Transgenerational phenotypic responses to herbicide stress are more rapid than to shade and simulated herbivory in Arabidopsis.

Weeds in agricultural settings continually adapt to stresses from ecological and anthropogenic sources, in some cases leading to resistant populations. However, consequences of repeated sub-lethal exposure of these stressors on fitness and stress "memory" over generations remain poorly understood. We measured plant performance over a transgenerational experiment with Arabidopsis thaliana where plants were exposed to sub-lethal stress induced by the herbicides glyphosate or trifloxysulfuron, stresses from clipping or shading in either one (G1) or four successive generations (G1-G4), and control plants that never received stress. We found that fourth-generation (G4) plants that had been subjected to three generations of glyphosate or trifloxysulfuron stress produced higher post-stress biomass, seed weight, and rosette area as compared to that produced by plants that experienced stress only in the first generation (G1). By the same measure, clipping and shade were more influential on floral development time (shade) and seed weight (clipping) but did not show responsive phenotypes for vegetative metrics after multiple generations. Overall, we found that plants exhibited more rapid transgenerational vegetative "stress memory" to herbicides while reproductive plasticity was stressor dependent and similar between clipping/shade and anthropogenic stressors. Our study suggests that maternal plant stress memory aids next-generation plants to respond and survive better under the same stressors.

Implications of germination tolerances on invasion potential of Arthraxon hispidus.

Arthraxon hispidus is an introduced, rapidly spreading, and newly invasive grass in the eastern United States, yet little is known about the foundational biology of this aggressive invader. Germination responses to environmental factors including salinity, pH, osmotic potential, temperature, and burial depth were investigated to better understand its germination niche. Seeds from six populations in the Mid-Atlantic US germinated 95% with an average mean time to germination of 3.42 days of imbibition in the dark at 23°C. Germination occurred across a temperature range of 8-37°C and a pH range of 5-10 (≥83%), suggesting that neither pH nor temperature will limit germination in many environments. Arthraxon hispidus germination occurred in high salinity (342 mM NaCl) and osmotic potentials as low as -0.83MPa. The NaCl concentration required to reduce germination by 50% exceeded salinity concentrations found in soil and some brackish water saltmarsh systems. While drought adversely affects A. hispidus, 50% germination occurred at osmotic potentials ranging from -0.25 to -0.67 MPa. Given the climatic conditions of North America, drought stress is unlikely to restrict germination in large regions. Finally, emergence greatly decreased with burial depth. Emergence was reduced to 45% at 1-2 cm burial depths, and 0% at 8 cm. Emergence depths in concert with adequate moisture, germination across a range of temperatures, and rapid germination suggests A. hispidus' seed bank may be short-lived in moist environments, but further investigation is warranted. Given the broad abiotic tolerances of A. hispidus and a widespread native range, A. hispidus has the potential to germinate in novel territories beyond its currently observed invaded range.

Adaptive constraints at the range edge of a widespread and expanding invasive plant.

Identifying the factors that facilitate and limit invasive species' range expansion has both practical and theoretical importance, especially at the range edges. Here, we used reciprocal common garden experiments spanning the North/South and East/West range that include the North American core, intermediate and range edges of the globally invasive plant, Johnsongrass (Sorghum halepense) to investigate the interplay of climate, biotic interactions (i.e. competition) and patterns of adaptation. Our results suggest that the rapid range expansion of Johnsongrass into diverse environments across wide geographies occurred largely without local adaptation, but that further range expansion may be restricted by a fitness trade-off that limits population growth at the range edge. Interestingly, plant competition strongly dampened Johnsongrass growth but did not change the rank order performance of populations within a garden, though this varied among gardens (climates). Our findings highlight the importance of including the range edge when studying the range dynamics of invasive species, especially as we try to understand how invasive species will respond to accelerating global changes.

Horsenettle (Solanum carolinense) fruit bacterial communities are not variable across fine spatial scales.

