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Van de Peer, Y.

Publications and source records attributed to Van de Peer, Y..

At least 19 recordsLinked to original sources

Subgenome-Level Phylogeny Reveals an Allopolyploid Origin of Chloranthales from Ancestral Monocot and Eudicot Lineages

Angiosperms (flowering plants) represent the most species-rich lineage of land plants, yet deep phylogenetic relationships among their major clades, particularly within mesangiosperms, remain notoriously difficult to resolve. Although hybridization and whole-genome duplication (WGD) are recognized as major evolutionary forces, the contribution of ancient allopolyploidization, which combines hybridization with WGD, to deep-node phylogenetic discordance in mesangiosperms remains poorly understood. Here, we analyzed genomes from seven representative early-diverging angiosperm lineages, each containing no more than one lineage-specific WGD event. Using a comparative phylogenomic framework, we characterized WGD-derived paralogs across five WGD-bearing lineages. In contrast to other polyploid lineages, Chloranthales WGD-derived paralogs rarely formed sister relationships in gene trees. After evaluating alternative explanations, including incomplete lineage sorting, ancient paralogy, and analytical artifacts, we demonstrate that this discordant phylogenetic signal reflects the genomic legacy of an ancient allopolyploidization event. We further resolved the Chloranthales subgenomes by exploiting biased fractionation patterns within conserved syntenic regions. Subgenome-resolved phylogenomic analyses revealed that the dominant Chloranthales subgenome exhibits phylogenetic affinity with eudicots, whereas the recessive subgenome is associated with monocots, indicating a deep reticulate origin involving ancestral lineages related to these major angiosperm clades. Our findings provide subgenome-resolved evidence that ancient allopolyploidization can connect deeply diverged lineages during early angiosperm evolution, highlighting the importance of incorporating reticulate polyploid histories into phylogenomic frameworks for resolving deep evolutionary relationships.

systems biology↗

Trichome and inflorescence evolution in the paleopolyploid tree genus Greyia Hook. & Harv.

The southern African endemic tree genus Greyia Hook. & Harv. (Francoaceae, Geraniales) comprises three species distinguished by striking variation in trichome morphology and floral architecture, yet the genomic and regulatory basis of these traits has remained largely unexplored. Here, we present chromosome-scale genome assemblies for all recognized Greyia species, namely Greyia radlkoferi, Greyia sutherlandii, and Greyia flanaganii, providing the first high-quality genomic resources for Geraniales. Phylogenomic analyses placed Geraniales as sister to Crossosomatales, with divergence at [~]103 million years ago (Mya), and indicated that Greyia diversified recently during the Quaternary ([~]1.39 Mya). Comparative genomics revealed a Greyia-specific whole-genome triplication event dated to [~]86.9 Mya, generating extensive gene duplication which has been retained. Transcriptomic analyses linked divergence in trichome morphology to regulatory subfunctionalization of the conserved MYB-bHLH-WD40 (MBW) complex, including transcriptional silencing of GL1 and shifts in GL3/EGL3 expression in G. sutherlandii. In addition, analyses of flower and inflorescence identified expansion of MADS-box transcription factor families and species-specific cis-regulatory divergence in LFY and FT. Notably, predicted AGL6 binding sites are retained in the LFY and FT promoters of G. radlkoferi and G. sutherlandii but absent in G. flanaganii, which aligns with differences in inflorescence density among species. Together, these results demonstrate how polyploidy and regulatory divergence of conserved developmental pathways have shaped morphological diversification in Greyia. Significance StatementUnderstanding how morphological diversity arises from conserved pathways is a central evolutionary challenge, particularly in lineages shaped by ancient polyploidy. We present the first chromosome-scale genomes for the order Geraniales, focusing on three southern African endemic Greyia species. We demonstrate that regulatory divergence following a lineage-specific whole-genome triplication, rather than changes in gene content, drives variation in trichome morphology and floral architecture.

genomics↗

Highly repeatable phenotypic consequences of whole genome duplication in Spirodela polyrhiza

