Foliar endophyte diversity in Eastern Asian-Eastern North American disjunct tree species – influences of host identity, environment, phylogeny, and geographic isolation

IntroductionThe well-known eastern Asian (EA) and eastern North American (ENA) floristic disjunction provides a unique system for biogeographic and evolutionary studies. Despite considerable interest in the disjunction, few studies have investigated the patterns and their underlying drivers of allop...

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Main Authors: Wenbin Zhou, Wei Shi, Pamela S. Soltis, Douglas E. Soltis, Qiu-Yun (Jenny) Xiang
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-12-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1274746/full
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author Wenbin Zhou
Wei Shi
Pamela S. Soltis
Pamela S. Soltis
Douglas E. Soltis
Douglas E. Soltis
Qiu-Yun (Jenny) Xiang
author_facet Wenbin Zhou
Wei Shi
Pamela S. Soltis
Pamela S. Soltis
Douglas E. Soltis
Douglas E. Soltis
Qiu-Yun (Jenny) Xiang
author_sort Wenbin Zhou
collection DOAJ
description IntroductionThe well-known eastern Asian (EA) and eastern North American (ENA) floristic disjunction provides a unique system for biogeographic and evolutionary studies. Despite considerable interest in the disjunction, few studies have investigated the patterns and their underlying drivers of allopatric divergence in sister species or lineages isolated in the two areas. Endophyte diversity and assembly in disjunct sister taxa, as an ecological trait, may have played an important role in the processes of allopatric evolution, but no studies have examined endophytes in these lineages. Here we compared foliar endophytic fungi and bacteria-archaea (FEF and FEB) in 17 EA-ENA disjunct species or clade pairs from genera representing conifers and 10 orders of five major groups of angiosperms and 23 species of Cornus from EA and North America. MethodsMetagenomic sequencing of fungal ITS and bacterial-archaeal 16S rDNA was used to capture the foliar endophytic communities. Alpha and beta diversity of fungi and bacteria were compared at multiple scales and dimensions to gain insights into the relative roles of historical geographic isolation, host identity, phylogeny, and environment from samples at different sites in shaping endophytic diversity patterns. ResultsWe found that beta diversity of endophytes varied greatly among plant individuals within species and between species among genera at the same sampling site, and among three sampling sites, but little variation between region-of-origin of all plant species (EA vs ENA) and between EA-ENA disjunct counterparts within genera. Various numbers of indicator fungal species differing in abundance were identified for each plant genus and Cornus species. An overall significant correlation between endophyte community dissimilarity and phylogenetic distance of plants was detected among the disjunct genera but not among species of Cornus. However, significant correlations between beta diversities at different taxonomic scales of endophytes and phylogenetic distances of Cornus species were observed. DiscussionOur results suggest important roles of host identity and environment (sampling sites), and a likely minor role of phylogenetic divergence and historical biogeographic isolation in shaping the pattern of foliar endophyte diversity and assembly in the EA-ENA disjunct genera and Cornus. The results lead to a hypothesis that the sister taxa in EA and ENA likely differ in FEF and FEB when growing in native habitats due to differences in local environments, which may potentially drive allopatric divergence of the functional features of species.