Fruit house microbial communities that are unique from the rest of the plant. While symbiotic microbial communities complete important functions for their hosts, the fruit microbiome is often understudied compared to other plant organs. Fruits are reproductive tissues that house, protect, and facilitate the dispersal of seeds, and thus they are directly tied to plant fitness. Fruit microbial communities may, therefore, also impact plant fitness. In this study, we assessed how bacterial communities associated with fruit of Solanum carolinense, a native herbaceous perennial weed, vary at fine spatial scales (<0.5 km). A majority of the studies conducted on plant microbial communities have been done at large spatial scales and have observed microbial community variation across these large spatial scales. However, both the environment and pollinators play a role in shaping plant microbial communities and likely have impacts on the plant microbiome at fine scales. We collected fruit samples from eight sampling locations, ranging from 2 to 450 m apart, and assessed the fruit bacterial communities using 16S rRNA gene amplicon sequencing. Overall, we found no differences in observed richness or microbial community composition among sampling locations. Bacterial community structure of fruits collected near one another were not more different than those that were farther apart at the scales we examined. These fine spatial scales are important to obligate out-crossing plant species such as S. carolinense because they are ecologically relevant to pollinators. Thus, our results could imply that pollinators serve to homogenize fruit bacterial communities across these smaller scales.

Into the weeds: new insights in plant stress.

Weeds, plants that thrive in the face of disturbance, have eluded human's attempts at control for >12 000 years, positioning them as a unique group of extreme stress tolerators. The most successful weeds have a suite of traits that enable them to rapidly adapt to environments typified by stress, growing in hostile conditions or subject to massive destruction from agricultural practices. Through their ability to persist and adapt, weeds illuminate principles of evolution and provide insights into weed management and crop improvement. Here we highlight why the time is right to move beyond traditional model systems and leverage weeds to gain a deeper understanding of the mechanisms, adaptations, and genetic and physiological bases for stress tolerance.

Habitat Suitability and Establishment Limitations of a Problematic Liana.

The US native liana, poison ivy (Toxicodendron radicans), responsible for contact dermatitis in humans, is a competitive weed with great potential for expansion in disturbed habitats. To facilitate a better understanding of this threat, we sought to evaluate habitat suitability, population demography, and biotic interactions of poison ivy, using a series of complementary field studies in the two habitats where it most commonly occurs-forest interiors and edges. Of the 2500 seeds planted across both habitats, poison ivy initially colonized forest interiors (32% emergence) at a higher rate than edge habitats (16.5% emergence). However, forest interior seedlings were less likely to survive (interior n = 3; edge n = 15), which might be attributed to herbivore pressure when the seedlings were smaller in the less competitive forest interior. Once established, the poison ivy seedlings appeared to be more tolerant of herbivory, except that of large grazers such as deer. The early life stage of seedling emergence, survival, and establishment are critical in poison ivy success, with biotic pressure, especially from plant competition and deer, limiting recruitment. A suitable habitat of this expanding native liana would increase with increasing forest fragmentation, but might be buffered by the expanding deer population.

Intraspecific, ecotypic and home climate variation in photosynthetic traits of the widespread invasive grass Johnsongrass.

Despite their near ubiquity across global ecosystems, the underlying mechanisms contributing to the success of invasive plants remain largely unknown. In particular, ecophysiological traits, which are fundamental to plants' performance and response to their environment, are poorly understood with respect to geographic and climate space. We evaluated photosynthetic trait variation among populations, ecotypes and home climates (i.e. the climates from the locations they were collected) of the widespread and expanding invader Johnsongrass (Sorghum halepense). We found that populations vary in the maximum net photosynthetic flux and the light-saturated net photosynthetic rate, and that agricultural and non-agricultural ecotypes vary in apparent quantum yield and water-use efficiency (WUE). We also found that populations from warmer home climates had lower dark respiration rates, light compensation points and WUEs. As Johnsongrass expands across the USA the abiotic and biotic environments are driving variation in its genetics, phenotypes and its underlying physiology. Our study demonstrates the importance of evaluating physiological traits in invasive plants, especially as they relate to home climates.

The Evolution of an Invasive Plant, Sorghum halepense L. ('Johnsongrass').

From noble beginnings as a prospective forage, polyploid Sorghum halepense ('Johnsongrass') is both an invasive species and one of the world's worst agricultural weeds. Formed by S. bicolor x S. propinquum hybridization, we show S. halepense to have S. bicolor-enriched allele composition and striking mutations in 5,957 genes that differentiate it from representatives of its progenitor species and an outgroup. The spread of S. halepense may have been facilitated by introgression from closely-related cultivated sorghum near genetic loci affecting rhizome development, seed size, and levels of lutein, a photochemical protectant and abscisic acid precursor. Rhizomes, subterranean stems that store carbohydrates and spawn clonal propagules, have growth correlated with reproductive rather than other vegetative tissues, and increase survival of both temperate cold seasons and tropical dry seasons. Rhizomes of S. halepense are more extensive than those of its rhizomatous progenitor S. propinquum, with gene expression including many alleles from its non-rhizomatous S. bicolor progenitor. The first surviving polyploid in its lineage in ∼96 million years, its post-Columbian spread across six continents carried rich genetic diversity that in the United States has facilitated transition from agricultural to non-agricultural niches. Projected to spread another 200-600 km northward in the coming century, despite its drawbacks S. halepense may offer novel alleles and traits of value to improvement of sorghum.

