The changing influence of host genetics on the leaf fungal microbiome throughout plant development

Host genetics and the environment influence which fungal microbes colonize a plant. A new study in PLOS Biology finds that the relative influence of these factors changes throughout the development of the biofuel crop switchgrass growing in field settings

Broad geographic sampling reveals the shared basis and environmental correlates of seasonal adaptation in Drosophila.

To advance our understanding of adaptation to temporally varying selection pressures, we identified signatures of seasonal adaptation occurring in parallel among Drosophila melanogaster populations. Specifically, we estimated allele frequencies genome-wide from flies sampled early and late in the growing season from 20 widely dispersed populations. We identified parallel seasonal allele frequency shifts across North America and Europe, demonstrating that seasonal adaptation is a general phenomenon of temperate fly populations. Seasonally fluctuating polymorphisms are enriched in large chromosomal inversions, and we find a broad concordance between seasonal and spatial allele frequency change. The direction of allele frequency change at seasonally variable polymorphisms can be predicted by weather conditions in the weeks prior to sampling, linking the environment and the genomic response to selection. Our results suggest that fluctuating selection is an important evolutionary force affecting patterns of genetic variation in Drosophila

Evidence that Adaptation in Drosophila Is Not Limited by Mutation at Single Sites

Adaptation in eukaryotes is generally assumed to be mutation-limited because of small effective population sizes. This view is difficult to reconcile, however, with the observation that adaptation to anthropogenic changes, such as the introduction of pesticides, can occur very rapidly. Here we investigate adaptation at a key insecticide resistance locus (Ace) in Drosophila melanogaster and show that multiple simple and complex resistance alleles evolved quickly and repeatedly within individual populations. Our results imply that the current effective population size of modern D. melanogaster populations is likely to be substantially larger (≥100-fold) than commonly believed. This discrepancy arises because estimates of the effective population size are generally derived from levels of standing variation and thus reveal long-term population dynamics dominated by sharp—even if infrequent—bottlenecks. The short-term effective population sizes relevant for strong adaptation, on the other hand, might be much closer to census population sizes. Adaptation in Drosophila may therefore not be limited by waiting for mutations at single sites, and complex adaptive alleles can be generated quickly without fixation of intermediate states. Adaptive events should also commonly involve the simultaneous rise in frequency of independently generated adaptive mutations. These so-called soft sweeps have very distinct effects on the linked neutral polymorphisms compared to the standard hard sweeps in mutation-limited scenarios. Methods for the mapping of adaptive mutations or association mapping of evolutionarily relevant mutations may thus need to be reconsidered

Differentiation between MAMP Triggered Defenses in <i>Arabidopsis thaliana</i>

A first line of defense against pathogen attack for both plants and animals involves the detection of microbe-associated molecular patterns (MAMPs), followed by the induction of a complex immune response. Plants, like animals, encode several receptors that recognize different MAMPs. While these receptors are thought to function largely redundantly, the physiological responses to different MAMPs can differ in detail. Responses to MAMP exposure evolve quantitatively in natural populations of Arabidopsis thaliana, perhaps in response to environment specific differences in microbial threat. Here, we sought to determine the extent to which the detection of two canonical MAMPs were evolving redundantly or distinctly within natural populations. Our results reveal negligible correlation in plant growth responses between the bacterial MAMPs EF-Tu and flagellin. Further investigation of the genetic bases of differences in seedling growth inhibition and validation of 11 candidate genes reveal substantial differences in the genetic loci that underlie variation in response to these two MAMPs. Our results indicate that natural variation in MAMP recognition is largely MAMP-specific, indicating an ability to differentially tailor responses to EF-Tu and flagellin in A. thaliana populations

Genome-Wide Patterns of Adaptation to Temperate Environments Associated with Transposable Elements in Drosophila

