Title: Phylotranscriptomics Illuminates the Placement of Whole Genome Duplications and Gene Retention in Ferns
Ferns are the second largest clade of vascular plants with over 10,000 species, yet the generation of genomic resources for the group has lagged behind other major clades of plants. Transcriptomic data have proven to be a powerful tool to assess phylogenetic relationships, using thousands of markers that are largely conserved across the genome, and without the need to sequence entire genomes. We assembled the largest nuclear phylogenetic dataset for ferns to date, including 2884 single-copy nuclear loci from 247 transcriptomes (242 ferns, five outgroups), and investigated phylogenetic relationships across the fern tree, the placement of whole genome duplications (WGDs), and gene retention patterns following WGDs. We generated a well-supported phylogeny of ferns and identified several regions of the fern phylogeny that demonstrate high levels of gene tree–species tree conflict, which largely correspond to areas of the phylogeny that have been difficult to resolve. Using a combination of approaches, we identified 27 WGDs across the phylogeny, including 18 large-scale events (involving more than one sampled taxon) and nine small-scale events (involving only one sampled taxon). Most inferred WGDs occur within single lineages (e.g., orders, families) rather than on the backbone of the phylogeny, although two inferred events are shared by leptosporangiate ferns (excluding Osmundales) and Polypodiales (excluding Lindsaeineae and Saccolomatineae), clades which correspond to the majority of fern diversity. We further examined how retained duplicates following WGDs compared across independent events and found that functions of retained genes were largely convergent, with processes involved in binding, responses to stimuli, and certain organelles over-represented in paralogs while processes involved in transport, organelles derived from endosymbiotic events, and signaling were under-represented. To date, our study is the most comprehensive investigation of the nuclear fern phylogeny, though several avenues for future research remain unexplored. more »« less
Lee, Aaron K.; Gilman, Ian S.; Srivastav, Mansa; Lerner, Ariel D.; Donoghue, Michael J.; Clement, Wendy L.(
, American Journal of Botany)
Premise
Phylogenetic relationships within major angiosperm clades are increasingly well resolved, but largely informed by plastid data. Areas of poor resolution persist within the Dipsacales, including placement ofHeptacodiumandZabelia, and relationships within the Caprifolieae and Linnaeeae, hindering our interpretation of morphological evolution. Here, we sampled a significant number of nuclear loci using a Hyb‐Seq approach and used these data to infer the Dipsacales phylogeny and estimate divergence times.
Methods
Sampling all major clades within the Dipsacales, we applied the Angiosperms353 probe set to 96 species. Data were filtered based on locus completeness and taxon recovery per locus, and trees were inferred using RAxML and ASTRAL. Plastid loci were assembled from off‐target reads, and 10 fossils were used to calibrate dated trees.
Results
Varying numbers of targeted loci and off‐target plastomes were recovered from most taxa. Nuclear and plastid data confidently placeHeptacodiumwith Caprifolieae, implying homoplasy in calyx morphology, ovary development, and fruit type. Placement ofZabelia, and relationships within the Caprifolieae and Linnaeeae, remain uncertain. Dipsacales diversification began earlier than suggested by previous angiosperm‐wide dating analyses, but many major splitting events date to the Eocene.
Conclusions
The Angiosperms353 probe set facilitated the assembly of a large, single‐copy nuclear dataset for the Dipsacales. Nevertheless, many relationships remain unresolved, and resolution was poor for woody clades with low rates of molecular evolution. We favor expanding the Angiosperms353 probe set to include more variable loci and loci of special interest, such as developmental genes, within particular clades.