Home climate and habitat drive ecotypic stress response differences in an invasive grass.

Invasive plants and agricultural weeds are a ubiquitous and ever-expanding threat to biosecurity, biodiversity and ecosystem services. Many of these species are known to succeed through rapid adaptation to biotic and abiotic stress regimes, often in highly disturbed systems. Given the current state of evidence for selection of weedy genotypes via primary physiological stresses like drought, flooding, heat, cold and nutrient deficiency, we posit that adaptation to land management regimes which comprise suites of these stresses can also be expected. To establish this link, we tested adaptation to water and nutrient stresses in five non-agricultural and five agricultural populations of the invader Johnsongrass (Sorghum halepense) sampled across a broad range of climates in the USA. We subjected seedlings from each population to factorial drought and nutrient stresses in a common garden greenhouse experiment. Agricultural and non-agricultural ecotypes did not respond differently to experimentally applied stresses. However, non-agricultural populations from more drought-prone and nutrient-poor locations outperformed their agricultural counterparts in shoot allocation and chlorophyll production, respectively. We also found evidence for root allocation adaptation to hotter climates, in line with other C4 grasses, while greater adaptation to drought treatment was associated with soil organic carbon (SOC)-rich habitats. These findings imply that adaptation to land-use types can interact with other macrohabitat parameters, which will be fluctuating in a changing climate and resource-needy world. We see that invasive plants are poised to take on novel habitats within their introduced ranges, leading to complications in the prevention and management of their spread.

Invasive plants negatively impact native, but not exotic, animals.

Despite our growing understanding of the impacts of invasive plants on ecosystem structure and function, important gaps remain, including whether native and exotic species respond differently to plant invasion. This would elucidate basic ecological interactions and inform management. We performed a meta-analytic review of the effects of invasive plants on native and exotic resident animals. We found that invasive plants reduced the abundance of native, but not exotic, animals. This varied by animal phyla, with invasive plants reducing the abundance of native annelids and chordates, but not mollusks or arthropods. We found dissimilar impacts among "wet" and "dry" ecosystems, but not among animal trophic levels. Additionally, the impact of invasive plants increased over time, but this did not vary with animal nativity. Our review found that no studies considered resident nativity differences, and most did not identify animals to species. We call for more rigorous studies of invaded community impacts across taxa, and most importantly, explicit consideration of resident biogeographic origin. We provide an important first insight into how native and exotic species respond differently to invasion, the consequences of which may facilitate cascading trophic disruptions further exacerbating global change consequences to ecosystem structure and function.

Considering weed management as a social dilemma bridges individual and collective interests.

Weeds pose severe threats to agricultural and natural landscapes worldwide. One major reason for the failure to effectively manage weeds at landscape scales is that current Best Management Practice guidelines, and research on how to improve such guidelines, focus too narrowly on property-level management decisions. Insufficiently considered are the aggregate effects of individual actions to determine landscape-scale outcomes, or whether there are collective practices that would improve weed management outcomes. Here, we frame landscape-scale weed management as a social dilemma, where trade-offs occur between individual and collective interests. We apply a transdisciplinary system approach-integrating the perspectives of ecologists, evolutionary biologists and agronomists into a social science theory of social dilemmas-to four landscape-scale weed management challenges: (i) achieving plant biosecurity, (ii) preventing weed seed contamination, (iii) maintaining herbicide susceptibility and (iv) sustainably using biological control. We describe how these four challenges exhibit characteristics of 'public good problems', wherein effective weed management requires the active contributions of multiple actors, while benefits are not restricted to these contributors. Adequate solutions to address these public good challenges often involve a subset of the eight design principles developed by Elinor Ostrom for 'common pool social dilemmas', together with design principles that reflect the public good nature of the problems. This paper is a call to action for scholars and practitioners to broaden our conceptualization and approaches to weed management problems. Such progress begins by evaluating the public good characteristics of specific weed management challenges and applying context-specific design principles to realize successful and sustainable weed management.

Identification of Differentially Methylated Sites with Weak Methylation Effects.

