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Wesley A. Bickford

Publications and source records attributed to Wesley A. Bickford.

13 recordsLinked to original sources

Comparative genomics reveals potential mechanisms of invasion in Phragmites australis (common reed)

Biological invasions are transforming ecosystems worldwide, yet the genomic bases enabling certain species to dominate new environments remain poorly understood. Phragmites australis , a widespread wetland grass with invasive and native subspecies co-occurring in North America, provides a powerful system to investigate genomic mechanisms of invasiveness. We generated independent chromosome-scale genome assemblies for invasive P. australis ssp. australis and co-occurring native ssp. americanus and used comparative genomic and transcriptomic analyses to identify lineage-specific innovations associated with invasive success. The invasive subspecies exhibits genomic novelties through functionally-biased single-copy orthologs, intronless genes, and subgenome expression asymmetry, along with a stress-ready basal transcriptome relative to the native subspecies. Following the removal of aboveground shoots (“cutback”), which measures the ability to recover from damage, the invasive subspecies undergoes stronger transcriptional reprogramming, increased shoot production, and higher biomass accumulation compared to the native. It also displays expansion of gene families and coordinately expressed gene modules that support resource mobilization, growth responses to light, and stress tolerance. Beyond Phragmites , comparative analyses across multiple grass genomes, including eight invasive species with related non-invasive species, revealed repeated expansion of gene families associated with abiotic stress tolerance and developmental regulation, suggesting convergent adaptive strategies in the grass family for invasive success. Together, these results demonstrate genomic architecture linked to invasion success and highlight potential targets for managing invasive grasses.

BioRxiv

Multi-year cut-to-drown management limits Phragmites australis growth, belowground resources, and rhizome viability in Great Lakes wetlands

The distribution and abundance of Phragmites in the Great Lakes coastal zone has expanded in part due to its unique ventilation physiology and its ability to take advantage of changes in lake levels over the past several decades. During an extended period of low lake levels in the early 2000s, Phragmites expanded into vast shallow water areas as lake bottoms were exposed. Many of those populations were able to persist when lake levels rose several years later. Here, we investigate a management strategy, known as cut-to-drown, that takes advantage of elevated water levels to effectively control Phragmites by cutting stems underwater, thereby drowning the plant and depleting its stored resources. We tested the impacts of cut timing and frequency on the effectiveness of the cut-to-drown strategy through a multi-year manipulative field study. After two seasons of treatments, we found a 92–99 % reduction in stem density, depending on cut timing. Carbohydrate reserves in rhizomes declined 75–92 %, such that rhizome viability was reduced by 73–100 %, depending on cut timing. We found that cutting continuously (every 2–3 weeks) throughout two growing seasons was the most effective way to implement cut-to-drown but provide evidence that less frequent cutting could produce similar results. Our study provides important evidence to inform best management practices for cut-to-drown. Particularly as lake level fluctuations become more frequent and extreme in the future, cut-to-drown could serve as a useful tool for limiting Phragmites’ ability to persist in high water environments.

Michigan, Ohio

Cell penetrating peptide-mediated delivery of gene-silencing nucleic acids to the invasive common reed Phragmites australis via foliar application

As a popular tool for gene function characterization and gene therapy, RNA interference (RNAi)-based gene silencing has been increasingly explored for potential applications to control invasive species. At least two major hurdles exist when applying this approach to invasive plants: (1) the design and screening of species- and gene-specific biomacromolecules (i.e., gene-silencing agents or GSAs) made of DNA, RNA, or peptides that can suppress the expression of target genes efficiently, and (2) the delivery vehicle needed to penetrate plant cell walls and other physical barriers (e.g., leaf cuticles). In this study, we investigated the cell-penetrating peptide (CPP)-mediated delivery of multiple types of GSAs (e.g., double-stranded RNA (dsRNA), artificial microRNA (amiRNA), and antisense oligonucleotide (ASO)) to knock down a putative phytoene desaturase ( PDS ) gene in the invasive common reed ( Phragmites australis spp. australis ). Both microscopic and quantitative gene expression evidence demonstrated the CPP-mediated internalization of GSA cargos and transient suppression of PDS expression in both treated and systemic leaves up to 7 days post foliar application. Although various GSA combinations and application rates and frequencies were tested, we observed limitations, including low gene-silencing efficiency and a lack of physiological trait alteration, likely owing to low CPP payload capacity and the incomplete characterization of the PDS-coding genes (e.g., the recent discovery of two PDS paralogs) in P. australis . Our work lays a foundation to support further research toward the development of convenient, cost-effective, field-deployable, and environmentally benign gene-silencing technologies for invasive P. australis management.