Foley, Nicole M.; Mason, Victor C.; Harris, Andrew J.; Bredemeyer, Kevin R.; Damas, Joana; Lewin, Harris A.; Eizirik, Eduardo; Gatesy, John; Karlsson, Elinor K.; Lindblad-Toh, Kerstin; et al(
, Science)
INTRODUCTION Resolving the role that different environmental forces may have played in the apparent explosive diversification of modern placental mammals is crucial to understanding the evolutionary context of their living and extinct morphological and genomic diversity. RATIONALE Limited access to whole-genome sequence alignments that sample living mammalian biodiversity has hampered phylogenomic inference, which until now has been limited to relatively small, highly constrained sequence matrices often representing <2% of a typical mammalian genome. To eliminate this sampling bias, we used an alignment of 241 whole genomes to comprehensively identify and rigorously analyze noncoding, neutrally evolving sequence variation in coalescent and concatenation-based phylogenetic frameworks. These analyses were followed by validation with multiple classes of phylogenetically informative structural variation. This approach enabled the generation of a robust time tree for placental mammals that evaluated age variation across hundreds of genomic loci that are not restricted by protein coding annotations. RESULTS Coalescent and concatenation phylogenies inferred from multiple treatments of the data were highly congruent, including support for higher-level taxonomic groupings that unite primates+colugos with treeshrews (Euarchonta), bats+cetartiodactyls+perissodactyls+carnivorans+pangolins (Scrotifera), all scrotiferans excluding bats (Fereuungulata), and carnivorans+pangolins with perissodactyls (Zooamata). However, because these approaches infer a single best tree, they mask signatures of phylogenetic conflict that result from incomplete lineage sorting and historical hybridization. Accordingly, we also inferred phylogenies from thousands of noncoding loci distributed across chromosomes with historically contrasting recombination rates. Throughout the radiation of modern orders (such as rodents, primates, bats, and carnivores), we observed notable differences between locus trees inferred from the autosomes and the X chromosome, a pattern typical of speciation with gene flow. We show that in many cases, previously controversial phylogenetic relationships can be reconciled by examining the distribution of conflicting phylogenetic signals along chromosomes with variable historical recombination rates. Lineage divergence time estimates were notably uniform across genomic loci and robust to extensive sensitivity analyses in which the underlying data, fossil constraints, and clock models were varied. The earliest branching events in the placental phylogeny coincide with the breakup of continental landmasses and rising sea levels in the Late Cretaceous. This signature of allopatric speciation is congruent with the low genomic conflict inferred for most superordinal relationships. By contrast, we observed a second pulse of diversification immediately after the Cretaceous-Paleogene (K-Pg) extinction event superimposed on an episode of rapid land emergence. Greater geographic continuity coupled with tumultuous climatic changes and increased ecological landscape at this time provided enhanced opportunities for mammalian diversification, as depicted in the fossil record. These observations dovetail with increased phylogenetic conflict observed within clades that diversified in the Cenozoic. CONCLUSION Our genome-wide analysis of multiple classes of sequence variation provides the most comprehensive assessment of placental mammal phylogeny, resolves controversial relationships, and clarifies the timing of mammalian diversification. We propose that the combination of Cretaceous continental fragmentation and lineage isolation, followed by the direct and indirect effects of the K-Pg extinction at a time of rapid land emergence, synergistically contributed to the accelerated diversification rate of placental mammals during the early Cenozoic. The timing of placental mammal evolution. Superordinal mammalian diversification took place in the Cretaceous during periods of continental fragmentation and sea level rise with little phylogenomic discordance (pie charts: left, autosomes; right, X chromosome), which is consistent with allopatric speciation. By contrast, the Paleogene hosted intraordinal diversification in the aftermath of the K-Pg mass extinction event, when clades exhibited higher phylogenomic discordance consistent with speciation with gene flow and incomplete lineage sorting.
Bell, David; Lin, Qianshi; Gerelle, Wesley K.; Joya, Steve; Chang, Ying; Taylor, Z. Nathan; Rothfels, Carl J.; Larsson, Anders; Villarreal, Juan Carlos; Li, Fay‐Wei; et al(
, American Journal of Botany)
Premise
Phylogenetic trees of bryophytes provide important evolutionary context for land plants. However, published inferences of overall embryophyte relationships vary considerably. We performed phylogenomic analyses of bryophytes and relatives using both mitochondrial and plastid gene sets, and investigated bryophyte plastome evolution.
