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Lysak, M. A.

Publications and source records attributed to Lysak, M. A..

9 recordsLinked to original sources

Why woodiness repeatedly evolves--and disappears

Derived woodiness--the evolution of woody growth from herbaceous ancestors--has arisen hundreds of times across flowering plants, yet the environmental conditions associated with its repeated evolution remain poorly understood. Here, we analyse woodiness evolution in the mustard family (Brassicaceae; ~4,150 species) using a time-calibrated phylogeny of 2,927 species, including 374 of the 385 known woody species, together with global growth-form and climatic niche data. We infer 231 independent origins of woodiness alongside 176 reversals to herbaceousness, indicating that woodiness evolves repeatedly but remains evolutionarily unstable. Although woody species are enriched on islands, most occur on the mainland, where woodiness is consistently associated with drought and reduced frost. Correlated-evolution analyses reveal that drought is associated primarily with the persistence of woodiness, whereas reduced frost is associated with gains of woodiness and increased frost with its loss. These findings identify distinct climatic associations with the gain, persistence, and loss of woody growth forms.

evolutionary biology↗

CRISPR-mediated centromere fission generates neo-chromosomes with distorted meiotic inheritance in Arabidopsis

Centromeres are essential for chromosome segregation and are epigenetically defined by CENH3/CENP-A nucleosomes. Centromere position along chromosomes varies within and between species, ranging from telocentric to metacentric architectures. Yet, how centromere position influences chromosome inheritance and karyotype evolution remains poorly understood. To reposition the centromere, we used CRISPR-Cas9 to break the centromeric satellite array of Arabidopsis thaliana chromosome 3. Fission chromosomes rapidly acquired telomeres, converting a metacentric into two stable telocentric neo-chromosomes. Neo-centromere formation involved genetic restructuring and de novo satellite higher-order repeat formation, together with epigenetic remodeling of CENH3 and DNA methylation. Crossing the six-chromosome fission line to five-chromosome wild type produced a meiosis-specific trivalent that mis-segregated and generated aneuploidy. Trivalent recombination doubled through two obligate crossovers, which were shifted towards the telomeres. Inheritance was strongly distorted in favor of the wild type centromere, as telocentrics segregated into inviable monosomic gametes. The reciprocal trisomic gametes were associated with centromere-proximal recombination, demonstrating that crossover position governs trivalent segregation. Distortion further increased when CENH3 was over-expressed, implicating centromere strength in the outcomes of trivalent meiosis. Our results reveal rapid centromere remodeling following karyotype change, and how trivalent centromere architecture distorts inheritance, with implications for hybrid incompatibility and synthetic chromosome design.

genetics↗

Building the meiotic bouquet: A nuclear polarity pathway in Arabidopsis

Meiotic chromosome pairing requires the establishment of a polarized nuclear architecture, but how this polarity emerges from the interplay of telomeres, the nucleolus, and the nuclear envelope remains incompletely understood in plants. Using stage-resolved three-dimensional imaging of intact Arabidopsis thaliana male meiocytes, we reconstruct the early meiotic sequence that links the premeiotic chromosome arrangement to telomere bouquet formation. We show that telomeres enter meiosis positioned around the nucleolus and, at the onset of leptotene, undergo a coordinated and directionally biased departure from the nucleolar surface. This transition establishes asymmetric early contacts with discrete SUN1/2-enriched domains of the nuclear envelope, well before visible clustering occurs, revealing that the envelope is pre-patterned into regions permissive for telomere attachment. As zygotene progresses, these early contacts consolidate into a nucleolus-associated bouquet, whereas the nucleolar organizer regions (NORs) maintain a stable position and remain unsynapsed. Centromeres reorganize in parallel and progressively shift away from the developing telomere domain, giving rise to the classical centromere-telomere opposition. Rare nuclei exhibiting bouquet formation opposite the nucleolus correspond to alternative SUN1/2 microdomain topologies, indicating that nuclear-envelope patterning, rather than telomere behavior, ultimately determines the polarity state. Together, these findings provide a mechanistic framework in which NOR stability, SUN-patterned membrane domains, and telomere migration act sequentially to generate a polarized meiotic nucleus in Arabidopsis.

plant biology↗

Orthologous synteny provides robust structural evidence for the ancestral angiosperm ε-WGD