Mississippi, Ohio

Phragmites management in high water: Cutting plants under water limits biomass production, carbohydrate storage, and rhizome viability

Invasion of Phragmites australis (common reed) in wetlands throughout North America, and particularly the Laurentian Great Lakes Basin, poses significant ecological problems. The extended period of low Great Lakes water levels from 2000 to 2013 created conditions for large expansions of Phragmites in the Great Lakes coastal zone. The following extended period of high water in the Great Lakes during late 2010’s, culminating in record high lake levels in 2020 allowed managers to take advantage of high water by using a cut-to-drown management strategy (i.e., cutting plants below the water surface to stop the flow of atmospheric gases) to control Phragmites populations. To examine the efficacy of a cut-to-drown control strategy, we conducted a controlled-greenhouse study that tested the effect of submergence and timing of cutting (early or late in growing season) on Phragmites growth and viability post treatment. To evaluate Phragmites growth and viability, we measured belowground biomass, rhizome non-structural carbohydrate content (NSC), and rhizome viability following a cut-to-drown treatment. Applying a cut-to-drown treatment reduced average belowground biomass production up to 99%, limited rhizome NSC content up to 83%, and inhibited rhizome viability, regardless of timing of cutting treatments. These results suggest that under high-water conditions, utilizing a cut-to-drown strategy has potential for being a useful control mechanism for Phragmites . However, further research is needed to determine to what extent these results will lead to sustained reductions in growth and viability under field conditions, where rhizome belowground biomass and storage capacity are much larger.

Wetlands Ecology and Management

Experimentally induced dieback conditions limit Phragmites australis growth

Phragmites australis is a cosmopolitan grass species common in wetland ecosystems across the world. In much of North America, the non-native subspecies of Phragmites threatens wetland biodiversity, hinders recreation, and is a persistent problem for natural resource managers. In other parts of the world, populations are in decline, as Reed Die-Back Syndrome (RDBS) plagues some Phragmites stands in its native range. RDBS is defined by a clumped growth form, stunted root and shoot growth, premature senescence, and shoot death. RDBS has been associated with a build-up of short-chain fatty acids (SCFAs) and altered bacterial and oomycete communities in soils, but the exact causes are unknown. To control invasive Phragmites populations, we sought to develop treatments that mimic the conditions of RDBS. We applied various SCFA treatments at various concentrations to mesocosm soils growing either Phragmites or native wetland plants. We found that the high-concentration SCFA treatments applied weekly induced strong significant declines in above- and belowground biomass of Phragmites . Declines were significant but slightly weaker in native species. In addition, soil bacterial abundance increased, diversity decreased, and bacterial community composition significantly differed following treatments, such that treated pots maintained a higher relative abundance of Pseudomonadaceae and fewer Acidobacteriaceae than untreated pots. Our results suggest that application of SCFAs to Phragmites can lead to stunted plants and altered soil bacterial communities similar to populations affected by RDBS. However, the lack of species-specificity and intensive application rate may not make this treatment ideal as a widespread management tool.