Whole-genome duplication (WGD) is widespread in plants, yet the extent to which it yields predictable phenotypic outcomes remains unclear. Here we show that the phenotypic consequences of genome doubling in a duckweed model system, Spirodela polyrhiza, are highly repeatable and largely deterministic. We previously generated three independent colchicine-induced autotetraploids from each of nine globally distributed diploid genotypes and, here, quantified growth and morphology across a salt gradient. In benign conditions, diploids grew faster, whereas tetraploids had larger, thicker fronds; with increasing salinity, the diploid advantage diminished and tetraploids often matched or exceeded diploid growth. Variance partitioning revealed that ploidy per se explains more phenotypic variation, including salt tolerance, than genotypic background, with rare within-genotype stochasticity. These results indicate that the shifts in morphology and stress tolerance from genome doubling are predictable and can outweigh the phenotypic effect from genetic sequence diversity.

evolutionary biology↗

Chromosomal-level genome of the Pinus massoniana 'Minlin WY36'

Owing to conifers complex and large genomes, it is challenging to construct a comprehensive reference genome and conduct evolutionary and genomic research. Here, we present the chromosome-level assembly of Pinus massoniana Minlin WY36, a pioneering conifer species used for afforestation, timber production, and oleoresin extraction. The genome size was determined to be 23.41 Gb, with a contig N50 value of 1.15 Mb and a scaffold N50 value of 2.02 Gb. A total of 23.16 Gb of reads (98.93% of the assembled genome) were anchored and oriented onto 12 pseudochromosomes, with chromosome lengths from 1.47 to 2.29 Gb. A total of 32,144 protein-coding genes were predicted, of which 27,173 (84.54%) were functionally annotated. The P. massoniana Minlin WY36 genome consists of 79.41% (18.57 Gb) repetitive sequences, among which long terminal repeat sequences (LTR) were the most abundant. Through comparative genomic analysis, we found that the unique and significantly expanded genes in P. massoniana Minlin WY36 were enriched in the metabolism related to resin synthesis. This study offers valuable insights into conifer evolution and contributes resources for further investigations of conifer adaptation and developmental processes.

genomics↗

Gene expression divergence following gene and genome duplications in spatially resolved plant transcriptomes

Gene and genome duplications are key drivers of plant genome evolution, expanding genetic repertoires and facilitating functional innovation. However, genes originating from different duplication mechanisms undergo different outcomes, especially at the expression level. Previous studies have demonstrated that segmental or whole-genome duplications generate duplicates with similar and somewhat redundant expression profiles across multiple tissues, while other duplicates display increased divergence, ultimately leading to functional innovations. However, little is known about how duplicates diverge in expression across cell types in a single tissue. Here, we used high-resolution spatial transcriptomic data from five species (Arabidopsis thaliana, Glycine max, Phalaenopsis aphrodite, Zea mays, and Hordeum vulgare) to investigate the evolution of gene expression following gene duplications. We found that genes originating from segmental or whole-genome duplications display increased expression levels, expression breadths, spatial variability, and number of coexpression partners. Duplication mechanisms that preserve cis-regulatory landscapes typically generate paralogs with more preserved expression profiles, but such differences by duplication mode disappear over time. Expression divergence also depends on gene functions, with dosage-sensitive gene families displaying highly preserved expression profiles, while families involved in more specialized processes (e.g., flowering and phytohormone biosynthesis) display increased divergence. Paralogs originating from large-scale (including whole-genome) duplications display redundant and/or overlapping expression profiles, indicating functional redundancy and/or subfunctionalization, while small-scale duplicates diverge asymmetrically, indicating neofunctionalization. Collectively, our findings provide new insights into the tempo and mode of gene expression evolution, helping understand how gene and genome duplications shape cell identities.