Methods
We employed diverse likelihood‐based analyses to infer large‐scale bryophyte phylogeny for mitochondrial and plastid data sets. We tested for changes in purifying selection in plastid genes of a mycoheterotrophic liverwort (Aneura mirabilis) and a putatively mycoheterotrophic moss (Buxbaumia), and compared 15 bryophyte plastomes for major structural rearrangements.
Results
Overall land‐plant relationships conflict across analyses, generally weakly. However, an underlying (unrooted) four‐taxon tree is consistent across most analyses and published studies. Despite gene coverage patchiness, relationships within mosses, liverworts, and hornworts are largely congruent with previous studies, with plastid results generally better supported. Exclusion ofRNAedit sites restores cases of unexpected non‐monophyly to monophyly forTakakiaand two hornwort genera. Relaxed purifying selection affects multiple plastid genes in mycoheterotrophicAneurabut notBuxbaumia. Plastid genome structure is nearly invariant across bryophytes, but thetufA locus, presumed lost in embryophytes, is unexpectedly retained in several mosses.
Conclusions
A common unrooted tree underlies embryophyte phylogeny, [(liverworts, mosses), (hornworts, vascular plants)]; rooting inconsistency across studies likely reflects substantial distance to algal outgroups. Analyses combining genomic and transcriptomic data may be misled locally for heavilyRNA‐edited taxa. TheBuxbaumiaplastome lacks hallmarks of relaxed selection found in mycoheterotrophicAneura. Autotrophic bryophyte plastomes, includingBuxbaumia, hardly vary in overall structure.
Abstract Background and Aims Cycads are regarded as an ancient lineage of living seed plants, and hold important clues to understand the early evolutionary trends of seed plants. The molecular phylogeny and spatio-temporal diversification of one of the species-rich genera of cycads, Macrozamia, have not been well reconstructed. Methods We analysed a transcriptome dataset of 4740 single-copy nuclear genes (SCGs) of 39 Macrozamia species and two outgroup taxa. Based on concatenated (maximum parsimony, maximum likelihood) and multispecies coalescent analyses, we first establish a well-resolved phylogenetic tree of Macrozamia. To identify cyto-nuclear incongruence, the plastid protein coding genes (PCGs) from transcriptome data are extracted using the software HybPiper. Furthermore, we explore the biogeographical history of the genus and shed light on the pattern of floristic exchange between three distinct areas of Australia. Six key diagnostic characters are traced on the phylogenetic framework using two comparative methods, and infra-generic classification is investigated. Key Results The tree topologies of concatenated and multi-species coalescent analyses of SCGs are mostly congruent with a few conflicting nodes, while those from plastid PCGs show poorly supported relationships. The genus contains three major clades that correspond to their distinct distributional areas in Australia. The crown group of Macrozamia is estimated to around 11.80 Ma, with a major expansion in the last 5–6 Myr. Six morphological characters show homoplasy, and the traditional phenetic sectional division of the genus is inconsistent with this current phylogeny. Conclusions This first detailed phylogenetic investigation of Macrozamia demonstrates promising prospects of SCGs in resolving phylogenetic relationships within cycads. Our study suggests that Macrozamia, once widely distributed in Australia, underwent major extinctions because of fluctuating climatic conditions such as cooling and mesic biome disappearance in the past. The current close placement of morphologically distinct species in the phylogenetic tree may be related to neotenic events that occurred in the genus.
