A Phylogenomic Assessment of Ancient Polyploidy and Genome Evolution Across the Poales

Comparisons of flowering plant genomes reveal multiple rounds of ancient polyploidy characterized by large intra-genomic syntenic blocks. Three such whole genome duplication (WGD) events, designated as rho (ρ), sigma (σ), and tau (τ), have been identified in the genomes of cereal grasses. Precise dating of these WGD events is necessary to investigate how they have influenced diversification rates, evolutionary innovations, and genomic characteristics such as the GC profile of protein coding sequences. The timing of these events has remained uncertain due to the paucity of monocot genome sequence data outside the grass family (Poaceae). Phylogenomic analysis of protein coding genes from sequenced genomes and transcriptome assemblies from 35 species, including representatives of all families within the Poales, has resolved the timing ofrho and sigma relative to speciation events and placed tau prior to divergence of Asparagales and the commelinids but after divergence with eudicots. Examination of gene family phylogenies indicates that rhooccurred just prior to the diversification of Poaceae and sigma occurred before early diversification of Poales lineages but after the Poales-commelinid split. Additional lineage specific WGD events were identified on the basis of the transcriptome data. Gene families exhibiting high GC content are underrepresented among those with duplicate genes that persisted following these genome duplications. However, genome duplications had little overall influence on lineage-specific changes in the GC content of coding genes. Improved resolution of the timing of WGD events in monocot history provides evidence for the influence of polyploidization on functional evolution and species diversification

Practical considerations for plant phylogenomics

Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/143756/1/aps31038_am.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/143756/2/aps31038.pd

Strongly asymmetric hybridization barriers shape the origin of a new polyploid species and its hybrid ancestor

PREMISE OF THE STUDY:Hybridization between diploids and tetraploids can lead to new allopolyploid species, often via a triploid intermediate. Viable triploids are often produced asymmetrically, with greater success observed for “maternal-excess” crosses where the mother has a higher ploidy than the father. Here we investigated the evolutionary origins ofMimulus peregrinus, an allohexaploid recently derived from the triploidM. ×robertsii, to determine whether reproductive asymmetry has shaped the formation of this new species.  METHODS:We used reciprocal crosses between the diploid (M. guttatus) and tetraploid (M. luteus) progenitors to determine the viability of triploidM. ×robertsiihybrids resulting from paternal- vs. maternal-excess crosses. To investigate whether experimental results predict patterns seen in the field, we performed parentage analyses comparing natural populations ofM. peregrinusto its diploid, tetraploid, and triploid progenitors. Organellar sequences obtained from pre-existing genomic data, supplemented with additional genotyping was used to establish the maternal ancestry of multipleM. peregrinusandM. ×robertsiipopulations.  KEY RESULTS:We found strong evidence for asymmetric origins ofM. peregrinus, but opposite to the common pattern, with paternal-excess crosses significantly more successful than maternal-excess crosses. These results successfully predicted hybrid formation in nature: 111 of 114M. ×robertsiiindividuals, and 27 of 27M. peregrinus, had anM. guttatusmaternal haplotype.  CONCLUSION:This study, which includes the firstMimuluschloroplast genome assembly, demonstrates the utility of parentage analysis through genome skimming. We highlight the benefits of complementing genomic analyses with experimental approaches to understand asymmetry in allopolyploid speciation

Ancient Polyploidy and Genome Evolution in Palms

Mechanisms of genome evolution are fundamental to our understanding of adaptation and the generation and maintenance of biodiversity, yet genome dynamics are still poorly characterized in many clades. Strong correlations between variation in genomic attributes and species diversity across the plant tree of life suggest that polyploidy or other mechanisms of genome size change confer selective advantages due to the introduction of genomic novelty. Palms (order Arecales, family Arecaceae) are diverse, widespread, and dominant in tropical ecosystems, yet little is known about genome evolution in this ecologically and economically important clade. Here, we take a phylogenetic comparative approach to investigate palm genome dynamics using genomic and transcriptomic data in combination with a recent, densely sampled, phylogenetic tree. We find conclusive evidence of a paleopolyploid event shared by the ancestor of palms but not with the sister clade, Dasypogonales. We find evidence of incremental chromosome number change in the palms as opposed to one of recurrent polyploidy. We find strong phylogenetic signal in chromosome number, but no signal in genome size, and further no correlation between the two when correcting for phylogenetic relationships. Palms thus add to a growing number of diverse, ecologically successful clades with evidence of whole-genome duplication, sister to a species-poor clade with no evidence of such an event. Disentangling the causes of genome size variation in palms moves us closer to understanding the genomic conditions facilitating adaptive radiation and ecological dominance in an evolutionarily successful, emblematic tropical clade

