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1. Diversity, taxonomic composition, and functional aspects of fungal communities in living, senesced, and fallen leaves at five sites across North America

   https://doi.org/10.7717/peerj.2768  

   U’Ren, Jana M. ; Arnold, A. Elizabeth ( December 2016 , PeerJ)

   Fungal endophytes inhabit symptomless, living tissues of all major plant lineages to form one of earth’s most prevalent groups of symbionts. Many reproduce from senesced and/or decomposing leaves and can produce extracellular leaf-degrading enzymes, blurring the line between symbiotrophy and saprotrophy. To better understand the endophyte–saprotroph continuum we compared fungal communities and functional traits of focal strains isolated from living leaves to those isolated from leaves after senescence and decomposition, with a focus on foliage of woody plants in five biogeographic provinces ranging from tundra to subtropical scrub forest.

   We cultured fungi from the interior of surface-sterilized leaves that were living at the time of sampling (i.e., endophytes), leaves that were dead and were retained in plant canopies (dead leaf fungi, DLF), and fallen leaves (leaf litter fungi, LLF) from 3–4 species of woody plants in each of five sites in North America. Our sampling encompassed 18 plant species representing two families of Pinophyta and five families of Angiospermae. Diversity and composition of fungal communities within and among leaf life stages, hosts, and sites were compared using ITS-partial LSU rDNA data. We evaluated substrate use and enzyme activity by a subset of fungi isolated only from living tissues vs. fungi isolated only from non-living leaves.

   Across the diverse biomes and plant taxa surveyed here, culturable fungi from living leaves were isolated less frequently and were less diverse than those isolated from non-living leaves. Fungal communities in living leaves also differed detectably in composition from communities in dead leaves and leaf litter within focal sites and host taxa, regardless of differential weighting of rare and abundant fungi. All focal isolates grew on cellulose, lignin, and pectin as sole carbon sources, but none displayed ligninolytic or pectinolytic activityin vitro. Cellulolytic activity differed among fungal classes. Within Dothideomycetes, activity differed significantly between fungi from living vs. non-living leaves, but such differences were not observed in Sordariomycetes.

   Although some fungi with endophytic life stages clearly persist for periods of time in leaves after senescence and incorporation into leaf litter, our sampling across diverse biomes and host lineages detected consistent differences between fungal assemblages in living vs. non-living leaves, reflecting incursion by fungi from the leaf exterior after leaf death and as leaves begin to decompose. However, fungi found only in living leaves do not differ consistently in cellulolytic activity from those fungi detected thus far only in dead leaves. Future analyses should consider Basidiomycota in addition to the Ascomycota fungi evaluated here, and should explore more dimensions of functional traits and persistence to further define the endophytism-to-saprotrophy continuum.

    

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2. Contributions of environmental and maternal transmission to the assembly of leaf fungal endophyte communities

   https://doi.org/10.1098/rspb.2021.0621  

   Bell-Dereske, Lukas P. ; Evans, Sarah E. ( August 2021 , Proceedings of the Royal Society B: Biological Sciences)

   null (Ed.)

   Leaf fungal endophytes (LFEs) contribute to plant growth and responses to stress. Fungi colonize leaves through maternal transmission, e.g. via the seed, and through environmental transmission, e.g. via aerial dispersal. The relative importance of these two pathways in assembly and function of the LFE community is poorly understood. We used amplicon sequencing to track switchgrass ( Panicum virgatum ) LFEs in a greenhouse and field experiment as communities assembled from seed endophytes and rain fungi (integration of wet and dry aerial dispersal) in germinating seeds, seedlings, and adult plants. Rain fungi varied temporally and hosted a greater portion of switchgrass LFE richness (greater than 65%) than were found in seed endophytes (greater than 25%). Exposure of germinating seeds to rain inoculum increased dissimilarity between LFE communities and seed endophytes, increasing the abundance of rain-derived taxa, but did not change diversity. In the field, seedling LFE composition changed more over time, with a decline in seed-derived taxa and an increase in richness, in response to environmental transmission than LFEs of adult plants. We show that environmental transmission is an important driver of LFE assembly, and likely plant growth, but its influence depends on both the conditions at the time of colonization and plant life stage. 

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3. Influence of Plant Host and Organ, Management Strategy, and Spore Traits on Microbiome Composition

   https://doi.org/10.1094/PBIOMES-08-19-0045-R  

   Gdanetz, Kristi ; Noel, Zachary ; Trail, Frances ( January 2021 , Phytobiomes Journal)

   null (Ed.)

