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At least 37 records · Page 2

Genomic diversifications of five Gossypium allopolyploid species and their impact on cotton improvement

Abstract Polyploidy is an evolutionary innovation for many animals and all flowering plants, but its impact on selection and domestication remains elusive. Here we analyze genome evolution and diversification for all five allopolyploid cotton species, including economically important Upland and Pima cottons. Although these polyploid genomes are conserved in gene content and synteny, they have diversified by subgenomic transposon exchanges that equilibrate genome size, evolutionary rate heterogeneities and positive selection between homoeologs within and among lineages. These differential evolutionary trajectories are accompanied by gene-family diversification and homoeolog expression divergence among polyploid lineages. Selection and domestication drive parallel gene expression similarities in fibers of two cultivated cottons, involving coexpression networks and N 6 -methyladenosine RNA modifications. Furthermore, polyploidy induces recombination suppression, which correlates with altered epigenetic landscapes and can be overcome by wild introgression. These genomic insights will empower efforts to manipulate genetic recombination and modify epigenetic landscapes and target genes for crop improvement.

59 BASIC BIOLOGICAL SCIENCES↗

Extraordinary preservation of gene collinearity over three hundred million years revealed in homosporous lycophytes

Homosporous lycophytes (Lycopodiaceae) are a deeply diverged lineage in the plant tree of life, having split from heterosporous lycophytes ( Selaginella and Isoetes ) ~400 Mya. Compared to the heterosporous lineage, Lycopodiaceae has markedly larger genome sizes and remains the last major plant clade for which no chromosome-level assembly has been available. Here, we present chromosomal genome assemblies for two homosporous lycophyte species, the allotetraploid Huperzia asiatica and the diploid Diphasiastrum complanatum . Remarkably, despite that the two species diverged ~350 Mya, around 30% of the genes are still in syntenic blocks. Furthermore, both genomes had undergone independent whole genome duplications, and the resulting intragenomic syntenies have likewise been preserved relatively well. Such slow genome evolution over deep time is in stark contrast to heterosporous lycophytes and is correlated with a decelerated rate of nucleotide substitution. Together, the genomes of H. asiatica and D. complanatum not only fill a crucial gap in the plant genomic landscape but also highlight a potentially meaningful genomic contrast between homosporous and heterosporous species.

59 BASIC BIOLOGICAL SCIENCES↗

Increasing bacterial tolerance and metabolism of the biofuel, n-butanol using community-level evolution and functional genomics

n-butanol is a strong biofuel candidate since it is more energy dense and less volatile than ethanol. The bottleneck for industrial production of biobutanol is the toxicity; most microbes cannot survive about 1.5% v/v. We propose to develop bioremediation capability along with the biofuel technology to mitigate future spills and their consequences. Two main approaches were used: community-level screening and functional genomics, both followed by directed evolution to increase biodegradation. For the first approach, a bacterial library from historic bioremediation projects was re-isolated and re-characterized, then mixed into artificial communities of ~20 strains (“master mixes”). These master mixes were screened for tolerance to butanol, and continuously exposed to increase tolerance. Promising communities were then tested for growth with butanol as the sole carbon source. Secondly, we looked for bacteria with alcohol dehydrogenase enzymes and looked to increase butanol metabolism. We found that the tolerance for n-butanol may be improved with repeated exposure, but it was difficult to switch from tolerance to metabolism. Bacterial community dynamics may be influenced by n-butanol concentration, and there was putative butanol metabolism found with both research approaches.

09 BIOMASS FUELS↗

Chromosome-scale Genome Assembly of the Most Abundant Ectomycorrhizal Fungus Cenococcum Geophilum Reveals Massive TE Expansion and RIP Defense Mechanism

