Biology subjects

Greenblum, S. I.

Publications and source records attributed to Greenblum, S. I..

7 recordsLinked to original sources

bioRxiv2026

Positional grammar of transcription factor binding partitions developmental and stress-response regulation in plants

Understanding how transcription factor binding site (TFBS) position influences gene regulation remains a fundamental challenge in plants. Here, we integrate conserved multiDAP TFBS maps for 244 transcription factors (TFs) with single-nucleus chromatin accessibility, cell type-resolved gene expression, and hormone-response datasets across Brassicaceae species to determine how TFBS position relates to regulatory function. Although conserved TFBSs are enriched near transcription start sites (TSSs), TSS-proximal accessibility poorly predicts cell type-specific expression. Instead, cell type-specific expression correlates best with conserved TFBSs embedded in cell type-restricted chromatin, with TF family-specific distributions across distal promoters and introns. In contrast, TSS-proximal TFBSs in broadly accessible chromatin are associated with rapid transcriptional responses to abiotic and biotic stress hormones. Coding sequence TFBSs mark a distinct regulatory context in which the same DNA sequence encodes both amino acid sequence and TF motifs, including evidence that CDS-localized ABR1 binding may contribute to repression during hormone response. Finally, distal upstream regions contain conserved multi-family TF clusters with enhancer-like features overlapping rare cell type-specific accessible chromatin and enriched near genes controlling embryonic, meristematic, and hormone-dependent developmental patterning. Together, these results support a positional grammar in which TFBS position and chromatin context jointly partition developmental, stress-responsive, and repressive regulatory output in plants.

genomics↗

bioRxiv2025

Ecological stoichiometry and life history theory, not the identity of genomic variants, predict rapid adaptation

SignificanceForecasting how populations adapt to changing environments is a central challenge in evolutionary biology. We tested the predictability of rapid adaptation by tracking both phenotypic and genomic trajectories of evolution in replicate outdoor populations of Drosophila melanogaster and comparing these data to predictions derived from life history theory, ecological stoichiometry, and genomic data. We found that life history theory and ecological stoichiometry forecasted the direction of phenotypic evolution, even with temporal changes in the direction of evolution. In contrast, genomic predictors were largely unable to forecast the SNPs or genes underlying adaptation. These results demonstrate the utility of ecological frameworks to provide general, but robust, forecasts of adaptation in complex environments. Determining the scale and scope of the predictability of evolution is fundamental to understanding biological processes and to managing biodiversity. Ecological frameworks, including life history theory and ecological stoichiometry, offer testable predictions about the direction of adaptation and trade-offs between traits in response to environmental change. Similarly, well-characterized molecular pathways, genotype-phenotype linkages, and prior evolutionary genomic studies could be predictive of the genomic architecture underlying adaptation. We tested whether ecological frameworks and evolutionary genomic data can be used to forecast rapid adaptation in replicated outdoor populations of Drosophila melanogaster evolving in response to natural seasonal fluctuations from summer to late fall. Life history theory predicted the observed pattern of adaptive tracking: in summer, reproductive output increased and stress tolerance decreased, while in fall, this direction reversed, with evolution of increased stress tolerance at the expense of reproduction. Stoichiometric phenotypic evolution was also predictable, with phosphorus and magnesium content, both linked to growth rate, and alkali metal, associated with maintaining homeostasis in response to thermal stress, showing rapid and parallel evolution indicative of adaptation. Temporal genomic data revealed a complex genomic architecture of temporal adaptation and the SNPs and genes involved in adaptation were largely unpredictable. These results demonstrate that ecological frameworks, more than genomic data, have utility in forecasting adaptation in complex and variable environments.

evolutionary biology↗

bioRxiv2024

Dominance reversal protects large-effect resistance polymorphisms in temporally varying environments

Large-effect functional genetic variation is commonly found in natural populations, even though natural selection should erode such variants. Theory suggests that under fluctuating selective pressures, beneficial reversal of dominance - where alleles are dominant when beneficial and recessive when deleterious - can protect these loci from selection, allowing them to persist. However, empirical evidence for this mechanism remains elusive because testing requires direct measurements of selection and dominance in natural conditions. Here, we show that insecticide-resistant alleles at the Ace locus in Drosophila melanogaster persist worldwide at intermediate frequencies and exhibit beneficial reversal of dominance. By combining laboratory and large-scale field mesocosm experiments with insecticide manipulation, and mathematical modeling, we show that the benefits of the resistant Ace alleles are dominant while their fitness costs recessive. We further show that fluctuating insecticide selection generates chromosome-scale genomic perturbations at sites linked to the resistant Ace alleles, revealing broader genomic consequences of this mechanism. Overall, our results suggest that beneficial reversal of dominance contributes to the maintenance of functional genetic variation and impacts patterns of genomic diversity via linked fluctuating selection.

evolutionary biology↗

bioRxiv2024

An atlas of conserved transcription factor binding sites reveals the cell type-resolved gene regulatory landscape of flowering plants