   Microbiomes from maize and soybean were characterized in a long-term three-crop rotation research site, under four different land management strategies, to begin unraveling the effects of common farming practices on microbial communities. The fungal and bacterial communities of leaves, stems, and roots in host species were characterized across the growing season using amplicon sequencing and compared with the results of a similar study on wheat. Communities differed across hosts and among plant growth stages and organs, and these effects were most pronounced in the bacterial communities of the wheat and maize phyllosphere. Roots consistently showed the highest number of bacterial operational taxonomic units compared with aboveground organs, whereas the α-diversity of fungi was similar between above- and belowground organs. Network analyses identified putatively influential members of the microbial communities of the three host plant species. The fungal taxa specific to roots, stems, or leaves were examined to determine whether the specificity reflected their life histories based on previous studies. The analysis suggests that fungal spore traits are drivers of organ specificity in the fungal community. Identification of influential taxa in the microbial community and understanding how community structure of specific crop organs is formed will provide a critical resource for manipulations of microbial communities. The ability to predict how organ-specific communities are influenced by spore traits will enhance our ability to introduce them sustainably. 

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4. Salinity legacy: Foliar microbiome's history affects mutualist‐conferred salinity tolerance

   https://doi.org/10.1002/ecy.3679  

   Subedi, Suresh C. ; Allen, Preston ; Vidales, Rosario ; Sternberg, Leonel ; Ross, Michael ; Afkhami, Michelle E. ( April 2022 , Ecology)

   The rapid human‐driven changes in the environment during the Anthropocene have placed extreme stress on many plants and animals. Beneficial interactions with microorganisms may be crucial for ameliorating these stressors and facilitating the ecosystem services host organisms provide. Foliar endophytes, microorganisms that reside within leaves, are found in essentially all plants and can provide important benefits (e.g., enhanced drought tolerance or resistance to herbivory). However, it remains unclear how important the legacy effects of the abiotic stressors that select on these microbiomes are for affecting the degree of stress amelioration provided to their hosts. To elucidate foliar endophytes' role in host‐plant salt tolerance, especially if salinity experienced in the field selects for endophytes that are better suited to improve the salt tolerance of their hosts, we combined field collections of 90 endophyte communities from 30 sites across the coastal Everglades with a manipulative growth experiment assessing endophyte inoculation effects on host‐plant performance. Specifically, we grew >350 red mangrove (Rhizophora mangle) seedlings in a factorial design that manipulated the salinity environment the seedlings experienced (freshwater vs. saltwater), the introduction of field‐collected endophytes (live vs. sterilized inoculum), and the legacy of salinity stress experienced by these introduced endophytes, ranging from no salt stress (0 parts per thousand [ppt] salinity) to high salt stress (40 ppt) environments. We found that inoculation with field‐collected endophytes significantly increased mangrove performance across almost all metrics examined (15%–20% increase on average), and these beneficial effects typically occurred when the endophytes were grown in saltwater. Importantly, our study revealed the novel result that endophyte‐conferred salinity tolerance depended on microbiome salinity legacy in a key coastal foundation species. Salt‐stressed mangroves inoculated with endophyte microbiomes from high‐salinity environments performed, on average, as well as plants grown in low‐stress freshwater, while endophytes from freshwater environments did not relieve host salinity stress. Given the increasing salinity stress imposed by sea level rise and the importance of foundation species like mangroves for ecosystem services, our results indicate that consideration of endophytic associations and their salinity legacy may be critical for the successful restoration and management of coastal habitats.

    

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5. Elevated carbon dioxide reduces a common soybean leaf endophyte

   https://doi.org/10.1111/gcb.15716  

   Christian, Natalie ; Espino Basurto, Baldemar ; Toussaint, Amber ; Xu, Xinyan ; Ainsworth, Elizabeth A. ; Busby, Posy E. ; Heath, Katy D. ( June 2021 , Global Change Biology)

   Free‐air CO₂enrichment (FACE) experiments have elucidated how climate change affects plant physiology and production. However, we lack a predictive understanding of how climate change alters interactions between plants and endophytes, critical microbial mediators of plant physiology and ecology. We leveraged the SoyFACE facility to examine how elevated [CO₂] affected soybean (Glycine max)leaf endophyte communities in the field. Endophyte community composition changed under elevated [CO₂], including a decrease in the abundance of a common endophyte,Methylobacteriumsp. Moreover,Methylobacteriumabundance was negatively correlated with co‐occurring fungal endophytes. We then assessed howMethylobacteriumaffected the growth of co‐occurring endophytic fungi in vitro.Methylobacteriumantagonized most co‐occurring fungal endophytes in vitro, particularly when it was more established in culture before fungal introduction. Variation in fungal response toMethylobacteriumwithin a single fungal operational taxonomic unit (OTU) was comparable to inter‐OTU variation. Finally, fungi isolated from elevated vs. ambient [CO₂] plots differed in colony growth and response toMethylobacterium, suggesting that increasing [CO₂] may affect fungal traits and interactions within the microbiome. By combining in situ and in vitro studies, we show that elevated [CO₂] decreases the abundance of a common bacterial endophyte that interacts strongly with co‐occurring fungal endophytes. We suggest that endophyte responses to global climate change will have important but largely unexplored implications for both agricultural and natural systems.

    

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