Michigan, Ohio

Plant effects on and response to soil microbes in native and non-native Phragmites australis

Plant–soil feedbacks (PSFs) mediate plant community dynamics and may plausibly facilitate plant invasions. Microbially mediated PSFs are defined by plant effects on soil microbes and subsequent changes in plant performance (responses), both positive and negative. For microbial interactions to benefit invasive plants disproportionately, native and invasive plants must either (1) have different effects on and responses to soil microbial communities or (2) only respond differently to similar microbial communities. In other words, invasive plants do not need to cultivate different microbial communities than natives if they respond differently to them. However, effects and responses are not often explored separately, making it difficult to determine the underlying causes of performance differences. We performed a reciprocal-transplant PSF experiment with multiple microbial inhibition treatments to determine how native and non-native lineages of Phragmites australis affect and respond to soil bacteria, fungi, and oomycetes. Non-native Phragmites is a large, fast-growing, cosmopolitan invasive plant, whereas the North American native variety is comparatively smaller, slower growing, and typically considered a desirable wetland plant. We identified the effects of each plant lineage on soil microbes using DNA meta-barcoding and linked plant responses to microbial communities. Both Phragmites lineages displayed equally weak, insignificant PSFs. We found evidence of slight differential effects on microbial community composition, but no significant differential plant responses. Soils conditioned by each lineage differed only slightly in bacterial community composition, but not in fungal composition. Additionally, native and non-native Phragmites lineages did not significantly differ in their response to similar soil microbial communities. Neither lineage appreciably differed when plant biomass was compared between those grown in sterile and live soils. Targeted microbial inhibitor treatments revealed both lineages were negatively impacted by soil bacteria, but the negative response was stronger in non-native Phragmites . These observations were opposite of expectations from invasion theory and imply that the success of non-native Phragmites , relative to the native lineage, does not result from its interaction with soil microorganisms. More broadly, quantifying plant effects on, and responses to soil microbes separately provides detailed and nuanced insight into plant-microbial interactions and their role in invasions, which could inform management outcomes for invasive plants.

Ecological Applications

Differences in rhizosphere microbial communities between native and non‐native Phragmites australis may depend on stand density

Microorganisms surrounding plant roots may benefit invasive species through enhanced mutualism or decreased antagonism, when compared to surrounding native species. We surveyed the rhizosphere soil microbiome of a prominent invasive plant, Phragmites australis , and its co‐occurring native subspecies for evidence of microbial drivers of invasiveness. If the rhizosphere microbial community is important in driving plant invasions, we hypothesized that non‐native Phragmites would cultivate a different microbiome from native Phragmites , containing fewer pathogens, more mutualists, or both. We surveyed populations of native and non‐native Phragmites across Michigan and Ohio USA, and we described rhizosphere microbial communities using culture‐independent next‐generation sequencing. We found little evidence that native and non‐native Phragmites cultivate distinct bacterial, fungal, or oomycete rhizosphere communities. Microbial community differences in our Michigan survey were not associated with plant lineage but were mainly driven by environmental factors, such as soil saturation and nutrient concentrations. Intensive sampling along transects consisting of dense monocultures of each lineage and mixed zones revealed bacterial community differences between lineages in dense monoculture, but not in mixture. We found no evidence of functional differences in the microbial communities surrounding each lineage. We extrapolate that the invasiveness of non‐native Phragmites , when compared to its native congener, does not result from the differential cultivation of beneficial or antagonistic rhizosphere microorganisms.

Michigan, Ohio

Growth and behavior of North American microbes on Phragmites australis leaves

Phragmites australis subsp. australis is a cosmopolitan wetland grass that is invasive in many regions of the world, including North America, where it co-occurs with the closely related Phragmites australis subsp. americanus. Because the difference in invasive behavior is unlikely to be related to physiological differences, we hypothesize that interactions with unique members of their microbiomes may significantly affect the behavior of each subspecies. Therefore, we systematically inoculated both plant lineages with a diverse array of 162 fungal and bacterial isolates to determine which could (1) differentiate between Phragmites hosts, (2) infect leaves at various stages of development, or (3) obtain plant-based carbon saprophytically. We found that many of the microbes isolated from Phragmites leaves behave as saprophytes. Only 1% (two taxa) were determined to be strong pathogens, 12% (20 taxa) were weakly pathogenic, and the remaining 87% were nonpathogenic. None of the isolates clearly discriminated between host plant lineages, and the Phragmites cuticle was shown to be a strong nonspecific barrier to infection. These results largely agree with the broad body of literature on leaf-associated phyllosphere microbes in Phragmites.