Deoxyribonucleic acid (DNA) methylation is an epigenetic alteration crucial for regulating stress responses. Identifying large-scale DNA methylation at single nucleotide resolution is made possible by whole genome bisulfite sequencing. An essential task following the generation of bisulfite sequencing data is to detect differentially methylated cytosines (DMCs) among treatments. Most statistical methods for DMC detection do not consider the dependency of methylation patterns across the genome, thus possibly inflating type I error. Furthermore, small sample sizes and weak methylation effects among different phenotype categories make it difficult for these statistical methods to accurately detect DMCs. To address these issues, the wavelet-based functional mixed model (WFMM) was introduced to detect DMCs. To further examine the performance of WFMM in detecting weak differential methylation events, we used both simulated and empirical data and compare WFMM performance to a popular DMC detection tool methylKit. Analyses of simulated data that replicated the effects of the herbicide glyphosate on DNA methylation in Arabidopsis thaliana show that WFMM results in higher sensitivity and specificity in detecting DMCs compared to methylKit, especially when the methylation differences among phenotype groups are small. Moreover, the performance of WFMM is robust with respect to small sample sizes, making it particularly attractive considering the current high costs of bisulfite sequencing. Analysis of empirical Arabidopsis thaliana data under varying glyphosate dosages, and the analysis of monozygotic (MZ) twins who have different pain sensitivities-both datasets have weak methylation effects of <1%-show that WFMM can identify more relevant DMCs related to the phenotype of interest than methylKit. Differentially methylated regions (DMRs) are genomic regions with different DNA methylation status across biological samples. DMRs and DMCs are essentially the same concepts, with the only difference being how methylation information across the genome is summarized. If methylation levels are determined by grouping neighboring cytosine sites, then they are DMRs; if methylation levels are calculated based on single cytosines, they are DMCs.

Climatic niche shifts are common in introduced plants.

Our understanding of how climate influences species distributions and our ability to assess the risk of introduced species depend on the assumption that species' climatic niches remain stable across space and time. While niche shifts have been detected in individual invasive species, one assessment of ~50 plants in Europe and North America concluded that niche shifts were rare, while another concluded the opposite. These contradictory findings, limited in species number and geographic scope, leave open a need to understand how often introduced species experience niche shifts and whether niche shifts can be predicted. We found evidence of climatic niche shifts in 65-100% of 815 terrestrial plant species introduced across five continents, depending on how niche shifts were measured. Individual species responses were idiosyncratic, but we generally saw that niche shifts reflected changes in climate availability at the continent scale and were largest in long-lived and cultivated species. Smaller intercontinental niche shifts occurred within species' native ranges. Overall, the climatic niches of terrestrial plant species were not conserved as they crossed continents. These results have major consequences for applying environmental niche models to assess the risk of invasive species and for predicting species responses to climate change. Our findings challenge the tenet that species' niches are conserved aspects of their ecology.

Epigenetic regulation - contribution to herbicide resistance in weeds?

Continuous use of herbicides has resulted in the evolution of resistance to all major herbicide modes of action worldwide. Besides the well-documented cases of newly acquired resistance through genetic changes, epigenetic regulation may also contribute to herbicide resistance in weeds. Epigenetics involves processes that modify the expression of specific genetic elements without changes in the DNA sequence, and play an important role in re-programming gene expression. Epigenetic modifications can be induced spontaneously, genetically or environmentally. Stress-induced epigenetic changes are normally reverted soon after stress exposure, although in specific cases they can also be carried over multiple generations, thereby having a selective benefit. Here, we provide an overview of the basis of epigenetic regulation in plants and discuss the possible effect of epigenetic changes on herbicide resistance. The understanding of these epigenetic changes would add a new perspective to our knowledge of environmental and management stresses and their effects on the evolution of herbicide resistance in weeds. © 2017 Society of Chemical Industry.

Multi-Phase US Spread and Habitat Switching of a Post-Columbian Invasive, Sorghum halepense.

