ABSTRACT
Model species continue to underpin groundbreaking plant science research. At the same time, the phylogenetic resolution of the land plant Tree of Life continues to improve. The intersection of these two research paths creates a unique opportunity to further extend the usefulness of model species across larger taxonomic groups. Here we promote the utility of the Arabidopsis thaliana model species, especially the ability to connect its genetic and functional resources, to species across the entire Brassicales order. We focus on the utility of using genomics and phylogenomics to bridge the evolution and diversification of several traits across the Brassicales to the resources in Arabidopsis, thereby extending scope from a model species by establishing a "model clade". These Brassicales-wide traits are discussed in the context of both the model species Arabidopsis thaliana and the family Brassicaceae. We promote the utility of such a "model clade" and make suggestions for building global networks to support future studies in the model order Brassicales.
ABSTRACT
The sacred datura plant (Solanales: Solanaceae: Datura wrightii) has been used to study plant-herbivore interactions for decades. The wealth of information that has resulted leads it to have potential as a model system for studying the ecological and evolutionary genomics of these interactions. We present a de novo Datura wrightii genome assembled using PacBio HiFi long-reads. Our assembly is highly complete and contiguous (N50 = 179Mb, BUSCO Complete = 97.6%). We successfully detected a previously documented ancient whole genome duplication using our assembly and have classified the gene duplication history that generated its coding sequence content. We use it as the basis for a genome-guided differential expression analysis to identify the induced responses of this plant to one of its specialized herbivores (Coleoptera: Chrysomelidae: Lema daturaphila). We find over 3000 differentially expressed genes associated with herbivory and that elevated expression levels of over 200 genes last for several days. We also combined our analyses to determine the role that different gene duplication categories have played in the evolution of Datura-herbivore interactions. We find that tandem duplications have expanded multiple functional groups of herbivore responsive genes with defensive functions, including UGT-glycosyltranserases, oxidoreductase enzymes, and peptidase inhibitors. Overall, our results expand our knowledge of herbivore-induced plant transcriptional responses and the evolutionary history of the underlying herbivore-response genes.
Subject(s)
Coleoptera , Datura , Animals , Herbivory , Gene Duplication , Datura/genetics , Datura/metabolism , Coleoptera/geneticsABSTRACT
The members of the tribe Brassiceae share a whole-genome triplication (WGT), and one proposed model for its formation is a two-step pair of hybridizations producing hexaploid descendants. However, evidence for this model is incomplete, and the evolutionary and functional constraints that drove evolution after the hexaploidy are even less understood. Here, we report a new genome sequence of Crambe hispanica, a species sister to most sequenced Brassiceae. Using this new genome and three others that share the hexaploidy, we traced the history of gene loss after the WGT using the Polyploidy Orthology Inference Tool (POInT). We confirm the two-step formation model and infer that there was a significant temporal gap between those two allopolyploidizations, with about a third of the gene losses from the first two subgenomes occurring before the arrival of the third. We also, for the 90,000 individual genes in our study, make parental subgenome assignments, inferring, with measured uncertainty, from which of the progenitor genomes of the allohexaploidy each gene derives. We further show that each subgenome has a statistically distinguishable rate of homoeolog losses. There is little indication of functional distinction between the three subgenomes: the individual subgenomes show no patterns of functional enrichment, no excess of shared protein-protein or metabolic interactions between their members, and no biases in their likelihood of having experienced a recent selective sweep. We propose a "mix and match" model of allopolyploidy, in which subgenome origin drives homoeolog loss propensities but where genes from different subgenomes function together without difficulty.
