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      Seed and Root Endophytic Fungi in a Range Expanding and a Related Plant Species

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          Abstract

          Climate change is accelerating the spread of plants and their associated species to new ranges. The differences in range shift capacity of the various types of species may disrupt long-term co-evolved relationships especially those belowground, however, this may be less so for seed-borne endophytic microbes. We collected seeds and soil of the range-expanding Centaurea stoebe and the congeneric Centaurea jacea from three populations growing in Slovenia (native range of both Centaurea species) and the Netherlands (expanded range of C. stoebe, native range of C. jacea). We isolated and identified endophytic fungi directly from seeds, as well as from roots of the plants grown in Slovenian, Dutch or sterilized soil to compare fungal endophyte composition. Furthermore, we investigated whether C. stoebe hosts a reduced community composition of endophytes in the expanded range due to release from plant-species specific fungi while endophyte communities in C. jacea in both ranges are similar. We cultivated 46 unique and phylogenetically diverse endophytes. A majority of the seed endophytes resembled potential pathogens, while most root endophytes were not likely to be pathogenic. Only one endophyte was found in both roots and seeds, but was isolated from different plant species. Unexpectedly, seed endophyte diversity of southern C. stoebe populations was lower than of populations from the north, while the seed endophyte community composition of northern C. stoebe populations was significantly different southern C. stoebe as well as northern and southern C. jacea populations. Root endophyte diversity was considerably lower in C. stoebe than in C. jacea independent of plant and soil origin, but this difference disappeared when plants were grown in sterile soils. We conclude that the community composition of fungal endophytes not only differs between related plant species but also between populations of plants that expand their range compared to their native habitat. Our results suggest that fungal endophytes of two Centaurea species are not able to systemically infect plants. We highlight that endophytes remain poorly studied and further work should investigate the functional importance of endophytes.

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          Most cited references60

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          Ecological and Evolutionary Responses to Recent Climate Change

          Ecological changes in the phenology and distribution of plants and animals are occurring in all well-studied marine, freshwater, and terrestrial groups. These observed changes are heavily biased in the directions predicted from global warming and have been linked to local or regional climate change through correlations between climate and biological variation, field and laboratory experiments, and physiological research. Range-restricted species, particularly polar and mountaintop species, show severe range contractions and have been the first groups in which entire species have gone extinct due to recent climate change. Tropical coral reefs and amphibians have been most negatively affected. Predator-prey and plant-insect interactions have been disrupted when interacting species have responded differently to warming. Evolutionary adaptations to warmer conditions have occurred in the interiors of species' ranges, and resource use and dispersal have evolved rapidly at expanding range margins. Observed genetic shifts modulate local effects of climate change, but there is little evidence that they will mitigate negative effects at the species level.
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            Fungal endophytes: diversity and functional roles.

            All plants in natural ecosystems appear to be symbiotic with fungal endophytes. This highly diverse group of fungi can have profound impacts on plant communities through increasing fitness by conferring abiotic and biotic stress tolerance, increasing biomass and decreasing water consumption, or decreasing fitness by altering resource allocation. Despite more than 100 yr of research resulting in thousands of journal articles, the ecological significance of these fungi remains poorly characterized. Historically, two endophytic groups (clavicipitaceous (C) and nonclavicipitaceous (NC)) have been discriminated based on phylogeny and life history traits. Here, we show that NC-endophytes represent three distinct functional groups based on host colonization and transmission, in planta biodiversity and fitness benefits conferred to hosts. Using this framework, we contrast the life histories, interactions with hosts and potential roles in plant ecophysiology of C- and NC-endophytes, and highlight several key questions for future work in endophyte biology.
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              FUNGAL ENDOPHYTES: A Continuum of Interactions with Host Plants

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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                29 August 2017
                2017
                : 8
                : 1645
                Affiliations
                [1] 1Department of Terrestrial Ecology, Netherlands Institute of Ecology Wageningen, Netherlands
                [2] 2Laboratory of Nematology, Wageningen University Wageningen, Netherlands
                [3] 3Institute of Biology, Scientific Research Centre of the Slovenian Academy of Sciences and Arts Ljubljana, Slovenia
                Author notes

                Edited by: Magdalena Frac, Institute of Agrophysics (PAN), Poland

                Reviewed by: Ram Prasad, Amity University, India; Birinchi Kumar Sarma, Banaras Hindu University, India

                *Correspondence: Stefan Geisen, s.geisen@ 123456nioo.knaw.nl

                This article was submitted to Fungi and Their Interactions, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2017.01645
                5581836
                28900420
                cb7aa9df-36fd-4202-a5dc-a888e7ae63f1
                Copyright © 2017 Geisen, Kostenko, Cnossen, ten Hooven, Vreš and van der Putten.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 30 May 2017
                : 15 August 2017
                Page count
                Figures: 5, Tables: 0, Equations: 0, References: 72, Pages: 11, Words: 0
                Funding
                Funded by: FP7 Ideas: European Research Council 10.13039/100011199
                Award ID: ERC-Adv 260-55290
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                endophytes,fungi,range expanding plant species,cultivation,phylogeny,soil,seeds,soil sterilization

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