evolutionary biology↗

Polyploid - diploid coexistence in the greater duckweed Spirodela polyrhiza

Polyploidy, resulting from whole-genome duplication (WGD), is widespread among plants and originates in sympatry with their lower-ploidy progenitors. New polyploids can only succeed when they overcome the competitive disadvantage against their progenitors or through sufficient niche differentiation as resulting in a negative frequency dependent growth. Because polyploidy is frequently associated with cold, dry, and saline environments, stress is anticipated to be the key to polyploid success. We examined the invasion of neotetraploid duckweed (Spirodela polyrhiza) strains in populations of their direct diploid progenitors, in control and salt stress conditions in replicated microcosms. We also tested the reverse scenario, that is, the invasion of diploids in neotetraploid populations, to determine if the initial proportion of tetraploids affects the outcome of competition. Our results showed that the proportion of tetraploids declined in all tetraploid and all diploid invasions and it did so at a different rate than expected from only differences in intrinsic growth rate. Salt stress affected the decline in tetraploid proportion differently across strains. We also found evidence for negative frequency dependent growth that, nonetheless, was insufficient to overcome competitive disadvantages of neopolyploids towards their diploid progenitor. We showcase a robust quantitative pipeline from flow cytometry of mixed-ploidy populations to population model fitting. In doing so, we demonstrate the important effect of competition and frequency dependency on neopolyploid establishment. Therefore, we caution for inferring neopolyploid success from intrinsic growth rates alone.

plant biology↗

The Rise of Polyploids During Environmental Catastrophes

Polyploidy, or whole-genome duplication (WGD), serves as both a significant evolutionary force and a potential evolutionary dead end, occurring extensively across the tree of life, particularly among angiosperms. Despite the prevalence of polyploid organisms, instances of ancient polyploidy are surprisingly rare, presenting a paradox that remains poorly understood. In this study, we constructed a comprehensive genomic dataset of 470 angiosperm species to address this issue. We developed a highly congruent evolutionary timescale and dated 132 ancient WGD events that are non-randomly distributed, revealing a clustering around pivotal periods of environmental upheaval and extinction. Notably, our findings highlight a strong correlation between waves of paleopolyploidization and significant events such as the Middle Miocene Disruption, the Eocene-Oligocene transition (EOT), the Paleocene-Eocene Thermal Maximum (PETM), the Cretaceous-Paleogene (K-Pg) extinction, and different oceanic anoxic (OAE) events, several of which can be linked to extinction events impacting flowering plant genera. By integrating multiple lines of evidence, we propose that polyploid organisms have an increased chance of survival during times of great environmental turmoil, a conclusion with important implications in the context of contemporary climate change and rapid global warming.

evolutionary biology↗

The spliceosomal component GAMETOPHYTIC FACTOR 1 (GFA1) regulates a key photoperiodic switch

Plants have evolved sophisticated mechanisms to perceive and interpret daytime in order to flower at an optimal time point. Here we show that the spliceosomal component GAMETOPHYTIC FACTOR 1 (GFA1) constitutes a previously unrecognized key photoperiodic switch, that is essential for flowering in long days. We show that gfa1 hypomorphic (gfa1hyp) plants fail to initiate flowering in long-days (LD), which correlates with ectopic activation of the short-day (SD) flowering repressor ARABIDOPSIS THALIANA CENTRORADIALIS (ATC). Accordingly, flowering is restored upon inactivation of ATC in gfa1hyp mutants. A novel tissue-specific in-planta splice assay and comprehensive RNAseq profiling of gfa1hyp mutants indicate that GFA1 mediated pre-mRNA splicing is substrate specific, as previously suggested for GFA1 orthologs. Furthermore, we show that gfa1hyp mutants accumulate nonsense transcripts of the photoreceptor components PHYB and RRC1, suggesting inappropriate photoreceptor signaling as a potential cause for the ectopic activation of the SD characteristic profile in gfa1hyp. In fact, known downstream targets of the phytochrome system such as RS31, SR34a, SRp30 accumulate reduced amounts of light-dependent splice isoforms. Together, our data reveal a link between spliceosome composition and long-day flowering, based on complex transcriptional readouts in response to day length.