Microorganisms

Intraspecific and biogeographical variation in foliar fungal communities and pathogen damage of native and invasive Phragmites australis

Aim Recent research has highlighted that the relationship between species interactions and latitude can differ between native and invasive plant taxa, generating biogeographical heterogeneity in community resistance to plant invasions. In the first study with foliar pathogens, we tested whether co‐occurring native and invasive lineages of common reed ( Phragmites australis ) exhibit non‐parallel latitudinal gradients in foliar fungal communities, pathogen susceptibility and damage, and whether these biogeographical patterns can influence the success of invasion. Location North America. Time period 2015–2017. Major taxa studied Perennial grass P. australis . Methods We surveyed 35 P. australis field populations, spanning 17° latitude and comprising four phylogeographical lineages, including one endemic to North America and one invasive from Europe. For each population, we quantified the percentage of leaf pathogen damage and cultured fungi from diseased leaves, which we identified using molecular tools. To assess whether latitudinal gradients in pathogen damage had a genetic basis, we inoculated plants from 73 populations with four putative pathogens in a complementary common garden experiment and measured P. australis susceptibility (i.e., diseased leaf area). Results We isolated 84 foliar fungal taxa. Phragmites australis lineage influenced fungal community composition but not diversity. Despite the invasive European P. australis lineage being the least susceptible to three of the four pathogens tested in the common garden experiment, pathogen damage in the field was similar between native and invasive lineages, providing no evidence that release from foliar pathogens contributes to the success of invasion. Genetically based latitudinal gradients in pathogen susceptibility observed in the common garden were isolate specific and obscured by local environmental conditions in the field, where pathogen damage was threefold higher for northern compared with southern populations, regardless of lineage. Main conclusions Our results highlight that host plant lineage and genetically based biogeographical gradients strongly influence foliar fungal communities and pathogen susceptibility, but do not translate to patterns of pathogen damage observed in the field.

Global Ecology and Biogeography

Root endophytes and invasiveness: no difference between native and non‐native Phragmites in the Great Lakes Region

Microbial interactions could play an important role in plant invasions. If invasive plants associate with relatively more mutualists or fewer pathogens than their native counterparts, then microbial communities could foster plant invasiveness. Studies examining the effects of microbes on invasive plants commonly focus on a single microbial group (e.g., bacteria) or measure only plant response to microbes, not documenting the specific taxa associating with invaders. We surveyed root microbial communities associated with co‐occurring native and non‐native lineages of Phragmites australis, across Michigan, USA. Our aim was to determine whether (1) plant lineage was a stronger predictor of root microbial community composition than environmental variables and (2) the non‐native lineage associated with more mutualistic and/or fewer pathogenic microbes than the native lineage. We used microscopy and culture‐independent molecular methods to examine fungal colonization rate and community composition in three major microbial groups (bacteria, fungi, and oomycetes) within roots. We also used microbial functional databases to assess putative functions of the observed microbial taxa. While fungal colonization of roots was significantly higher in non‐native Phragmites than the native lineage, we found no differences in root microbial community composition or potential function between the two Phragmites lineages. Community composition did differ significantly by site, with soil saturation playing a significant role in structuring communities in all three microbial groups. The relative abundance of some specific bacterial taxa did differ between Phragmites lineages at the phylum and genus level (e.g., Proteobacteria, Firmicutes ). Purported function of root fungi and respiratory mode of root bacteria also did not differ between native and non‐native Phragmites . We found no evidence that native and non‐native Phragmites harbored distinct root microbial communities; nor did those communities differ functionally. Therefore, if the trends revealed at our sites are widespread, it is unlikely that total root microbial communities are driving invasion by non‐native Phragmites plants.

