecious plant, Mallotus japonicus (Euphorbiaceae)
Environmental DNA
dioecy
flower microbial community
Mallotus japonicus
pollination
sexual difference
title Contrasting microbial communities on male and female flowers of a dioecious plant, Mallotus japonicus (Euphorbiaceae)
title_full Contrasting microbial communities on male and female flowers of a dioecious plant, Mallotus japonicus (Euphorbiaceae)
title_fullStr Contrasting microbial communities on male and female flowers of a dioecious plant, Mallotus japonicus (Euphorbiaceae)
title_full_unstemmed Contrasting microbial communities on male and female flowers of a dioecious plant, Mallotus japonicus (Euphorbiaceae)
title_short Contrasting microbial communities on male and female flowers of a dioecious plant, Mallotus japonicus (Euphorbiaceae)
title_sort contrasting microbial communities on male and female flowers of a dioecious plant mallotus japonicus euphorbiaceae
topic dioecy
flower microbial community
Mallotus japonicus
pollination
sexual difference
url https://doi.org/10.1002/edn3.271
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