Investigating spatial patterns of loci under selection can give insight into how populations evolved in response to selective pressures and can provide monitoring tools for detecting the impact of environmental changes on populations. Drosophila is a particularly good model to study adaptation to environmental heterogeneity since it is a tropical species that originated in sub-Saharan Africa and has only recently colonized the rest of the world. There is strong evidence for the adaptive role of Transposable Elements (TEs) in the evolution of Drosophila, and TEs might play an important role specifically in adaptation to temperate climates. In this work, we analyzed the frequency of a set of putatively adaptive and putatively neutral TEs in populations with contrasting climates that were collected near the endpoints of two known latitudinal clines in Australia and North America. The contrasting results obtained for putatively adaptive and putatively neutral TEs and the consistency of the patterns between continents strongly suggest that putatively adaptive TEs are involved in adaptation to temperate climates. We integrated information on population behavior, possible environmental selective agents, and both molecular and functional information of the TEs and their nearby genes to infer the plausible phenotypic consequences of these insertions. We conclude that adaptation to temperate environments is widespread in Drosophila and that TEs play a significant role in this adaptation. It is remarkable that such a diverse set of TEs located next to a diverse set of genes are consistently adaptive to temperate climate-related factors. We argue that reverse population genomic analyses, as the one described in this work, are necessary to arrive at a comprehensive picture of adaptation.[Author Summary] The potential of geographic studies of genetic variation for the understanding of adaptation has been recognized for some time. In Drosophila, most of the available studies are based on a priori candidates giving a biased picture of the genes and traits under spatially varying selection. In this work, we performed a genome-wide scan of adaptations to temperate climates associated with Transposable Element (TE) insertions. We integrated the available information of the identified TEs and their nearby genes to provide plausible hypotheses about the phenotypic consequences of these insertions. Considering the diversity of these TEs and the variety of genes into which they are inserted, it is surprising that their adaptive effects are consistently related to temperate climate-related factors. The TEs identified in this work add substantially to the markers available to monitor the impact of climate change on populations.This work was supported by grants from the National Institutes of Health (GM 077368) and the National Science Foundation (0317171) to DAP. PWM is a Human Frontier Science Program Postdoctoral Fellow.Peer reviewe

What natural variation can teach us about resistance durability

Breeding a crop variety to be resistant to a pathogen usually takes years. This is problematic because pathogens, with short generation times and fluid genomes, adapt quickly to overcome resistance. The triumph of the pathogen is not inevitable, however, as there are numerous examples of durable resistance, particularly in wild plants. Which factors then contribute to such resistance stability over millennia? We review current knowledge of wild and agricultural pathosystems, detailing the importance of genetic, species and spatial heterogeneity in the prevention of pathogen outbreaks. We also highlight challenges associated with increasing resistance diversity in crops, both in light of pathogen (co-)evolution and breeding practices. Historically it has been difficult to incorporate heterogeneity into agriculture due to reduced efficiency in harvesting. Recent advances implementing computer vision and automation in agricultural production may improve our ability to harvest mixed genotype and mixed species plantings, thereby increasing resistance durability

Similar levels of gene content variation observed for <i>Pseudomonas syringae</i> populations extracted from single and multiple host species

Bacterial strains of the same species collected from different hosts frequently exhibit differences in gene content. In the ubiquitous plant pathogen Pseudomonas syringae, more than 30% of genes encoded by each strain are not conserved among strains colonizing other host species. Although they are often implicated in host specificity, the role of this large fraction of the genome in host-specific adaptation is largely unexplored. Here, we sought to relate variation in gene content between strains infecting different species to variation that persists between strains on the same host. We fully sequenced a collection of P. syringae strains collected from wild Arabidopsis thaliana populations in the Midwestern United States. We then compared patterns of variation observed in gene content within these A. thaliana-isolated strains to previously published P. syringae sequence from strains collected on a diversity of crop species. We find that strains collected from the same host, A. thaliana, differ in gene content by 21%, 2/3 the level of gene content variation observed across strains collected from different hosts. Furthermore, the frequency with which specific genes are present among strains collected within the same host and among strains collected from different hosts is highly correlated. This implies that most gene content variation is maintained irrespective of host association. At the same time, we identify specific genes whose presence is important for P. syringae’s ability to flourish within A. thaliana. Specifically, the A. thaliana strains uniquely share a genomic island encoding toxins active against plants and surrounding microbes, suggesting a role for microbe-microbe interactions in dictating the abundance within this host. Overall, our results demonstrate that while variation in the presence of specific genes can affect the success of a pathogen within its host, the majority of gene content variation is not strongly associated with patterns of host use

Differentiation between MAMP Triggered Defenses in <i>Arabidopsis thaliana</i>

<div><p>A first line of defense against pathogen attack for both plants and animals involves the detection of microbe-associated molecular patterns (MAMPs), followed by the induction of a complex immune response. Plants, like animals, encode several receptors that recognize different MAMPs. While these receptors are thought to function largely redundantly, the physiological responses to different MAMPs can differ in detail. Responses to MAMP exposure evolve quantitatively in natural populations of <i>Arabidopsis thaliana</i>, perhaps in response to environment specific differences in microbial threat. Here, we sought to determine the extent to which the detection of two canonical MAMPs were evolving redundantly or distinctly within natural populations. Our results reveal negligible correlation in plant growth responses between the bacterial MAMPs EF-Tu and flagellin. Further investigation of the genetic bases of differences in seedling growth inhibition and validation of 11 candidate genes reveal substantial differences in the genetic loci that underlie variation in response to these two MAMPs. Our results indicate that natural variation in MAMP recognition is largely MAMP-specific, indicating an ability to differentially tailor responses to EF-Tu and flagellin in <i>A. thaliana</i> populations.</p></div