Subject(s)
Genome , Polyploidy , Evolution, Molecular , Genome, Plant , Humans , Hybridization, Genetic , PhylogenyABSTRACT
PREMISE: The history of angiosperms is marked by repeated rounds of ancient whole-genome duplications (WGDs). Here we used state-of-the-art methods to provide an up-to-date view of the distribution of WGDs in the history of angiosperms that considers both uncertainty introduced by different WGD inference methods and different underlying species-tree hypotheses. METHODS: We used the distribution synonymous divergences (Ks) of paralogs and orthologs from transcriptomic and genomic data to infer and place WGDs across two hypothesized angiosperm phylogenies. We further tested these WGD hypotheses with syntenic inferences and Bayesian models of duplicate gene gain and loss. RESULTS: The predicted number of WGDs in the history of angiosperms (~170) based on the current taxon sampling is largely similar across different inference methods, but varies in the precise placement of WGDs on the phylogeny. Ks-based methods often yield alternative hypothesized WGD placements due to variation in substitution rates among lineages. Phylogenetic models of duplicate gene gain and loss are more robust to topological variation. However, errors in species-tree inference can still produce spurious WGD hypotheses, regardless of method used. CONCLUSIONS: Here we showed that different WGD inference methods largely agree on an average of 3.5 WGD in the history of individual angiosperm species. However, the precise placement of WGDs on the phylogeny is subject to the WGD inference method and tree topology. As researchers continue to test hypotheses regarding the impacts ancient WGDs have on angiosperm evolution, it is important to consider the uncertainty of the phylogeny as well as WGD inference methods.
Subject(s)
Gene Duplication , Genome, Plant , Magnoliopsida , Phylogeny , Magnoliopsida/genetics , Bayes Theorem , Evolution, MolecularABSTRACT
All flowering plants are now recognized as diploidized paleopolyploids (Jiao et al., 2011; One Thousand Plant Transcriptomes Initiative, 2019), and polyploid species comprise approximately 30% of contemporary plant species (Wood et al., 2009; Barker et al., 2016a). A major implication of these discoveries is that, to appreciate the evolution of plant diversity, we need to understand the fundamental biology of polyploids and diploidization. This need is broadly recognized by our community as there is a continued, growing interest in polyploidy as a research topic. Over the past 25 years, the sequencing and analysis of plant genomes has revolutionized our understanding of the importance of polyploid speciation to the evolution of land plants.
Subject(s)
Genome, Plant , Genomics , Polyploidy , Biological Evolution , Magnoliopsida/geneticsABSTRACT
Chimonanthus salicifolius, a member of the Calycanthaceae of magnoliids, is one of the most famous medicinal plants in Eastern China. Here, we report a chromosome-level genome assembly of C. salicifolius, comprising 820.1 Mb of genomic sequence with a contig N50 of 2.3 Mb and containing 36 651 annotated protein-coding genes. Phylogenetic analyses revealed that magnoliids were sister to the eudicots. Two rounds of ancient whole-genome duplication were inferred in the C. salicifolious genome. One is shared by Calycanthaceae after its divergence with Lauraceae, and the other is in the ancestry of Magnoliales and Laurales. Notably, long genes with >â 20 kb in length were much more prevalent in the magnoliid genomes compared with other angiosperms, which could be caused by the length expansion of introns inserted by transposon elements. Homologous genes within the flavonoid pathway for C. salicifolius were identified, and correlation of the gene expression and the contents of flavonoid metabolites revealed potential critical genes involved in flavonoids biosynthesis. This study not only provides an additional whole-genome sequence from the magnoliids, but also opens the door to functional genomic research and molecular breeding of C. salicifolius.
Subject(s)
Calycanthaceae/genetics , Evolution, Molecular , Flavonoids/biosynthesis , Genome, Plant/genetics , Magnoliaceae/genetics , Calycanthaceae/metabolism , Chromosomes, Plant/genetics , Flavonoids/genetics , Gene Duplication/genetics , Genes, Plant/genetics , Phylogeny , Sequence Alignment , Sequence Analysis, DNAABSTRACT
Demographic inference using the site frequency spectrum (SFS) is a common way to understand historical events affecting genetic variation. However, most methods for estimating demography from the SFS assume random mating within populations, precluding these types of analyses in inbred populations. To address this issue, we developed a model for the expected SFS that includes inbreeding by parameterizing individual genotypes using beta-binomial distributions. We then take the convolution of these genotype probabilities to calculate the expected frequency of biallelic variants in the population. Using simulations, we evaluated the model's ability to coestimate demography and inbreeding using one- and two-population models across a range of inbreeding levels. We also applied our method to two empirical examples, American pumas (Puma concolor) and domesticated cabbage (Brassica oleracea var. capitata), inferring models both with and without inbreeding to compare parameter estimates and model fit. Our simulations showed that we are able to accurately coestimate demographic parameters and inbreeding even for highly inbred populations (F = 0.9). In contrast, failing to include inbreeding generally resulted in inaccurate parameter estimates in simulated data and led to poor model fit in our empirical analyses. These results show that inbreeding can have a strong effect on demographic inference, a pattern that was especially noticeable for parameters involving changes in population size. Given the importance of these estimates for informing practices in conservation, agriculture, and elsewhere, our method provides an important advancement for accurately estimating the demographic histories of these species.