developmental biology↗

Expanding the toolkit for ploidy manipulation in Chlamydomonas reinhardtii

SummaryO_LIWhole genome duplications, widely observed in plant lineages, have significant evolutionary and ecological impacts. Yet, our current understanding of the direct implications of ploidy shifts on short- and long-term plant evolution remains fragmentary, necessitating further investigations across multiple ploidy levels. C_LIO_LIChlamydomonas reinhardtii, a haploid green alga, is a valuable model organism with profound potential to study the impact of ploidy increase on the longer-term in a laboratory environment. This is partly due to the ability to successfully increase the ploidy level. C_LIO_LIWe developed a strategy to engineer ploidy in Chlamydomonas reinhardtii using a collection of non-interfering antibiotic selectable markers. This approach allows to induce higher ploidy levels in Chlamydomonas reinhardtii and is applicable to field isolates, which expands beyond specific auxotroph laboratory strains and broadens the genetic diversity of parental haploid strains that can be crossed. We implement flow cytometry for precise measurement of the genome size of strains of different ploidy. C_LIO_LIWe demonstrate the creation of diploids, triploids and tetraploids by engineering North American field isolates, broadening the application of synthetic biology principles in Chlamydomonas reinhardtii. C_LIO_LIOur study greatly facilitates the application of Chlamydomonas reinhardtii to study polyploidy, both in fundamental and applied settings. C_LI

synthetic biology↗

The Draparnaldia genome: alternative mechanisms for multicellularity and terrestrialization in green plants

Green plants contain two algal lineages: Streptophyte algae that diverged into land plants and Chlorophyte algae that are mostly aquatic. Draparnaldia is a Chlorophyte alga morphologically resembling mosses and living in both, the aquatic and terrestrial habitats. Because of its complex morphology and terrestrial adaptations, Draparnaldia can provide new insights into the evolution of multicellularity and terrestrialization in green plants. To develop Draparnaldia into a model, we de novo sequenced its genome and transcriptomes, and profiled its phytohormone repertoire. We found that 1) Expanded gene families in Draparnaldia with respect to unicellular Chlamydomonas are linked to multicellularity and abiotic stresses. 2) Draparnaldias terrestrial adaptations are reflected at both the morphological and molecular levels. 3) Draparnaldia synthesizes most of the phytohormones used by land plants to thrive in terrestrial habitats. All of this makes Draparnaldia a powerful model to uncover and study alternative evolutionary trajectories towards multicellularity and terrestrialization in plants.

evolutionary biology↗

Asymmetric genome merging leads to gene expression novelty through nucleo-cytoplasmic disruptions and transcriptomic shock in Chlamydomonas triploids

Genome merging is a common phenomenon in many organisms, causing a wide range of consequences on phenotype, adaptation, and gene expression, among other effects, yet its broader implications are not well understood. Two consequences of genome merging on gene expression remain poorly understood: dosage effects and evolution of expression. In this study, we employed Chlamydomonas reinhardtii as a model to investigate the effects of asymmetric genome merging by crossing a diploid with a haploid strain to create a novel triploid line. Five independent clonal lineages derived from this triploid line were evolved for 425 asexual generations in a laboratory natural selection (LNS) experiment. Utilizing fitness assays, qPCR, and RNA-Seq, we assessed the immediate consequences of genome merging and subsequent evolution over time. Our findings reveal substantial alterations in gene expression, protein homeostasis (proteostasis) and cytonuclear stoichiometry. Notably, gene expression exhibited expression level dominance and transgressivity (i.e., expression level higher or lower than either parent). Ongoing expression level dominance and a pattern of "functional dominance" from the haploid parent was observed, alongside remarkable stability in expression patterns across generations. Despite major nucleo-cytoplasmic disruptions, enhanced fitness was detected in the triploid strain. By comparing gene expression across generations, our results indicate that proteostasis restoration is a critical component of rapid adaptation following genome merging in Chlamydomonas reinhardtii and possibly other systems.

evolutionary biology↗

HybridExpress: an R/Bioconductor package for comparative transcriptomic analyses of hybrids and their progenitors

