Fungal communities associated with plants often decrease in similarity as the distance between sampling sites increases (i.e., they demonstrate distance decay). In the southwestern USA, forests occur in highlands separated from one another by warmer, drier biomes with plant and fungal communities that differ from those at higher elevations. These disjunct forests are broadly similar in climate to one another, offering an opportunity to examine drivers of distance decay in plant-associated fungi across multiple ecologically similar yet geographically disparate landscapes. We examined ectomycorrhizal and foliar endophytic fungi associated with a dominant forest tree (Pinus ponderosa) in forests across ca. 550 km of geographic distance from northwestern to southeastern Arizona (USA). Both guilds of fungi showed distance decay, but drivers differed for each: ectomycorrhizal fungi are constrained primarily by dispersal limitation, whereas foliar endophytes are constrained by specific environmental conditions. Most ectomycorrhizal fungi were found in only a single forested area, as were many endophytic fungi. Such regional-scale perspectives are needed for baseline estimates of fungal diversity associated with forest trees at a landscape scale, with attention to the sensitivity of different guilds of fungal symbionts to decreasing areas of suitable habitat, increasing disturbance, and related impacts of climate change.
One contribution of 16 to a theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.Electronic supplementary material is available online at https://dx.Herbarium specimens represent important records of morphological and genetic diversity of plants that inform questions relevant to global change, including species distributions, phenology and functional traits. It is increasingly appreciated that plant microbiomes can influence these aspects of plant biology, but little is known regarding the historic distribution of microbes associated with plants collected in the pre-molecular age. If microbiomes can be observed reliably in herbarium specimens, researchers will gain a new lens with which to examine microbial ecology, evolution, species interactions. Here, we describe a method for accessing historical plant microbiomes from preserved herbarium specimens, providing a proof of concept using two plant taxa from the imperiled boreal biome (Andromeda polifolia and Ledum palustre subsp. groenlandicum, Ericaceae). We focus on fungal endophytes, which occur within symptomless plant tissues such as leaves. Through a three-part approach (i.e. culturing, cloning and next-generation amplicon sequencing via the Illumina MiSeq platform, with extensive controls), we examined endophyte communities in dried, pressed leaves that had been processed as regular herbarium specimens and stored at room temperature in a herbarium for four years. We retrieved only one endophyte in culture, but cloning and especially the MiSeq analysis revealed a rich community of foliar endophytes. The phylogenetic distribution and diversity of endophyte assemblages, especially among the Ascomycota, resemble endophyte communities from fresh plants collected in the boreal biome. We could distinguish communities of endophytes in each plant species and differentiate likely endophytes from fungi that could be surface contaminants. Taxa found by cloning were observed in the larger MiSeq dataset, but species richness was greater when subsets of the same tissues were evaluated with the MiSeq approach. Our findings provide a proof of concept for capturing endophyte DNA from herbarium specimens, supporting the importance of herbarium records as roadmaps for understanding the dynamics of plant-associated microbial biodiversity in the Anthropocene.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.
Biodiversity collections contain a wealth of information encapsulated both in specimens and in their metadata, providing the foundation for diverse studies in fields such as ecology. Yet biodiversity repositories can present a challenge for ecological inferences because collections rarely are structured with ecological questions in mind: collections may be opportunistic in space or time, may focus on particular taxonomic groups, may reflect different collection strategies in different places or times, or may not be exhaustive in terms of retaining every specimen or having similar metadata for each record. In addition to its primary holdings, the Robert L. Gilbertson Mycological Herbarium at the University of Arizona holds a collection of living specimens of fungi isolated from the interior of healthy plants and lichens (i.e., endophytic and endolichenic fungi). Over the past decade, more than 7000 isolates from the southwestern United States were accessioned, including strains from diverse hosts in more than 50 localities across the biotically rich state of Arizona. This collection is distinctive in that metadata and barcode sequences are available for each specimen, many localities have been sampled with consistent methods, and all isolates obtained in surveys have been retained. Here, we use this herbarium collection to examine endophyte community structure in an ecological and evolutionary context. We then artificially restructure the collection to resemble collections more typical of biodiversity repositories, providing a case study for ecological insights that can be gleaned from collections that were not structured explicitly to address ecological questions. Overall, our analyses highlight the relevance of biogeography, climate, hosts, and geographic separation in endophyte community composition. This study showcases the importance of extensive metadata in collections and highlights the utility of biodiversity collections that can yield emergent insights from many surveys to answer ecological questions in mycology, ultimately providing information for understanding and conserving fungal biodiversity.
Our results suggest relatively tight linkages between EM and climate, soil chemistry, and plant communities. That FE appear less linked with these factors may speak to limitations of a culture-based approach, but more likely reflects the small spatial scale encompassed by our study. Future work should consider comparable methods for characterizing these functional groups, and additional transects to understand relationships of EM and FE to environmental factors that are likely to shift as a function of climate change.
Biological invasions are a leading ecological issue of the 21st century because of their worldwide contributions to biodiversity loss and degradation of ecosystem services. Answering general questions about the mechanisms facilitating the spread of successful invasives is key to understanding how to manage them moving forward. The success of introduced primary producers has often been attributed to superior competitive ability or to their release from natural enemies that constrained them in their native range. In contrast, nonnative primary producers can successfully invade and establish in new areas by releasing allelochemical compounds into the environment that are toxic to the native flora. The interactive effects of allelopathy and competition remain underexplored. Here, we evaluated the mechanism of invasion by Guinea grass, a globally distributed tallgrass from tropical and subtropical Africa with known allelopathic effects associated with 2-hydroxyphenylacetic acid (2HPAA). We asked if allelopathy and light availability interact to give Guinea grass a competitive advantage during seedling establishment in its introduced range. We used a fully factorial greenhouse experiment in which allelochemical concentrations and light availability treatments were based on empirical measurements of these variables at an invaded site in South Texas. Seedling recruitment and growth were assessed for three native species and for Guinea grass itself. We also described the metabolome (the complete set of small molecules) of an invasive grass for the first time to facilitate a comparison of the effect of the known allelochemical 2HPAA with that of the whole-plant chemical extract. Shading and allelochemistry each reduced recruitment and growth by themselves, and a significant interaction of these stressors exacerbated the negative effects in the shade, resulting in short plants, low biomass, and ultimately decreased seedling recruitment. The whole-plant metabolomic extract had significantly stronger effects than pure 2HPAA, and these negative effects were intensified in
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