Subject(s)
Inbreeding , Models, Genetic , Animals , Brassica/genetics , Computer Simulation , Polymorphism, Single Nucleotide , Population Dynamics , Puma/geneticsABSTRACT
Plant genomes demonstrate significant presence/absence variation (PAV) within a species; however, the factors that lead to this variation have not been studied systematically in Brassica across diploids and polyploids. Here, we developed pangenomes of polyploid Brassica napus and its two diploid progenitor genomes B. rapa and B. oleracea to infer how PAV may differ between diploids and polyploids. Modelling of gene loss suggests that loss propensity is primarily associated with transposable elements in the diploids while in B. napus, gene loss propensity is associated with homoeologous recombination. We use these results to gain insights into the different causes of gene loss, both in diploids and following polyploidization, and pave the way for the application of machine learning methods to understanding the underlying biological and physical causes of gene presence/absence.
Subject(s)
Brassica napus , Brassica , Brassica/genetics , Brassica napus/genetics , Diploidy , Genome, Plant/genetics , PolyploidyABSTRACT
Many crops are polyploid or have a polyploid ancestry. Recent phylogenetic analyses have found that polyploidy often preceded the domestication of crop plants. One explanation for this observation is that increased genetic diversity following polyploidy may have been important during the strong artificial selection that occurs during domestication. In order to test the connection between domestication and polyploidy, we identified and examined candidate genes associated with the domestication of the diverse crop varieties of Brassica rapa. Like all 'diploid' flowering plants, B. rapa has a diploidized paleopolyploid genome and experienced many rounds of whole genome duplication (WGD). We analyzed transcriptome data of more than 100 cultivated B. rapa accessions. Using a combination of approaches, we identified > 3000 candidate genes associated with the domestication of four major B. rapa crop varieties. Consistent with our expectation, we found that the candidate genes were significantly enriched with genes derived from the Brassiceae mesohexaploidy. We also observed that paleologs were significantly more diverse than non-paleologs. Our analyses find evidence for that genetic diversity derived from ancient polyploidy played a key role in the domestication of B. rapa and provide support for its importance in the success of modern agriculture.
Subject(s)
Brassica rapa , Domestication , Brassica rapa/genetics , Genome, Plant/genetics , Phylogeny , PolyploidyABSTRACT
Understanding the mechanisms that underlie chromosome evolution could provide insights into the processes underpinning the origin, persistence and evolutionary tempo of lineages. Here, we present the first database of chromosome counts for animals (the Animal Chromosome Count database, ACC) summarizing chromosome numbers for ~15,000 species. We found remarkable a similarity in the distribution of chromosome counts between animals and flowering plants. Nevertheless, the similarity in the distribution of chromosome numbers between animals and plants is likely to be explained by different drivers. For instance, we found that while animals and flowering plants exhibit similar frequencies of speciation-related changes in chromosome number, plant speciation is more often related to changes in ploidy. By leveraging the largest data set of chromosome counts for animals, we describe a previously undocumented pattern across the Tree of Life-animals and flowering plants show remarkably similar distributions of haploid chromosome numbers.