The ancestral angiosperm whole-genome duplication ({varepsilon}-WGD) is a pivotal yet contentious event that has long been debated. A recent study refuted its occurrence based on deviations from expected retention patterns of dosage-sensitive genes. Here, we provide both structural (orthologous synteny) and phylogenetic (subgenome-aware) evidence to revisit this debate. With improved annotation of the Ginkgo genome, we uncover a clear 1:2 orthologous synteny ratio between Ginkgo and early-diverging angiosperms (Amborella and Aristolochia), which lack lineage-specific WGDs. Subgenome-aware phylogenomic analyses further demonstrate that the Amborella/Aristolochia subgenomes diverged after the gymnosperm-angiosperm split but before the radiation of extant angiosperms. Together, these findings provide direct structural evidence for an ancestral angiosperm tetraploidization in the early Jurassic, following divergence from gymnosperms. We argue that the recent refutation of the {varepsilon}-WGD relies on restrictive assumptions regarding ploidy level and duplicate retention that may not hold for deep-time polyploidy events. Our results provide a robust resolution to this long-standing debate and reaffirm the {varepsilon}-WGD as a shared synapomorphy of extant angiosperms.

evolutionary biology↗

Kinetochore and ionomic adaptation to whole genome duplication

Transforming genomic and cellular landscapes in a single generation, whole genome duplication (WGD) brings fundamental challenges, but is also associated with diversification. How is WGD tolerated, and what processes commonly evolve to stabilize the resulting polyploid? Here we study this in Cochlearia spp., which have experienced multiple WGDs in the last 300,000 years. We first generate a chromosome-scale genome and sequence 113 individuals from 33 diploid, tetraploid, hexaploid, and outgroup populations. We detect the clearest post-WGD selection signatures in functionally interacting kinetochore components and ion transporters. We structurally model these derived selected alleles, identifying striking WGD-relevant functional variation, and then compare these results to independent recent post-WGD selection in Arabidopsis arenosa and Cardamine amara. Most prominent in these results is genetic evidence of at least four functionally interacting kinetochore complex subunits in adaptation to WGD at the centromere among our very top selective sweep outliers. In addition, some of the same biological processes evolve in all three WGDs, but specific genes recruited are flexible. This points to a polygenic basis for modifying systems that control the kinetochore, meiotic crossover number, DNA repair, ion homeostasis, and cell cycle. Given that DNA management (especially repair) is the most salient category with the strongest selection signal, we speculate that the generation rate of structural genomic variants may be altered by WGD in young polyploids, contributing to their occasionally spectacular adaptability observed across kingdoms. Significance StatementWhole-genome duplication (WGD) occurs in all kingdoms and is linked to adaptation, speciation, domestication, and even cancer outcome. But WGD is a shock to the system, and commonly disrupts cell division due to increased DNA management burden and transformed cell physiology. Nevertheless, the hopeful monster that survives WGD is special, occasionally experiencing runaway success. Why do some thrive but others die? Here we introduce a powerful new model, Cochlearia, which has benefitted from multiple WGDs, and we provide the first genetic evidence of rapid adaptation of functionally interacting components of the cell division machinery, the kinetochore. We also compare which processes and genes evolve to stabilize the new polyploid in three independent cases and highlight common mechanisms.

evolutionary biology↗

Global Phylogeny of the Brassicaceae Provides Important Insights into Gene Discordance

The mustard family (Brassicaceae) is a scientifically and economically important family, containing the model plant Arabidopsis thaliana and numerous crop species that feed billions worldwide. Despite its relevance, most published family phylogenies are incompletely sampled, generally contain massive polytomies, and/or show incongruent topologies between datasets. Here, we present the most complete Brassicaceae genus-level family phylogenies to date (Brassicaceae Tree of Life, or BrassiToL) based on nuclear (>1,000 genes, almost all 349 genera and 53 tribes) and plastome (60 genes, 79% of the genera, all tribes) data. We found cytonuclear discordance between nuclear and plastome-derived phylogenies, which is likely a result of rampant hybridisation among closely and more distantly related species, and highlight rogue taxa. To evaluate the impact of this rampant hybridisation on the nuclear phylogeny reconstruction, we performed four different sampling routines that increasingly removed variable data and likely paralogs. Our resulting cleaned subset of 297 nuclear genes revealed high support for the tribes, while support for the main lineages remained relatively low. Calibration based on the 20 most clock-like nuclear genes suggests a late Eocene to late Oligocene icehouse origin of the family. Finally, we propose five new or re-established tribes, including the recognition of Arabidopsideae, a monotypic tribe to accommodate Arabidopsis. With a worldwide community of thousands of researchers working on this family, our new, densely sampled family phylogeny will be an indispensable tool to further highlight Brassicaceae as an excellent model family for studies on biodiversity and plant biology.

evolutionary biology↗

Chromosome-level genome assembly of Rorippa aquatica revealed its allotetraploid origin and mechanisms of heterophylly upon submergence

