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

Front Plant Sci. 2023 Dec 13:14:1274746. doi: 10.3389/fpls.2023.1274746. eCollection 2023.

Abstract

Introduction: The 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.

Methods: Metagenomic 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.

Results: We 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.

Discussion: Our 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.

Keywords: Cornus; allopatric divergence; alpha and beta diversity; bacterial 16S rDNA; comparative analyses; foliar endophytic community; fungal ITS; phylogeny.

Associated data

  • Dryad/10.5061/dryad.s7h44j1cf

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was funded by U.S. National Science Foundation grants DEB-1442161 to QX and WS and DEB-1442280 to PS and DS and the Shiu-Ying Hu Student/Post-Doctoral Exchange Award from the Arnold Arboretum of Harvard University to WZ. This work also benefited from the USDA National Institute of Food and Agriculture, Hatch project 02718.