Hybridization, the process of crossing individuals from diverse genetic backgrounds, plays a pivotal role in evolution, biological invasiveness, and crop breeding. At the transcriptional level, hybridization often leads to complex non-additive effects, presenting challenges for understanding its consequences. Although standard transcriptomic analyses exist to compare hybrids to their progenitors, such analyses have not been implemented in a software package, hindering reproducibility. Here, we introduce HybridExpress, an R/Bioconductor package designed to facilitate the analysis, visualization, and comparison of gene expression patterns in hybrid triplets (hybrids and their progenitors). HybridExpress provides users with a user-friendly and comprehensive workflow that includes all standard comparative analyses steps, including data normalization, calculation of midparent expression values, sample clustering, expression-based gene classification into categories and classes, and overrepresentation analysis for functional terms. We illustrate the utility of HybridExpress through comparative transcriptomic analyses of cotton allopolyploidization and rice root trait heterosis. HybridExpress is designed to streamline comparative transcriptomic studies of hybrid triplets, advancing our understanding of evolutionary dynamics in allopolyploids, and enhancing plant breeding strategies. HybridExpress is freely accessible from Bioconductor (https://bioconductor.org/packages/HybridExpress) and its source code is available on GitHub (https://github.com/almeidasilvaf/HybridExpress).

bioinformatics↗

doubletrouble: an R/Bioconductor package for the identification, classification, and analysis of gene and genome duplications

Gene and genome duplications are major evolutionary forces that shape the diversity and complexity of life. However, different duplication modes have distinct impacts on gene function, expression, and regulation. Existing tools for identifying and classifying duplicated genes are either outdated or not user-friendly. Here, we present doubletrouble, an R/Bioconductor package that provides a comprehensive and robust framework for analyzing duplicated genes from genomic data. doubletrouble can detect and classify gene pairs as derived from six duplication modes (segmental, tandem, proximal, retrotransposon-derived, DNA transposon-derived, and dispersed duplications), calculate substitution rates, detect signatures of putative whole-genome duplication events, and visualize results as publication-ready figures. We applied doubletrouble to classify the duplicated gene repertoire in 822 eukaryotic genomes, which we made available through a user-friendly web interface (available at https://almeidasilvaf.github.io/doubletroubledb). doubletrouble is freely accessible from Bioconductor (https://bioconductor.org/packages/doubletrouble), and it provides a valuable resource to study the evolutionary consequences of gene and genome duplications.

bioinformatics↗

Interspecific transfer of genetic information through polyploid bridges

Many organisms have more than two sets of chromosomes, due to whole genome duplication (WGD), and are thus polyploid. Despite usually being an ephemeral state in the history of life, polyploidy is widely recognized as an important source of genetic novelty over macroevolutionary scales. More recently, polyploidy has also been shown to facilitate interspecific gene flow, circumventing reproductive barriers between their diploid ancestors. Yet, the implications of WGD-linked introgression on community-level evolutionary dynamics remain unknown. Here, we develop a model of cytotype dynamics within mixed-ploidy populations to demonstrate that polyploidy can in fact serve as a bridge for gene flow between diploid lineages, where introgression is fully or partially hampered by the species barrier. Polyploid bridges emerge in the presence of triploid organisms, which despite critically low levels of viability, can still allow the transfer of alleles between diploid states of independently evolving mixed-ploidy species. Notably, while marked genetic divergence prevents WGD-mediated interspecific gene flow, we show that increased recombination rates can offset these evolutionary constraints, which allows a more efficient sorting of alleles at higher-ploidy levels before introgression into diploid gene pools. Additionally, we derive an analytical approximation for the rate of gene flow at the tetraploid level necessary to supersede introgression between diploids with non-zero introgression rates, which is especially relevant for plant species complexes, where interspecific gene flow is ubiquitous. Altogether, our results illustrate the potential impact of polyploid bridges on evolutionary change within and between mixed-ploidy populations.

evolutionary biology↗

Rapid establishment of species barriers in plants compared to animals

Speciation, the process through which new reproductively isolated species emerge from ancestral populations, occurs due to the gradual accumulation of barriers to gene flow within genomes. To date, the notion that interspecific genetic exchange occurs more frequently between plant species than animals species has gained a strong footing in the scientific discourse. By examining the dynamics of gene flow across a continuum of divergence in both kingdoms, we observe the opposite relationship: plants experience less introgression than animals at the same level of genetic divergence, suggesting that species barriers are established more rapidly in plants. This pattern raises questions about which differences in microevolutionary processes between plants and animals influence the dynamics of reproductive isolation establishment at the macroevolutionary scale. One Sentence SummaryGenetic exchange is more frequent between animal species than plants, challenging historical views.

evolutionary biology↗

A metabolic perspective on polyploid invasion and the emergence of life histories: insights from a mechanistic model