Transcription factors (TFs) are proteins that bind DNA to control where and when genes are expressed. In plants, dozens of TF families interact with distinct sets of binding sites (TFBSs) that reflect each TFs role in organismal function and species-specific adaptations. However, defining these roles and understanding broader patterns of regulatory evolution remains challenging, as predicted TFBSs may lack a clear impact on transcription, and experimentally-derived TF binding maps to date are modest in scale or restricted to model organisms. Here, we present a scalable TFBS assay that we leveraged to create an atlas of nearly 3,000 genome-wide binding site maps for 360 TFs in 10 species spanning 150 million years of flowering plant evolution. We find that TF orthologs from distant species retain nearly identical binding preferences, suggesting that regulatory evolution primarily arises from gain and loss of TFBSs. Within lineages however, conserved TFBSs are over-represented and found in regions harboring signatures of functional regulatory elements. Moreover, genes with conserved TFBSs showed a striking enrichment for cell type-specific expression in single-nuclei RNA atlases, providing a robust marker of each TFs activity and developmental role. Finally, we compare distant lineages, illustrating how ancient regulatory modules were recruited and rewired to enable adaptations underlying the evolutionary success of grasses.

genomics↗

bioRxiv2024

Drosophila melanogaster pigmentation demonstrates adaptive phenotypic parallelism but genomic unpredictability over multiple timescales

Populations are capable of responding to environmental change over ecological timescales via adaptive tracking. However, the translation from patterns of allele frequency change to rapid adaptation of complex traits remains unresolved. We used abdominal pigmentation in Drosophila melanogaster as a model phenotype to address the nature, genetic architecture, and repeatability of rapid adaptation in the field. We show that D. melanogaster pigmentation evolves as a highly parallel and deterministic response to shared environmental gradients across latitude and season in natural North American populations. We then experimentally evolved replicate, genetically diverse fly populations in field mesocosms to remove any confounding effects of demography and/or cryptic structure that may drive patterns in wild populations; we show that pigmentation rapidly responds, in parallel, in fewer than fifteen generations. Thus, pigmentation evolves concordantly in response to spatial and temporal climatic gradients. We next examined whether phenotypic differentiation was associated with allele frequency change at loci with established links to genetic variance in pigmentation in natural populations. We found that across all spatial and temporal scales, phenotypic patterns were associated with variation at pigmentation-related loci, and the sets of genes we identified in each context were largely nonoverlapping. Therefore, our findings suggest that parallel phenotypic evolution is associated with distinct components of the polygenic architecture shifting across each environmental gradient to produce redundant adaptive patterns.

evolutionary biology↗

bioRxiv2021

Direct observation of adaptive tracking on ecological timescales in Drosophila

Direct observation of evolution in response to natural environmental change can resolve fundamental questions about adaptation including its pace, temporal dynamics, and underlying phenotypic and genomic architecture. We tracked evolution of fitness-associated phenotypes and allele frequencies genome-wide in ten replicate field populations of Drosophila melanogaster over ten generations from summer to late fall. Adaptation was evident over each sampling interval (1-4 generations) with exceptionally rapid phenotypic adaptation and large allele frequency shifts at many independent loci. The direction and basis of the adaptive response shifted repeatedly over time, consistent with the action of strong and rapidly fluctuating selection. Overall, we find clear phenotypic and genomic evidence of adaptive tracking occurring contemporaneously with environmental change, demonstrating the temporally dynamic nature of adaptation. One sentence summaryRapid environmental change drives continuous phenotypic and polygenic adaptation, demonstrating the temporal dynamism of adaptation.

evolutionary biology↗

bioRxiv2019

Microbiome composition shapes rapid genomic adaptation of Drosophila melanogaster

Population genomic data has revealed patterns of genetic variation associated with adaptation in many taxa. Yet understanding the adaptive process that drives such patterns is challenging - it requires disentangling the ecological agents of selection, determining the relevant timescales over which evolution occurs, and elucidating the genetic architecture of adaptation. Doing so for the adaptation of hosts to their microbiome is of particular interest with growing recognition of the importance and complexity of host-microbe interactions. Here, we track the pace and genomic architecture of adaptation to an experimental microbiome manipulation in replicate populations of Drosophila melanogaster in field mesocosms. Manipulation of the microbiome altered population dynamics and increased divergence between treatments in allele frequencies genome-wide, with regions showing strong divergence found on all chromosomes. Moreover, at divergent loci previously associated with adaptation across natural populations, we found that the more common allele in fly populations experimentally enriched for a certain microbial group was also more common in natural populations with high relative abundance of that microbial group. These results suggest that microbiomes may be an agent of selection that shapes the pattern and process of adaptation and, more broadly, that variation in a single ecological factor within a complex environment can drive rapid, polygenic adaptation over short timescales.\n\nSignificance statementNatural selection can drive evolution over short timescales. However, there is little understanding of which ecological factors are capable of driving rapid evolution and how this rapid evolution alters allele frequencies across the genome. Here we combine a field experiment with population genomic data from natural populations across a latitudinal gradient to assess whether and how microbiome composition drives rapid genomic evolution of host populations. We find that differences in microbiome composition cause divergence in allele frequencies genome-wide, including in genes previously associated with local adaptation. Moreover, we observed concordance between experimental and natural populations in terms of the direction of allele frequency change, suggesting that microbiome composition may be an agent of selection that drives adaptation in the wild.

evolutionary biology↗