The ability to respond to environmental variability is essential for living systems, especially to sessile organisms such as plants. The amphibious plant Rorippa aquatica exhibits a drastic type of phenotypic plasticity known as heterophylly, a phenomenon where leaf form is altered in response to the surrounding environment. Although heterophylly has been studied in various plant species, its molecular mechanism has not been fully elucidated. To establish the genetic basis and analyze the evolutionary processes responsible for heterophylly, we assembled the chromosome-level genome of R. aquatica by combining data from Illumina short-read sequencing, PacBio long-read sequencing, and High-throughput Chromosome Conformation Capture (Hi-C) sequencing technologies. Fine-scale comparative chromosome painting and chromosomal genomics revealed that allopolyploidization and subsequent post-polyploid descending dysploidy occurred during R. aquatica speciation. The genomic information above was the basis for the transcriptome analyses to examine the mechanisms involved in heterophylly, especially in response to the submerged condition, which uncovered that the ethylene and blue light signaling pathways participate in regulating heterophylly under submerged conditions. The assembled R. aquatica reference genome provides novel insights into the molecular mechanisms and evolution of heterophylly.

plant biology↗

Intact rDNA arrays of Potentilla-origin detected in Erythronium nucleus suggest recent eudicot-to-monocot horizontal transfer

The occurrence of horizontal gene transfer (HGT) in Eukarya is increasingly gaining recognition. Nuclear-to-nuclear jump of DNA between plant species at high phylogenetic distance and devoid of intimate association (e.g., parasitism) is still scarcely reported. Within eukaryotes, components of ribosomal DNA (rDNA) multigene family have been found to be horizontally transferred in protists, fungi and grasses. However, in neither case HGT occurred between phylogenetic families, nor the transferred rDNA remained tandemly arrayed and transcriptionally active in the recipient organism. This study aimed to characterize an alien eudicot-type of 45S nuclear rDNA, assumingly transferred horizontally to the genome of monocot European Erythronium (Liliaceae). Genome skimming coupled by PacBio HiFi sequencing of a BAC clone were applied to determine DNA sequence of the alien rDNA. A clear phylogenetic signal traced the origin of the alien rDNA of Erythronium back to the Argentea clade of Potentilla (Rosaceae) and deemed the transfer to have occurred in the common ancestor of E. dens-canis and E. caucasicum. Though being discontinuous, transferred rDNA preserved its general tandemly arrayed feature in the host organism. Southern blotting, molecular cytogenetics, and sequencing of a BAC clone derived from flow-sorted nuclei indicated integration of the alien rDNA into the recipients nuclear genome. Unprecedently, dicot-type alien rDNA was found to be transcribed in the monocot Erythronium albeit much less efficiently than the native counterpart. This study adds a new example to the growing list of naturally transgenic plants while holding the scientific community continually in suspense about the mode of DNA transfer. Significance StatementRibosomal DNA is an essential component of all cellular genomes. In plants, accidental movement of rDNA via horizontal gene transfer has only been reported in sexually incompatible grasses (monocots) where it involved non-functional rDNA units. In this study, we propose that evolutionary trajectories of eudicots and monocots were bypassed by the jump of rDNA from a Potentilla species (Rosaceae) to a common ancestor of Erythronium dens-canis and E. caucasicum (Liliaceae). The alien eudicot-type rDNA appeared relatively well conserved in the examined host Erythronium genome, being able to be expressed while preserving its general tandemly repeated feature, evidences that have no match in earlier literature.

plant biology↗

Gradual evolution of allopolyploidy in Arabidopsis suecica

The majority of diploid organisms have polyploid ancestors. The evolutionary process of polyploidization (and subsequent re-diploidization) is poorly understood, but has frequently been conjectured to involve some form of "genome shock" -- partly inspired by studies in crops, where polyploidy has been linked to major genomic changes such as genome reorganization and subgenome expression dominance. It is unclear, however, whether such dramatic changes would be characteristic of natural polyploidization, or whether they are a product of domestication. Here, we study polyploidization in Arabidopsis suecica (n = 13), a post-glacial allopolyploid species formed via hybridization of A. thaliana (n = 5) and A. arenosa (n = 8). We generated a chromosome-level genome assembly of A. suecica and complemented it with polymorphism and transcriptome data from multiple individuals of all species. Despite a divergence of [~]6 Mya between the two ancestral species and appreciable differences in their genome composition, we see no evidence of a genome shock: the A. suecica genome is highly colinear with the ancestral genomes, there is no subgenome dominance in expression, and transposable element dynamics appear to be stable. We do, however, find strong evidence for changes suggesting gradual adaptation to polyploidy. In particular, the A. thaliana subgenome shows upregulation of meiosis-related genes, possibly in order to prevent aneuploidy and undesirable homeologous exchanges that are frequently observed in experimentally generated A. suecica, and the A. arenosa subgenome shows upregulation of cyto-nuclear related processes, possibly in response to the new cytoplasmic environment of A. suecica, with plastids maternally inherited from A. thaliana.

evolutionary biology↗