Whole genome duplication (WGD, polyploidization), the fusion of unreduced gametes, has been identified as a driver of genetic and phenotypic novelty. Unreduced gamete formation is common in a wide range of species, but surprisingly, few polyploidization events have shown to be ecologically successful. Positive density dependence, by minority cytotype exclusion, and niche shifts are currently considered the most important drivers behind ecological failure or success. Genome doubling also results in increased cell sizes and metabolic expenses which, on their own may be sufficient to drive polyploid establishment in stable environments where their simple ancestors thrive. We developed a mechanistic model, motivated by data from natural plant polyploid species, to test whether realistic changes in size and metabolic efficiency allow polyploids to coexist with, or even invade, their original diploid population. Central to the model is metabolic efficiency, a functional trait that determines how energy gained from size-dependent photosynthetic metabolism is allocated to basal metabolism, somatic growth and reproductive growth. Polyploid invasion was observed across a wide range of metabolic efficiency differences between polyploids and their ancestors. Higher metabolic efficiency facilitates polyploid invasion, but even with minor deficits, establishment was facilitated by recurrent formation in these settings of high competition for nutrients. Interestingly, a long-term coexistence with the diploid ancestor was found to be possible only within a narrow range of this parameter space. Perenniality of the plants did not qualitatively affect these insights. Feedbacks between size-dependent metabolism and allocation of gained energy generated eventually size and age differences, resulting in intra- and intercytotype competition for nutrients as the major force for population dynamics. We thus demonstrate that changes in metabolic efficiency on their own are sufficient to impose establishment, but these advantages do not need to be substantial.

ecology↗

The duplication of genomes and gene regulatory networks and its potential for evolutionary adaptation and survival

The importance of whole genome duplication (WGD), or polyploidy, for evolution, is controversial. Whereas some view WGD mainly as detrimental and an evolutionary dead end, there is growing evidence that (the establishment of) polyploidy can help overcome environmental change, stressful conditions, or periods of extinction. However, despite much research, the mechanistic underpinnings of why and how polyploids might be able to outcompete or outlive non-polyploids at times of environmental upheaval remain elusive, especially for autopolyploids, in which heterosis effects are limited. On the longer term, WGD might increase both mutational and environmental robustness due to redundancy and increased genetic variation, but on the short - or even immediate - term, selective advantages of WGDs are harder to explain. Here, by duplicating artificially generated Gene Regulatory Networks (GRNs), we show that duplicated GRNs - and thus duplicated genomes - show higher signal output variation than non-duplicated GRNs. This increased variation leads to niche expansion and can provide polyploid populations with substantial advantages to survive environmental turmoil. In contrast, under stable environments, GRNs might be maladaptive to changes, a phenomenon that is exacerbated in duplicated GRNs. We believe that these results provide new insights into how genome duplication and (auto)polyploidy might help organisms to adapt quickly to novel conditions and to survive ecological uproar or even cataclysmic events.

evolutionary biology↗

Assessing the quality of comparative genomics data and results with the cogeqc R/Bioconductor package

Comparative genomics has become an indispensable part of modern biology due to the advancements in high-throughput sequencing technologies and the accumulation of genomic data in public databases. However, the quality of genomic data and the choice of parameters used in software tools used for comparative genomics can greatly impact the accuracy of results. To address these issues, we present cogeqc, an R/Bioconductor package that provides researchers with a toolkit to assess genome assembly and annotation quality, orthogroup inference, and synteny detection. The package offers context-guided assessments of assembly and annotation statistics by comparing observed statistics to those of closely-related species on NCBI. To assess orthogroup inference, cogeqc calculates a protein domain-aware orthogroup score that aims at maximizing the number of shared protein domains within the same orthogroup. The assessment of synteny detection consists in representing anchor gene pairs as a synteny network and analyzing its graph properties, such as clustering coefficient, node count, and scale-free topology fit. The application of cogeqc to real data sets allowed for an evaluation of multiple parameter combinations for orthogroup inference and synteny detection, providing researchers with guidelines to aid in the selection of the most appropriate tools and parameters for their specific data.

bioinformatics↗