Transposable elements (TEs) play crucial roles in genome evolution and ecological adaptation in fungi, yet their dynamics in ectomycorrhizal species remain poorly understood. Cenococcum geophilum, the most widespread ectomycorrhizal fungus in boreal and temperate forests with its large, repeat-rich genome, represents an ideal system to investigate TE-mediated adaptation to the physical environment and symbiotic lifestyle. However, previous studies have been limited by fragmented genome assemblies that prevented the resolution of repeat-rich regions. We assembled a telomere-to-telomere reference genome of C. geophilum strain 1.58 using PacBio HiFi and Hi-C datasets, resulting in a 178.54 Mbp genome with seven contiguous chromosomes. We identified 14,145 genes and over 78% of the genome consists of transposable elements (TEs). Of these, 94% are affected by repeat-induced point mutations (RIP), a genome defense mechanism that acts during the sexual reproduction phase, indicating cryptic or ancient sexual reproduction in this putatively asexual fungus. Long terminal repeat retrotransposons, LINEs, and DNA transposons dominate, with three TE families (Ty3, Ty1, and Tad1) contributing over 60% of the genome size, indicating recent transposition bursts. Screening of 15 additional C. geophilum strains revealed recent and lineage-specific TE expansions, implying that several TEs escaped the RIP machinery and retained potential activity. Supporting TE activity in the context of symbiosis, we found 56 TEs differentially transcribed between ectomycorrhizal and free-living mycelium tissues. An even higher number (n = 66) of TEs were differentially expressed between stress resistance morphology (i.e. sclerotia) and free-living mycelium. This supports that TEs are differentially regulated as a response to symbiotic and stress-related conditions. Our results demonstrate that the C. geophilum genome expansion was driven by a few lineage-specific TE families in recent history, with high RIP activity attesting to sexual reproduction. We also provide insights how TEs could respond to lifestyle transitions and traits associated with desiccation resistance.

Cenococcum geophilum↗

Vicennial metagenomic time series unveils evolutionary dynamics of giant viruses in a freshwater ecosystem

Giant viruses play crucial ecological roles in aquatic ecosystems, yet their evolutionary dynamics in response to environmental changes, particularly in freshwater environments, are not well understood. We analyzed a 20-year time series (2000-2019) of 471 co-assembled metagenomes from Lake Mendota (USA) to reconstruct 1512 giant virus metagenome-assembled genomes, providing insights into viral genome evolution. Viruses in the order Imitervirales dominate the virome, remaining consistent across seasons and years. Our findings reveal gene duplication (23% of genes) and horizontal gene transfer (29% of genes) as key drivers of genomic innovation. A co-occurrence network analysis indicates increased virus-host interactions following the introduction of an invasive predatory zooplankton in 2009, highlighting potential hosts in Bigyra, Perkinsea, and Euglenozoa. While single nucleotide polymorphism analysis shows predominantly purifying selection in viral genes, there is a significant increase in positively selected genes post-invasion, particularly those related to infection. Comparative evolutionary analyses reveal that giant viruses exhibit genome-wide substitution rates similar to co-occurring bacteria but significantly slower than smaller dsDNA phages, suggesting both stability and adaptability. Our study demonstrates that freshwater giant viruses employ various evolutionary strategies to respond to environmental change. These results underscore their significant yet often underappreciated role in freshwater ecosystem dynamics.

Vasquez, Yumary M↗

Distinct and rich assemblages of giant viruses in Arctic and Antarctic lakes

Giant viruses (GVs) are key players in ecosystem functioning, biogeochemistry, and eukaryotic genome evolution. GV diversity and abundance in aquatic systems can exceed that of prokaryotes, but their diversity and ecology in lakes, especially polar ones, remain poorly understood. We conducted a comprehensive survey and meta-analysis of GV diversity across 20 lakes, spanning polar to temperate regions, combining our extensive lake metagenome database from the Canadian Arctic and subarctic with publicly available datasets. Leveraging a novel GV genome identification tool, we identified 3304 GV metagenome-assembled genomes, revealing lakes as untapped GV reservoirs. Phylogenomic analysis highlighted their dispersion across all Nucleocytoviricota orders. Strong GV population endemism emerged between lakes from similar regions and biomes (Antarctic and Arctic), but a polar/temperate barrier in lacustrine GV populations and differences in their gene content could be observed. Our study establishes a robust genomic reference for future investigations into lacustrine GV ecology in fast changing polar environments.