Subject(s)
Magnoliopsida , Animals , Chromosomes , Magnoliopsida/genetics , Phylogeny , Plants/genetics , PolyploidyABSTRACT
Polyploidy or whole genome duplication (WGD) is a major contributor to genome evolution and diversity. Although polyploidy is recognized as an important component of plant evolution, it is generally considered to play a relatively minor role in animal evolution. Ancient polyploidy is found in the ancestry of some animals, especially fishes, but there is little evidence for ancient WGDs in other metazoan lineages. Here we use recently published transcriptomes and genomes from more than 150 species across the insect phylogeny to investigate whether ancient WGDs occurred during the evolution of Hexapoda, the most diverse clade of animals. Using gene age distributions and phylogenomics, we found evidence for 18 ancient WGDs and six other large-scale bursts of gene duplication during insect evolution. These bursts of gene duplication occurred in the history of lineages such as the Lepidoptera, Trichoptera, and Odonata. To further corroborate the nature of these duplications, we evaluated the pattern of gene retention from putative WGDs observed in the gene age distributions. We found a relatively strong signal of convergent gene retention across many of the putative insect WGDs. Considering the phylogenetic breadth and depth of the insect phylogeny, this observation is consistent with polyploidy as we expect dosage balance to drive the parallel retention of genes. Together with recent research on plant evolution, our hexapod results suggest that genome duplications contributed to the evolution of two of the most diverse lineages of eukaryotes on Earth.
Subject(s)
Evolution, Molecular , Gene Duplication , Genome, Insect , Insecta/genetics , Phylogeny , AnimalsABSTRACT
Polyploid speciation entails substantial and rapid postzygotic reproductive isolation of nascent species that are initially sympatric with one or both parents. Despite strong postzygotic isolation, ecological niche differentiation has long been thought to be important for polyploid success. Using biogeographic data from across vascular plants, we tested whether the climatic niches of polyploid species are more differentiated than their diploid relatives and if the climatic niches of polyploid species differentiated faster than those of related diploids. We found that polyploids are often more climatically differentiated from their diploid parents than the diploids are from each other. Consistent with this pattern, we estimated that polyploid species generally have higher rates of multivariate niche differentiation than their diploid relatives. In contrast to recent analyses, our results confirm that ecological niche differentiation is an important component of polyploid speciation and that niche differentiation is often significantly faster in polyploids.
Subject(s)
Diploidy , Polyploidy , Ecosystem , Family , Humans , PlantsABSTRACT
Although polyploidy is widespread across the plant Tree of Life, its long-term evolutionary significance is still poorly understood. Here, we examine the effects of polyploidy in explaining the large-scale evolutionary patterns within angiosperms by focusing on a single family exhibiting extensive interspecific variation in chromosome numbers. We inferred ploidy from haploid chromosome numbers for 80% of species in the most comprehensive species-level chronogram for the Brassicaceae. After evaluating a total of 94 phylogenetic models of diversification, we found that ploidy influences diversification rates across the Brassicaceae. We also found that despite diversifying at a similar rate to diploids, polyploids have played a significant role in driving present-day differences in species richness among clades. Overall, in addition to highlighting the complexity in the evolutionary consequences of polyploidy, our results suggest that rare successful polyploids persist while significantly contributing to the long-term evolution of clades. Our findings further indicate that polyploidy has played a major role in driving the long-term evolution of the Brassicaceae and highlight the potential of polyploidy in shaping present-day diversity patterns across the plant Tree of Life.
Subject(s)
Brassicaceae/genetics , Diploidy , Polyploidy , Biological Evolution , Genetic Variation , Genome, Plant , Magnoliopsida , Phylogeny , PloidiesABSTRACT
PREMISE: Whole-genome duplications (WGDs) are prevalent throughout the evolutionary history of plants. For example, dozens of WGDs have been phylogenetically localized across the order Brassicales, specifically, within the family Brassicaceae. A WGD event has also been identified in the Cleomaceae, the sister family to Brassicaceae, yet its placement, as well as that of WGDs in other families in the order, remains unclear. METHODS: Phylo-transcriptomic data were generated and used to infer a nuclear phylogeny for 74 Brassicales taxa. Genome survey sequencing was also performed on 66 of those taxa to infer a chloroplast phylogeny. These phylogenies were used to assess and confirm relationships among the major families of the Brassicales and within Brassicaceae. Multiple WGD inference methods were then used to assess the placement of WGDs on the nuclear phylogeny. RESULTS: Well-supported chloroplast and nuclear phylogenies for the Brassicales and the putative placement of the Cleomaceae-specific WGD event Th-É are presented. This work also provides evidence for previously hypothesized WGDs, including a well-supported event shared by at least two members of the Resedaceae family, and a possible event within the Capparaceae. CONCLUSIONS: Phylogenetics and the placement of WGDs within highly polyploid lineages continues to be a major challenge. This study adds to the conversation on WGD inference difficulties by demonstrating that sampling is especially important for WGD identification and phylogenetic placement. Given its economic importance and genomic resources, the Brassicales continues to be an ideal group for assessing WGD inference methods.
