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Hale, C. O.

Publications and source records attributed to Hale, C. O..

8 recordsLinked to original sources

Convergent genome- and gene-level constraints shape repeated environmental adaptation in grasses

Grasses (Poaceae) dominate terrestrial ecosystems and sustain global food security, yet the genomic principles enabling their repeated adaptation to extreme environments remain unresolved. Combining dense phylogenomic sampling, global environmental data, and genomic large language models (gLLMs), we characterize the mutational targets underlying environmental adaptation across 707 genomes from 569 species spanning 17 climate zones. We identify 19-30 phylogenetically independent transitions into extreme temperature, water, and soil environments, accompanied by convergent shifts in genome-scale molecular properties, including the Nitrogen-to-Carbon balance and the biosynthetic cost of the proteome. Our gLLMs-informed phylogenetic mixed modeling framework identifies 330 genes that repeatedly underlie distinct axes of environmental adaptation, highlighting the importance of protein modification and localization within extracellular and organellar compartments. Overlaying independent convergent adaptation tests identifies 17 high-confidence candidates for further characterization. Together, our results show that grass adaptation is canalized by layered constraints at genome-wide and gene-specific scales, producing predictable evolutionary trajectories.

evolutionary biology↗

High-Quality Draft Genome Assemblies and Comparative Genomics of Three Bouteloua Species (Poaceae: Chloridoideae)

Bouteloua is a PACMAD grass genus that dominates much of the central and southern North American prairies and plains, where species such as sideoats grama (B. curtipendula), blue grama (B. gracilis), and black grama (B. eriopoda) are both ecologically dominant and among the most valuable forage grasses of arid rangelands. Yet, genomic resources for the genus remain limited. We generated PacBio HiFi draft assemblies for B. curtipendula (653 Mb, N50 25.5 Mb), B. gracilis (808 Mb, N50 4.1 Mb), and B. eriopoda (1.67 Gb, N50 1.0 Mb). All assemblies showed >98.5% BUSCO completeness. Helixer predicted 83,877-215,536 gene models per assembly. However, syntenic copy numbers (2 in B. curtipendula, 3 in B. gracilis, and 6 in B. eriopoda) indicate that at least two species are polyploid, and the inflated gene model counts likely reflect homeologous copies and fragmented predictions rather than true gene numbers. panEDTA identified 25-40% transposable-element content, dominated by LTR retrotransposons. These assemblies provide foundational genomic references for Bouteloua and support comparative studies across PACMAD grasses.

plant biology↗

Variation in response to water availability across Phlox species

Plants adapt to environmental variation both by evolving divergent trait means and by plastically adjusting trait expression in response to local conditions. While these dual strategies are essential for persistence in diverse environments, how they interact and vary across closely related species is understudied. For plants, water availability is a particularly important selective force that shapes species distributions, selects for growth habit and life history strategy, and can dictate individuals plastic expressions of trait values and reproductive success. Here, we use ecological niche modeling, field soil collections, and a controlled drought experiment to test how biogeography and evolutionary history influence responses to limited water availability in three closely related Texas annual Phlox species and their F1 hybrids. We infer that the species occupy distinct niches that diverge along a primary axis of water availably and soil moisture. Each species has a distinct vegetative growth habit that does not match broad predictions of divergence in response to water availability. Nevertheless, we find that all the species show a significant morphological response to controlled soil dry down with reduced biomass, smaller leaves, and fewer flowers, as would be predicted in a response to drought. We find that Phlox drummondii, which occupies intermediate habitats, exhibits the strongest plastic response to water limitation, despite it not having the broadest environmental niche. Additionally, most hybrids involving P. drummondii display intermediate phenotypes in both wet and dry treatments, while hybrids between P. cuspidata and P. roemeriana show phenotypes consistent with hybrid vigor. These results challenge the hypothesis that species from broader environments evolve greater plasticity. Instead, the most plastic species did not have the broadest niche, suggesting plasticity and niche breadth may evolve independently.

evolutionary biology↗

Grass Rhizome Proteomics Reveals Convergent Freezing-Tolerance Strategies

O_LIGrasses in the PACMAD clade independently colonized cold environments from warm-climate ancestors, but whether their molecular responses to freezing reflect shared evolutionary solutions or lineage-specific innovations remains unknown. We used comparative proteomics to test whether protein-level cold responses show stronger cross-species conservation than previously observed at the transcript level. C_LIO_LIWe quantified seasonal rhizome proteomes (winter vs summer) from five PACMAD species grown in a common garden exposed to sustained sub-zero temperatures, identified differentially abundant proteins, and compared fold-change magnitudes across species using orthogroup-based correlation analyses. We further examined LEA3 protein structure through hydropathy profiling and motif analysis. C_LIO_LIShared cold-responsive proteins showed higher cross-species fold-change correlation ({rho} = 0.80) than background proteins ({rho} = 0.45), despite greater divergence in baseline abundance. LEA3 was the only ortholog elevated across all five species. Cold-tolerant species contained more tandem 11-mer repeats than the cold-sensitive maize, and two species accumulated multiple LEA3 paralogs, increasing total LEA3 abundance. C_LIO_LIIndependent evolution of freezing tolerance in PACMAD grasses is governed by evolutionary constraints on protein-level response magnitude, reflecting the retention of an ancestral protective capacity. Structural divergence of LEA3 in maize suggests that transcriptional induction alone does not ensure freezing tolerance; functional protection likely requires intact motif architecture. C_LI