59 BASIC BIOLOGICAL SCIENCES↗

Exceptional subgenome stability and functional divergence in the allotetraploid Ethiopian cereal teff

Teff (Eragrostis tef) is a cornerstone of food security in the Horn of Africa, where it is prized for stress resilience, grain nutrition, and market value. Here, we report a chromosome-scale assembly of allotetraploid teff (variety Dabbi) and patterns of subgenome dynamics. The teff genome contains two complete sets of homoeologous chromosomes, with most genes maintaining as syntenic gene pairs. TE analysis allows us to estimate that the teff polyploidy event occurred ~1.1 million years ago (mya) and that the two subgenomes diverged ~5.0 mya. Despite this divergence, we detect no large-scale structural rearrangements, homoeologous exchanges, or biased gene loss, in contrast to many other allopolyploids. The two teff subgenomes have partitioned their ancestral functions based on divergent expression across a diverse expression atlas. Together, these genomic resources will be useful for accelerating breeding of this underutilized grain crop and for fundamental insights into polyploid genome evolution.

54 ENVIRONMENTAL SCIENCES↗

Machine learning reveals genes impacting oxidative stress resistance across yeasts

Reactive oxygen species (ROS) are highly reactive molecules encountered by yeasts during routine metabolism and during interactions with other organisms, including host infection. Here, we characterize the variation in resistance to the ROS-inducing compound tert -butyl hydroperoxide across the ancient yeast subphylum Saccharomycotina and use machine learning (ML) to identify gene families whose sizes are predictive of ROS resistance. The most predictive features are enriched in gene families related to cell wall organization and include two reductase gene families. We estimate the quantitative contributions of features to each species’ classification to guide experimental validation and show that overexpression of the old yellow enzyme (OYE) reductase increases ROS resistance in Kluyveromyces lactis , while Saccharomyces cerevisiae mutants lacking multiple mannosyltransferase-encoding genes are hypersensitive to ROS. Altogether, this work provides a framework for how ML can uncover genetic mechanisms underlying trait variation across diverse species and inform trait manipulation for clinical and biotechnological applications.

59 BASIC BIOLOGICAL SCIENCES↗

The complex polyploid genome architecture of sugarcane

Sugarcane, the world’s most harvested crop by tonnage, has shaped global history, trade and geopolitics, and is currently responsible for 80% of sugar production worldwide. While traditional sugarcane breeding methods have effectively generated cultivars adapted to new environments and pathogens, sugar yield improvements have recently plateaued. The cessation of yield gains may be due to limited genetic diversity within breeding populations, long breeding cycles and the complexity of its genome, the latter preventing breeders from taking advantage of the recent explosion of whole-genome sequencing that has benefited many other crops. Thus, modern sugarcane hybrids are the last remaining major crop without a reference-quality genome. Here we take a major step towards advancing sugarcane biotechnology by generating a polyploid reference genome for R570, a typical modern cultivar derived from interspecific hybridization between the domesticated species (Saccharum officinarum) and the wild species (Saccharum spontaneum). In contrast to the existing single haplotype (‘monoploid’) representation of R570, our 8.7 billion base assembly contains a complete representation of unique DNA sequences across the approximately 12 chromosome copies in this polyploid genome. Using this highly contiguous genome assembly, we filled a previously unsized gap within an R570 physical genetic map to describe the likely causal genes underlying the single-copy Bru1 brown rust resistance locus. This polyploid genome assembly with fine-grain descriptions of genome architecture and molecular targets for biotechnology will help accelerate molecular and transgenic breeding and adaptation of sugarcane to future environmental conditions.

59 BASIC BIOLOGICAL SCIENCES↗

Chromoanagenesis in the asy1 meiotic mutant of Arabidopsis

Chromoanagenesis is a catastrophic event that involves localized chromosomal shattering and reorganization. In this study, we report a case of chromoanagenesis resulting from defective meiosis in the MEIOTIC ASYNAPTIC MUTANT 1 (asy1) background in Arabidopsis thaliana. We provide a detailed characterization of the genomic structure of this individual with a severely shattered segment of chromosome 1. We identified 260 novel DNA junctions in the affected region, most of which affect gene sequence on 1 or both sides of the junction. Our results confirm that asy1-related defective meiosis is a potential trigger for chromoanagenesis. This is the first example of chromoanagenesis associated with female meiosis and indicates the potential for genome evolution during oogenesis.