Subject(s)
Gene Duplication , Magnoliopsida/genetics , Evolution, Molecular , Genome , Genome, Plant/genetics , Humans , Phylogeny , PolyploidyABSTRACT
Hybridization and polyploidy followed by genome-wide diploidization had a significant impact on the diversification of land plants. The ancient At-α whole-genome duplication (WGD) preceded the diversification of crucifers (Brassicaceae). Some genera and tribes also experienced younger, mesopolyploid WGDs concealed by subsequent genome diploidization. Here we tested if multiple base chromosome numbers originated due to genome diploidization after independent mesopolyploid WGDs and how diploidization affected post-polyploid gene retention. Sixteen species representing 10 Brassicaceae tribes were analyzed by comparative chromosome painting and/or whole-transcriptome analysis of gene age distributions and phylogenetic analyses of gene duplications. Overall, we found evidence for at least 13 independent mesopolyploidies followed by different degrees of diploidization across the Brassicaceae. New mesotetraploid events were uncovered for the tribes Anastaticeae, Iberideae and Schizopetaleae, and mesohexaploid WGDs for Cochlearieae and Physarieae. In contrast, we found convergent patterns of gene retention and loss among these independent WGDs. Our combined analyses of genomic data for Brassicaceae indicate that extant chromosome number variation in many plant groups, and especially monophyletic taxa with multiple base chromosome numbers, can result from clade-specific genome duplications followed by diploidization. Our observation of parallel gene retention and loss across multiple independent WGDs provides one of the first multi-species tests of the predictability of patterns of post-polyploid genome evolution.
Subject(s)
Brassicaceae/genetics , Genome, Plant/genetics , Evolution, Molecular , Gene Duplication/genetics , Phylogeny , Plant Proteins/genetics , Plant Proteins/metabolism , PolyploidyABSTRACT
PREMISE OF THE STUDY: Polyploidy or whole-genome duplication (WGD) pervades the evolutionary history of angiosperms. Despite extensive progress in our understanding of WGD, the role of these events in promoting diversification is still not well understood. We seek to clarify the possible association between WGD and diversification rates in flowering plants. METHODS: Using a previously published phylogeny spanning all land plants (31,749 tips) and WGD events inferred from analyses of the 1000 Plants (1KP) transcriptome data, we analyzed the association of WGDs and diversification rates following numerous WGD events across the angiosperms. We used a stepwise AIC approach (MEDUSA), a Bayesian mixture model approach (BAMM), and state-dependent diversification analyses (MuSSE) to investigate patterns of diversification. Sister-clade comparisons were used to investigate species richness after WGDs. KEY RESULTS: Based on the density of 1KP taxon sampling, 106 WGDs were unambiguously placed on the angiosperm phylogeny. We identified 334-530 shifts in diversification rates. We found that 61 WGD events were tightly linked to changes in diversification rates, and state-dependent diversification analyses indicated higher speciation rates for subsequent rounds of WGD. Additionally, 70 of 99 WGD events showed an increase in species richness compared to the sister clade. CONCLUSIONS: Forty-six of the 106 WGDs analyzed appear to be closely associated with upshifts in the rate of diversification in angiosperms. Shifts in diversification do not appear more likely than random within a four-node lag phase following a WGD; however, younger WGD events are more likely to be followed by an upshift in diversification than older WGD events.