Abstract Phylogenomic data from a rapidly increasing number of studies provide new evidence for resolving relationships in recently radiated clades, but they also pose new challenges for inferring evolutionary histories. Most existing methods for reconstructing phylogenetic hypotheses rely solely on algorithms that only consider incomplete lineage sorting (ILS) as a cause of intra- or intergenomic discordance. Here, we utilize a variety of methods, including those to infer phylogenetic networks, to account for both ILS and introgression as a cause for nuclear and cytoplasmic-nuclear discordance using phylogenomic data from the recently radiated flowering plant genus Polemonium (Polemoniaceae), an ecologically diverse genus in Western North America with known and suspected gene flow between species. We find evidence for widespread discordance among nuclear loci that can be explained by both ILS and reticulate evolution in the evolutionary history of Polemonium. Furthermore, the histories of organellar genomes show strong discordance with the inferred species tree from the nuclear genome. Discordance between the nuclear and plastid genome is not completely explained by ILS, and only one case of discordance is explained by detected introgression events. Our results suggest that multiple processes have been involved in the evolutionary history of Polemonium and that the plastid genome does not accurately reflect species relationships. We discuss several potential causes for this cytoplasmic-nuclear discordance, which emerging evidence suggests is more widespread across the Tree of Life than previously thought. [Cyto-nuclear discordance, genomic discordance, phylogenetic networks, plastid capture, Polemoniaceae, Polemonium, reticulations.]
Pelosi, Jessie A., Kim, Emily H., Barbazuk, W. Brad, and Sessa, Emily B. Phylotranscriptomics Illuminates the Placement of Whole Genome Duplications and Gene Retention in Ferns. Retrieved from https://par.nsf.gov/biblio/10443654. Frontiers in Plant Science 13. Web. doi:10.3389/fpls.2022.882441.
Pelosi, Jessie A., Kim, Emily H., Barbazuk, W. Brad, & Sessa, Emily B. Phylotranscriptomics Illuminates the Placement of Whole Genome Duplications and Gene Retention in Ferns. Frontiers in Plant Science, 13 (). Retrieved from https://par.nsf.gov/biblio/10443654. https://doi.org/10.3389/fpls.2022.882441
Pelosi, Jessie A., Kim, Emily H., Barbazuk, W. Brad, and Sessa, Emily B.
"Phylotranscriptomics Illuminates the Placement of Whole Genome Duplications and Gene Retention in Ferns". Frontiers in Plant Science 13 (). Country unknown/Code not available. https://doi.org/10.3389/fpls.2022.882441.https://par.nsf.gov/biblio/10443654.
@article{osti_10443654,
place = {Country unknown/Code not available},
title = {Phylotranscriptomics Illuminates the Placement of Whole Genome Duplications and Gene Retention in Ferns},
url = {https://par.nsf.gov/biblio/10443654},
DOI = {10.3389/fpls.2022.882441},
abstractNote = {Ferns are the second largest clade of vascular plants with over 10,000 species, yet the generation of genomic resources for the group has lagged behind other major clades of plants. Transcriptomic data have proven to be a powerful tool to assess phylogenetic relationships, using thousands of markers that are largely conserved across the genome, and without the need to sequence entire genomes. We assembled the largest nuclear phylogenetic dataset for ferns to date, including 2884 single-copy nuclear loci from 247 transcriptomes (242 ferns, five outgroups), and investigated phylogenetic relationships across the fern tree, the placement of whole genome duplications (WGDs), and gene retention patterns following WGDs. We generated a well-supported phylogeny of ferns and identified several regions of the fern phylogeny that demonstrate high levels of gene tree–species tree conflict, which largely correspond to areas of the phylogeny that have been difficult to resolve. Using a combination of approaches, we identified 27 WGDs across the phylogeny, including 18 large-scale events (involving more than one sampled taxon) and nine small-scale events (involving only one sampled taxon). Most inferred WGDs occur within single lineages (e.g., orders, families) rather than on the backbone of the phylogeny, although two inferred events are shared by leptosporangiate ferns (excluding Osmundales) and Polypodiales (excluding Lindsaeineae and Saccolomatineae), clades which correspond to the majority of fern diversity. We further examined how retained duplicates following WGDs compared across independent events and found that functions of retained genes were largely convergent, with processes involved in binding, responses to stimuli, and certain organelles over-represented in paralogs while processes involved in transport, organelles derived from endosymbiotic events, and signaling were under-represented. To date, our study is the most comprehensive investigation of the nuclear fern phylogeny, though several avenues for future research remain unexplored.},
journal = {Frontiers in Plant Science},
volume = {13},
author = {Pelosi, Jessie A. and Kim, Emily H. and Barbazuk, W. Brad and Sessa, Emily B.},
}
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