Johnsongrass (Sorghum halepense) is a striking example of a post-Columbian founder event. This natural experiment within ecological time-scales provides a unique opportunity for understanding patterns of continent-wide genetic diversity following range expansion. Microsatellite markers were used for population genetic analyses including leaf-optimized Neighbor-Joining tree, pairwise FST, mismatch analysis, principle coordinate analysis, Tajima's D, Fu's F and Bayesian clusterings of population structure. Evidence indicates two geographically distant introductions of divergent genotypes, which spread across much of the US in <200 years. Based on geophylogeny, gene flow patterns can be inferred to have involved five phases. Centers of genetic diversity have shifted from two introduction sites separated by ~2000 miles toward the middle of the range, consistent with admixture between genotypes from the respective introductions. Genotyping provides evidence for a 'habitat switch' from agricultural to non-agricultural systems and may contribute to both Johnsongrass ubiquity and aggressiveness. Despite lower and more structured diversity at the invasion front, Johnsongrass continues to advance northward into cooler and drier habitats. Association genetic approaches may permit identification of alleles contributing to the habitat switch or other traits important to weed/invasive management and/or crop improvement.

Plant Invasions Associated with Change in Root-Zone Microbial Community Structure and Diversity.

The importance of plant-microbe associations for the invasion of plant species have not been often tested under field conditions. The research sought to determine patterns of change in microbial communities associated with the establishment of invasive plants with different taxonomic and phenetic traits. Three independent locations in Virginia, USA were selected. One site was invaded by a grass (Microstegium vimineum), another by a shrub (Rhamnus davurica), and the third by a tree (Ailanthus altissima). The native vegetation from these sites was used as reference. 16S rRNA and ITS regions were sequenced to study root-zone bacterial and fungal communities, respectively, in invaded and non-invaded samples and analyzed using Quantitative Insights Into Microbial Ecology (QIIME). Though root-zone microbial community structure initially differed across locations, plant invasion shifted communities in similar ways. Indicator species analysis revealed that Operational Taxonomic Units (OTUs) closely related to Proteobacteria, Acidobacteria, Actinobacteria, and Ascomycota increased in abundance due to plant invasions. The Hyphomonadaceae family in the Rhodobacterales order and ammonia-oxidizing Nitrospirae phylum showed greater relative abundance in the invaded root-zone soils. Hyphomicrobiaceae, another bacterial family within the phyla Proteobacteria increased as a result of plant invasion, but the effect associated most strongly with root-zones of M. vimineum and R. davurica. Functional analysis using Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt) showed bacteria responsible for nitrogen cycling in soil increased in relative abundance in association with plant invasion. In agreement with phylogenetic and functional analyses, greater turnover of ammonium and nitrate was associated with plant invasion. Overall, bacterial and fungal communities changed congruently across plant invaders, and support the hypothesis that nitrogen cycling bacteria and functions are important factors in plant invasions. Whether the changes in microbial communities are driven by direct plant microbial interactions or a result of plant-driven changes in soil properties remains to be determined.

Global Invader Impact Network (GIIN): toward standardized evaluation of the ecological impacts of invasive plants.

Terrestrial invasive plants are a global problem and are becoming ubiquitous components of most ecosystems. They are implicated in altering disturbance regimes, reducing biodiversity, and changing ecosystem function, sometimes in profound and irreversible ways. However, the ecological impacts of most invasive plants have not been studied experimentally, and most research to date focuses on few types of impacts, which can vary greatly among studies. Thus, our knowledge of existing ecological impacts ascribed to invasive plants is surprisingly limited in both breadth and depth. Our aim was to propose a standard methodology for quantifying baseline ecological impact that, in theory, is scalable to any terrestrial plant invader (e.g., annual grasses to trees) and any invaded system (e.g., grassland to forest). The Global Invader Impact Network (GIIN) is a coordinated distributed experiment composed of an observational and manipulative methodology. The protocol consists of a series of plots located in (1) an invaded area; (2) an adjacent removal treatment within the invaded area; and (3) a spatially separate uninvaded area thought to be similar to pre-invasion conditions of the invaded area. A standardized and inexpensive suite of community, soil, and ecosystem metrics are collected allowing broad comparisons among measurements, populations, and species. The method allows for one-time comparisons and for long-term monitoring enabling one to derive information about change due to invasion over time. Invader removal plots will also allow for quantification of legacy effects and their return rates, which will be monitored for several years. GIIN uses a nested hierarchical scale approach encompassing multiple sites, regions, and continents. Currently, GIIN has network members in six countries, with new members encouraged. To date, study species include representatives of annual and perennial grasses; annual and perennial forbs; shrubs; and trees. The goal of the GIIN framework is to create a standard yet flexible platform for understanding the ecological impacts of invasive plants, allowing both individual and synthetic analyses across a range of taxa and ecosystems. If broadly adopted, this standard approach will offer unique insight into the ecological impacts of invasive plants at local, regional, and global scales.