evolutionary biology↗

Extensive modulation of a conserved cis-regulatory code across 589 grass species

The growing availability of genomes from non-model organisms offers new opportunities to identify functional loci underlying trait variation through comparative genomics. While cis-regulatory regions drive much of phenotypic evolution, linking them to specific functions remains challenging. We identified 514 cis-regulatory motifs enriched in regulatory regions of five diverse grass species, with 73% consistently enriched across all, suggesting a deeply conserved regulatory code. We then quantified conservation of specific motif instances across 589 grass species, revealing widespread gain and loss over evolutionary time. Conservation declined rapidly over the first few million years of divergence, yet [~]50% of motif instances were conserved back to the origin of grasses [~]100 million years ago. Conservation patterns varied by gene class, with modestly higher conservation at transcription factor genes. To test for adaptive cis-regulatory changes, we used phylogenetic mixed models to identify motif gains and losses associated with ecological niche transitions. Our models revealed polygenic adaptation across 810 motif-orthogroup combinations, including convergent gains of HSF/GARP motifs at an Alpha-N-acetylglucosaminidase gene associated with adaptation to temperate environments. Our results support a "stable code, variable sites" model in which cis-regulatory evolution involves extensive turnover of individual binding site instances while largely preserving transcription factors binding preferences. Cis-regulatory changes at hundreds to thousands of genes appear to contribute to environmental adaptation. Our results highlight the potential of comparative genomics and phylogenetic mixed models to reveal the genetic basis of complex traits.

genomics↗

Extensive genome evolution distinguishes maize within a stable tribe of grasses

Over the last 20 million years, the Andropogoneae tribe of grasses has evolved to dominate 17% of global land area. Domestication of these grasses in the last 10,000 years has yielded our most productive crops, including maize, sugarcane, and sorghum. The majority of Andropogoneae species, including maize, show a history of polyploidy - a condition that, while offering the evolutionary advantage of multiple gene copies, poses challenges to basic cellular processes, gene expression, and epigenetic regulation. Genomic studies of polyploidy have been limited by sparse sampling of taxa in groups with multiple polyploidy events. Here, we present 33 genome assemblies from 27 species, including chromosome-scale assemblies of maize relatives Zea and Tripsacum. In maize, the after-effects of polyploidy have been widely studied, showing reduced chromosome number, biased fractionation of duplicate genes, and transposable element (TE) expansions. While we observe these patterns within the genus Zea, 12 other polyploidy events deviate significantly. Those tetraploids and hexaploids retain elevated chromosome number, maintain nearly complete complements of duplicate genes, and have only stochastic TE amplifications. These genomes reveal variable outcomes of polyploidy, challenging simple predictions and providing a foundation for understanding its evolutionary implications in an ecologically and economically important clade.

evolutionary biology↗

Contrasting Rhizosphere Nitrogen Dynamics in Andropogoneae Grasses: Implications for Sustainable Agriculture

Background: Nitrogen (N) fertilization in crop production significantly impacts ecosystems, often disrupting natural plant-microbe-soil interactions and causing environmental pollution. Our research tested the hypothesis that phylogenetically related perennial grasses might preserve rhizosphere management strategies conducive to a sustainable N economy for crops. Method: We analyzed the N cycle in the rhizospheres of 36 Andropogoneae grass species related to maize and sorghum, investigating their impacts on N availability and losses. This assay is supplemented with the collection and comparison of native habitat environment data for ecological inference as well as cross-species genomic and transcriptomic association analyses for candidate gene discovery. Result: Contrary to our hypothesis, all examined annual species, including sorghum and maize, functioned as N "Conservationists," reducing soil nitrification potential and conserving N. In contrast, some perennial species enhanced nitrification and leaching ("Leachers"). Yet a few other species exhibited similar nitrification stimulation effects but limited NO3- losses ("Nitrate Keepers"). We identified significant soil characteristics as influential factors in the eco- evolutionary dynamics of plant rhizospheres, and highlighted the crucial roles of a few transporter genes in soil N management and utilization. Conclusion: These findings serve as valuable guidelines for future breeding efforts for global sustainability.

plant biology↗

A multi-dimensional selective landscape drives adaptive divergence between and within closely related Phlox species

Natural selection shapes diversity across micro and macro-evolutionary scales. Selection causes local adaptation across populations within species and is simultaneously responsible for much of the divergence between species. However, it is unclear if either the force of or the response to selection is the same or different across these scales. Here we show that natural selection drives adaptive divergence between closely related species in a pattern that is distinct from local adaptation within a species. We use reciprocal common-garden transplant experiments across three species of Phlox wildflowers to show widespread adaptive divergence causing species to have highest fitness in their native habitats. Using provenance trials, we also find that one of these Phlox species has strong local adaptation between populations. We compare the axes of divergence and selection between these two scales of diversity and discover that one suite of traits predicts fitness differences between species and that an independent suite of traits predicts fitness variation within species across individuals. Our work reveals how forces of selection can both drive key divergence between species, allowing for and causing speciation, while simultaneously causing extensive diversity that is maintained across populations within a species. The selection landscape is complex and multidimensional

evolutionary biology↗