59 BASIC BIOLOGICAL SCIENCES↗

The Enterprise , a massive transposon carrying Spok meiotic drive genes

The genomes of eukaryotes are full of parasitic sequences known as transposable elements (TEs). Here, we report the discovery of a putative giant tyrosine-recombinase-mobilized DNA transposon, Enterprise, from the model fungus Podospora anserina. Previously, we described a large genomic feature called the Spok block which is notable due to the presence of meiotic drive genes of the Spok gene family. The Spok block ranges from 110 kb to 247 kb and can be present in at least four different genomic locations within P. anserina, despite what is an otherwise highly conserved genome structure. We propose that the reason for its varying positions is that the Spok block is not only capable of meiotic drive but is also capable of transposition. More precisely, the Spok block represents a unique case where the Enterprise has captured the Spoks, thereby parasitizing a resident genomic parasite to become a genomic hyperparasite. Furthermore, we demonstrate that Enterprise (without the Spoks) is found in other fungal lineages, where it can be as large as 70 kb. Lastly, we provide experimental evidence that the Spok block is deleterious, with detrimental effects on spore production in strains which carry it. This union of meiotic drivers and a transposon has created a selfish element of impressive size in Podospora, challenging our perception of how TEs influence genome evolution and broadening the horizons in terms of what the upper limit of transposition may be.

59 BASIC BIOLOGICAL SCIENCES↗

Mycena genomes resolve the evolution of fungal bioluminescence

Mushroom-forming fungi in the order Agaricales represent an independent origin of bioluminescence in the tree of life; yet the diversity, evolutionary history, and timing of the origin of fungal luciferases remain elusive. We sequenced the genomes and transcriptomes of five bonnet mushroom species ( Mycena spp.), a diverse lineage comprising the majority of bioluminescent fungi. Two species with haploid genome assemblies ~150 Mb are among the largest in Agaricales, and we found that a variety of repeats between Mycena species were differentially mediated by DNA methylation. We show that bioluminescence evolved in the last common ancestor of mycenoid and the marasmioid clade of Agaricales and was maintained through at least 160 million years of evolution. Analyses of synteny across genomes of bioluminescent species resolved how the luciferase cluster was derived by duplication and translocation, frequently rearranged and lost in most Mycena species, but conserved in the Armillaria lineage. Luciferase cluster members were coexpressed across developmental stages, with the highest expression in fruiting body caps and stipes, suggesting fruiting-related adaptive functions. Our results contribute to understanding a de novo origin of bioluminescence and the corresponding gene cluster in a diverse group of enigmatic fungal species.

54 ENVIRONMENTAL SCIENCES↗

The flying spider-monkey tree fern genome provides insights into fern evolution and arborescence

To date, little is known about the evolution of fern genomes, with only two small genomes published from the heterosporous Salviniales. Here we assembled the genome of Alsophila spinulosa, known as the flying spider-monkey tree fern, onto 69 pseudochromosomes. The remarkable preservation of synteny, despite resulting from an ancient whole-genome duplication over 100 million years ago, is unprecedented in plants and probably speaks to the uniqueness of tree ferns. Our detailed investigations into stem anatomy and lignin biosynthesis shed new light on the evolution of stem formation in tree ferns. We identified a phenolic compound, alsophilin, that is abundant in xylem, and we provided the molecular basis for its biosynthesis. Finally, analysis of demographic history revealed two genetic bottlenecks, resulting in rapid demographic declines of A. spinulosa. The A. spinulosa genome fills a crucial gap in the plant genomic landscape and helps elucidate many unique aspects of tree fern biology.