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spelling doaj.art-a4e45db7568a4ea691d72bc428e95f4c2023-12-13T05:34:26ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-12-011410.3389/fpls.2023.12747461274746Foliar endophyte diversity in Eastern Asian-Eastern North American disjunct tree species – influences of host identity, environment, phylogeny, and geographic isolationWenbin Zhou0Wei Shi1Pamela S. Soltis2Pamela S. Soltis3Douglas E. Soltis4Douglas E. Soltis5Qiu-Yun (Jenny) Xiang6Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC, United StatesDepartment of Crop and Soil Sciences, North Carolina State University, Raleigh, NC, United StatesFlorida Museum of Natural History, University of Florida, Gainesville, FL, United StatesDepartment of Biology, University of Florida, Gainesville, FL, United StatesFlorida Museum of Natural History, University of Florida, Gainesville, FL, United StatesDepartment of Biology, University of Florida, Gainesville, FL, United StatesDepartment of Plant and Microbial Biology, North Carolina State University, Raleigh, NC, United StatesIntroductionThe well-known eastern Asian (EA) and eastern North American (ENA) floristic disjunction provides a unique system for biogeographic and evolutionary studies. Despite considerable interest in the disjunction, few studies have investigated the patterns and their underlying drivers of allopatric divergence in sister species or lineages isolated in the two areas. Endophyte diversity and assembly in disjunct sister taxa, as an ecological trait, may have played an important role in the processes of allopatric evolution, but no studies have examined endophytes in these lineages. Here we compared foliar endophytic fungi and bacteria-archaea (FEF and FEB) in 17 EA-ENA disjunct species or clade pairs from genera representing conifers and 10 orders of five major groups of angiosperms and 23 species of Cornus from EA and North America. MethodsMetagenomic sequencing of fungal ITS and bacterial-archaeal 16S rDNA was used to capture the foliar endophytic communities. Alpha and beta diversity of fungi and bacteria were compared at multiple scales and dimensions to gain insights into the relative roles of historical geographic isolation, host identity, phylogeny, and environment from samples at different sites in shaping endophytic diversity patterns. ResultsWe found that beta diversity of endophytes varied greatly among plant individuals within species and between species among genera at the same sampling site, and among three sampling sites, but little variation between region-of-origin of all plant species (EA vs ENA) and between EA-ENA disjunct counterparts within genera. Various numbers of indicator fungal species differing in abundance were identified for each plant genus and Cornus species. An overall significant correlation between endophyte community dissimilarity and phylogenetic distance of plants was detected among the disjunct genera but not among species of Cornus. However, significant correlations between beta diversities at different taxonomic scales of endophytes and phylogenetic distances of Cornus species were observed. DiscussionOur results suggest important roles of host identity and environment (sampling sites), and a likely minor role of phylogenetic divergence and historical biogeographic isolation in shaping the pattern of foliar endophyte diversity and assembly in the EA-ENA disjunct genera and Cornus. The results lead to a hypothesis that the sister taxa in EA and ENA likely differ in FEF and FEB when growing in native habitats due to differences in local environments, which may potentially drive allopatric divergence of the functional features of species.https://www.frontiersin.org/articles/10.3389/fpls.2023.1274746/fullallopatric divergenceCornuscomparative analysesfoliar endophytic communityfungal ITSbacterial 16S rDNA
spellingShingle Wenbin Zhou
Wei Shi
Pamela S. Soltis
Pamela S. Soltis
Douglas E. Soltis
Douglas E. Soltis
Qiu-Yun (Jenny) Xiang
Foliar endophyte diversity in Eastern Asian-Eastern North American disjunct tree species – influences of host identity, environment, phylogeny, and geographic isolation
Frontiers in Plant Science
allopatric divergence
Cornus
comparative analyses
foliar endophytic community
fungal ITS
bacterial 16S rDNA
title Foliar endophyte diversity in Eastern Asian-Eastern North American disjunct tree species – influences of host identity, environment, phylogeny, and geographic isolation
title_full Foliar endophyte diversity in Eastern Asian-Eastern North American disjunct tree species – influences of host identity, environment, phylogeny, and geographic isolation
title_fullStr Foliar endophyte diversity in Eastern Asian-Eastern North American disjunct tree species – influences of host identity, environment, phylogeny, and geographic isolation
title_full_unstemmed Foliar endophyte diversity in Eastern Asian-Eastern North American disjunct tree species – influences of host identity, environment, phylogeny, and geographic isolation
title_short Foliar endophyte diversity in Eastern Asian-Eastern North American disjunct tree species – influences of host identity, environment, phylogeny, and geographic isolation
title_sort foliar endophyte diversity in eastern asian eastern north american disjunct tree species influences of host identity environment phylogeny and geographic isolation
topic allopatric divergence
Cornus
comparative analyses
foliar endophytic community
fungal ITS
bacterial 16S rDNA
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1274746/full
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