Ecosphere

Fungal endophytes from seeds of invasive, non-native Phragmites australis and their potential role in germination and seedling growth

Background and aims We characterized fungal endophytes of seeds of invasive, non-native Phragmites from three sites in the Great Lakes region to determine if fungal symbiosis could contribute to invasiveness through their effects on seed germination and seedling growth. Methods Field-collected seeds were surface sterilized and plated on agar to culture endophytes for ITS sequencing. Prevalence of specific endophytes from germinated and non-germinated seeds, and from seedlings, was compared. Results One-third of 740 seeds yielded endophyte isolates. Fifteen taxa were identified with Alternaria sp. representing 54% of all isolates followed by Phoma sp. (21%) and Penicillium corylophilum (12%). Overall germination of seeds producing an isolate (36%) was significantly higher than seeds not producing an isolate (20%). Penicillium in particular was strongly associated with increased germination of seeds from one site. Sixty-three isolates and 11 taxa were also obtained from 30 seedlings where Phoma , Penicillium and Alternaria respectively were most prevalent. There was a significant effect of isolating an endophyte from the seed on seedling growth. Conclusions These results suggest that many endophyte taxa are transmitted in seeds and can increase seed germination and seedling growth of invasive Phragmites . The role of fungal endophytes in host establishment, growth and invasiveness in nature requires further research.

Michigan, Ohio

Diversity of fungal endophytes in non-native Phragmites australis in the Great Lakes

Plant–microbial interactions may play a key role in plant invasions. One common microbial interaction takes place between plants and fungal endophytes when fungi asymptomatically colonize host plant tissues. The objectives of this study were to isolate and sequence fungal endophytes colonizing non-native Phragmites australis in the Great Lakes region to evaluate variation in endophyte community composition among three host tissue types and three geographical regions. We collected entire ramets from multiple clones and populations, surface sterilized plant tissues, and plated replicate tissue samples from leaves, stems, and rhizomes on corn meal agar plates to culture and isolate fungal endophytes. Isolates were then subjected to Sanger sequencing of the ITS region of the nuclear ribosomal DNA. Sequences were compared to fungal databases to define operational taxonomic units (OTUs) that were analyzed statistically for community composition. In total, we obtained 173 endophyte isolates corresponding to 55 OTUs, 39 of which were isolated only a single time. The most common OTU corresponded most closely to Sarocladium strictum and comprised 25 % of all fungal isolates. More OTUs were found in stem tissues, but endophyte diversity was greatest in rhizome tissues. PERMANOVA analyses indicated significant differences in endophyte communities among tissue types, geographical regions, and the interaction between those factors, but no differences among individual ramets were detected. The functional role of the isolated endophytes is not yet known, but one genus isolated here ( Stagonospora ) has been reported to enhance Phragmites growth. Understanding the diversity and functions of Phragmites endophytes may provide targets for control measures based on disrupting host plant/endophyte interactions.

Great Lakes region

Advancing the science of microbial symbiosis to support invasive species management: a case study on Phragmites in the Great Lakes

A growing body of literature supports microbial symbiosis as a foundational principle for the competitive success of invasive plant species. Further exploration of the relationships between invasive species and their associated microbiomes, as well as the interactions with the microbiomes of native species, can lead to key new insights into invasive success and potentially new and effective control approaches. In this manuscript, we review microbial relationships with plants, outline steps necessary to develop invasive species control strategies that are based on those relationships, and use the invasive plant species Phragmites australis (common reed) as an example of how development of microbial-based control strategies can be enhanced using a collective impact approach. The proposed science agenda, developed by the Collaborative for Microbial Symbiosis and Phragmites Management, contains a foundation of sequential steps and mutually-reinforcing tasks to guide the development of microbial-based control strategies for Phragmites and other invasive species. Just as the science of plant-microbial symbiosis can be transferred for use in other invasive species, so too can the model of collective impact be applied to other avenues of research and management.

Frontiers in Microbiology