59 BASIC BIOLOGICAL SCIENCES↗

Increasing Bacterial Tolerance and Metabolism of the Biofuel, N-Butanol Using Community-Level Evolution and Functional Genomics

Bioremediation capability should be developed along with biofuel technology to mitigate the potential damage of future spills. One biofuel that is being developed is biobutanol, since n-butanol is more energy dense and less volatile than ethanol. A bottleneck for industrial production of biobutanol is its toxicity; most microbes cannot survive about 1.5% v/v. Thus, microbial bioremediation of n-butanol would need microbes that can both tolerate and metabolize butanol. We used ecological and evolutionary biology approaches to find bacteria that could tolerate and metabolize butanol. We then tried to increase the metabolism of butanol by promising bacterial strains and communities. Ecological community-level assays and screenings were conducted followed by 16S amplicon sequencing to identify butanol-tolerant artificial bacterial communities. Promising communities were then tested for growth with butanol as the sole carbon source. Secondly, we looked for bacteria with alcohol dehydrogenase enzymes and looked to increase butanol metabolism. We found that the tolerance for n-butanol may be improved with repeated exposure, but it was difficult to switch from tolerance to metabolism. Bacterial community v dynamics may be influenced by n-butanol concentration, and there was putative butanol metabolism found with both research approaches.

09 BIOMASS FUELS↗

A genomic perspective on fungal diversity and evolution

Originating from aquatic unicellular ancestors, over the course of ~1 billion years, the fungi have evolved to occupy nearly all aerobic environments on the planet, diversified into millions of different ‘species’ and have developed complex multicellular structures. Their relatively small, simple genomes have facilitated massive-scale sequencing and allowed us to explore genome evolution across an ancient eukaryotic kingdom. With thousands of genomes from diverse lineages now available, this Review will discuss insights into fungal biology and evolution gleaned with genomics and other multi-omics approaches. Using published genomes available through GenBank and the Joint Genome Institute’s MycoCosm platform, we generated kingdom-wide phylogenies and used them to highlight how fungal genomes have changed over time. With this phylogeny as a guide, we also discuss major evolutionary transitions that occurred across the fungal kingdom. Although progress has been made, these efforts are hampered by biases in genome representation and limited characterization of gene functions. Here, in this study, we discuss these challenges and possible future directions to address them, including initiatives to characterize conserved genes of unknown function and scale up sequencing towards 10,000 annotated fungal genomes.

Mondo, Stephen J. [USDOE Joint Genome Institute (J↗

Files_used_for_figures

This folder includes all the relevant files used to generate the main Figures in the paper.

DNA repair↗

FutureTense

Protective vaccines and reliable diagnostics are essential tools for controlling viral diseases. However, the efficacy of these tools can be diminished by mutations in viral genomes. The delay between the emergence of new viral strains and the redesign of vaccines and diagnostics allows for continued viral transmission. Is it possible to address this challenge by computationally predicting viral genome sequence evolution? Can we “future-proof” vaccines and diagnostics by targeting both current and anticipated future sequence variants? While predicting viral evolution is still an unsolved, “grand challenge” problem in biology, the large, and rapidly growing, number of SARS-CoV-2 genome sequences provide an opportunity to quantify the ability of machine learning to predict viral genome sequence evolution. Towards this end, we have developed a simple computational model for predicting viral evolution at the level of individual nucleotides. The key metric for quantifying the per-base, prediction accuracy for viral evolution is the Mann-Whitney U statistic (or, equivalently, the area under the receiver operator curve). Since the Mann-Whitney U statistic is not a differentiable function, existing deep leaning packages (like Pytorch and Keras/TensorFlow) are not useful, as they require that the accuracy metric/objective function be analytically differentiable with respect to the model parameters. To overcome this challenge, we have implemented custom software, “FutureTense”, that can train a machine learning model by maximizing the non-differentiable Mann-Whitney U statistic. This software trains a machine learning model by exploring along the direction of the discrete gradient of the Mann-Whitney U statistic in the model parameter space. Parallel computing and genome sequence-specific optimizations are used to accelerate model training. The resulting machine learning model learns the observed high C->U mutation rates in the SARS-CoV-2 genome (which are potentially induced by host defenses) and provides prediction accuracies that are significantly better than one would expect from random chance. While predicting viral evolution is still quite far from a solved problem, the surprising performance of this simple model gives hope that the accuracy of predicting viral genome evolution can be further increased by more sophisticated approaches.

Gans, Jason↗