Subject(s)
Biological Evolution , Gene Duplication , Genome, Plant , Magnoliopsida/genetics , Phylogeny , Polyploidy , Bayes Theorem , Evolution, Molecular , Genetic Speciation , Genomics/methods , Models, Genetic , Species Specificity , TranscriptomeABSTRACT
Coevolutionary interactions are thought to have spurred the evolution of key innovations and driven the diversification of much of life on Earth. However, the genetic and evolutionary basis of the innovations that facilitate such interactions remains poorly understood. We examined the coevolutionary interactions between plants (Brassicales) and butterflies (Pieridae), and uncovered evidence for an escalating evolutionary arms-race. Although gradual changes in trait complexity appear to have been facilitated by allelic turnover, key innovations are associated with gene and genome duplications. Furthermore, we show that the origins of both chemical defenses and of molecular counter adaptations were associated with shifts in diversification rates during the arms-race. These findings provide an important connection between the origins of biodiversity, coevolution, and the role of gene and genome duplications as a substrate for novel traits.
Subject(s)
Brassicaceae/genetics , Butterflies/genetics , Gene Duplication , Genome, Insect/genetics , Genome, Plant/genetics , Animals , Bayes Theorem , Biodiversity , Brassicaceae/classification , Brassicaceae/parasitology , Butterflies/classification , Butterflies/physiology , Evolution, Molecular , Gene Expression , Genes, Insect/genetics , Genes, Plant/genetics , Genetic Variation , Host-Parasite Interactions/genetics , Insect Proteins/genetics , Phylogeny , Plant Proteins/genetics , Species SpecificityABSTRACT
Demographic modelling is often used with population genomic data to infer the relationships and ages among populations. However, relatively few analyses are able to validate these inferences with independent data. Here, we leverage written records that describe distinct Brassica rapa crops to corroborate demographic models of domestication. Brassica rapa crops are renowned for their outstanding morphological diversity, but the relationships and order of domestication remain unclear. We generated genomewide SNPs from 126 accessions collected globally using high-throughput transcriptome data. Analyses of more than 31,000 SNPs across the B. rapa genome revealed evidence for five distinct genetic groups and supported a European-Central Asian origin of B. rapa crops. Our results supported the traditionally recognized South Asian and East Asian B. rapa groups with evidence that pak choi, Chinese cabbage and yellow sarson are likely monophyletic groups. In contrast, the oil-type B. rapa subsp. oleifera and brown sarson were polyphyletic. We also found no evidence to support the contention that rapini is the wild type or the earliest domesticated subspecies of B. rapa. Demographic analyses suggested that B. rapa was introduced to Asia 2,400-4,100 years ago, and that Chinese cabbage originated 1,200-2,100 years ago via admixture of pak choi and European-Central Asian B. rapa. We also inferred significantly different levels of founder effect among the B. rapa subspecies. Written records from antiquity that document these crops are consistent with these inferences. The concordance between our age estimates of domestication events with historical records provides unique support for our demographic inferences.
Subject(s)
Brassica rapa/genetics , Domestication , Plant Breeding , Asia , Documentation , Founder Effect , Polymorphism, Single Nucleotide , TranscriptomeABSTRACT
Reconstructing the origin and evolution of land plants and their algal relatives is a fundamental problem in plant phylogenetics, and is essential for understanding how critical adaptations arose, including the embryo, vascular tissue, seeds, and flowers. Despite advances in molecular systematics, some hypotheses of relationships remain weakly resolved. Inferring deep phylogenies with bouts of rapid diversification can be problematic; however, genome-scale data should significantly increase the number of informative characters for analyses. Recent phylogenomic reconstructions focused on the major divergences of plants have resulted in promising but inconsistent results. One limitation is sparse taxon sampling, likely resulting from the difficulty and cost of data generation. To address this limitation, transcriptome data for 92 streptophyte taxa were generated and analyzed along with 11 published plant genome sequences. Phylogenetic reconstructions were conducted using up to 852 nuclear genes and 1,701,170 aligned sites. Sixty-nine analyses were performed to test the robustness of phylogenetic inferences to permutations of the data matrix or to phylogenetic method, including supermatrix, supertree, and coalescent-based approaches, maximum-likelihood and Bayesian methods, partitioned and unpartitioned analyses, and amino acid versus DNA alignments. Among other results, we find robust support for a sister-group relationship between land plants and one group of streptophyte green algae, the Zygnematophyceae. Strong and robust support for a clade comprising liverworts and mosses is inconsistent with a widely accepted view of early land plant evolution, and suggests that phylogenetic hypotheses used to understand the evolution of fundamental plant traits should be reevaluated.