The draft genome of the C\u3csub\u3e3\u3c/sub\u3e panicoid grass species \u3ci\u3eDichanthelium oligosanthes\u3c/i\u3e

Background: Comparisons between C3 and C4 grasses often utilize C3 species from the subfamilies Ehrhartoideae or Pooideae and C4 species from the subfamily Panicoideae, two clades that diverged over 50 million years ago. The divergence of the C3 panicoid grass Dichanthelium oligosanthes from the independent C4 lineages represented by Setaria viridis and Sorghum bicolor occurred approximately 15 million years ago, which is significantly more recent than members of the Bambusoideae, Ehrhartoideae, and Pooideae subfamilies. D. oligosanthes is ideally placed within the panicoid clade for comparative studies of C3 and C4 grasses. Results: We report the assembly of the nuclear and chloroplast genomes of D. oligosanthes, from high-throughput short read sequencing data and a comparative transcriptomics analysis of the developing leaf of D. oligosanthes, S. viridis, and S. bicolor. Physiological and anatomical characterizations verified that D. oligosanthes utilizes the C3 pathway for carbon fixation and lacks Kranz anatomy. Expression profiles of transcription factors along developing leaves of D. oligosanthes and S. viridis were compared with previously published data from S. bicolor, Zea mays, and Oryza sativa to identify a small suite of transcription factors that likely acquired functions specifically related to C4 photosynthesis. Conclusions: The phylogenetic location of D. oligosanthes makes it an ideal C3 plant for comparative analysis of C4 evolution in the panicoid grasses. This genome will not only provide a better C3 species for comparisons with C4 panicoid grasses, but also highlights the power of using high-throughput sequencing to address questions in evolutionary biology

Origin and evolution of the octoploid strawberry genome.

Cultivated strawberry emerged from the hybridization of two wild octoploid species, both descendants from the merger of four diploid progenitor species into a single nucleus more than 1 million years ago. Here we report a near-complete chromosome-scale assembly for cultivated octoploid strawberry (Fragaria × ananassa) and uncovered the origin and evolutionary processes that shaped this complex allopolyploid. We identified the extant relatives of each diploid progenitor species and provide support for the North American origin of octoploid strawberry. We examined the dynamics among the four subgenomes in octoploid strawberry and uncovered the presence of a single dominant subgenome with significantly greater gene content, gene expression abundance, and biased exchanges between homoeologous chromosomes, as compared with the other subgenomes. Pathway analysis showed that certain metabolomic and disease-resistance traits are largely controlled by the dominant subgenome. These findings and the reference genome should serve as a powerful platform for future evolutionary studies and enable molecular breeding in strawberry

A genome triplication associated with early diversification of the core eudicots

Background: Although it is agreed that a major polyploidy event, gamma, occurred within the eudicots, the phylogenetic placement of the event remains unclear. Results: To determine when this polyploidization occurred relative to speciation events in angiosperm history, we employed a phylogenomic approach to investigate the timing of gene set duplications located on syntenic gamma blocks. We populated 769 putative gene families with large sets of homologs obtained from public transcriptomes of basal angiosperms, magnoliids, asterids, and more than 91.8 gigabases of new next-generation transcriptome sequences of non-grass monocots and basal eudicots. The overwhelming majority (95%) of well-resolved gamma duplications was placed before the separation of rosids and asterids and after the split of monocots and eudicots, providing strong evidence that the gamma polyploidy event occurred early in eudicot evolution. Further, the majority of gene duplications was placed after the divergence of the Ranunculales and core eudicots, indicating that the gamma appears to be restricted to core eudicots. Molecular dating estimates indicate that the duplication events were intensely concentrated around 117 million years ago. Conclusions: The rapid radiation of core eudicot lineages that gave rise to nearly 75% of angiosperm species appears to have occurred coincidentally or shortly following the gamma triplication event. Reconciliation of gene trees with a species phylogeny can elucidate the timing of major events in genome evolution, even when genome sequences are only available for a subset of species represented in the gene trees. Comprehensive transcriptome datasets are valuable complements to genome sequences for high-resolution phylogenomic analysis

Phylogenomic analysis of transcriptome data elucidates co-occurrence of a paleopolyploid event and the origin of bimodal karyotypes in Agavoideae (Asparagaceae)

Premise of the study: The stability of the bimodal karyotype found in Agave and closely related species has long interested botanists. The origin of the bimodal karyotype has been attributed to allopolyploidy, but this hypothesis has not been tested. Next-generation transcriptome sequence data were used to test whether a paleopolyploid event occurred on the same branch of the Agavoideae phylogenetic tree as the origin of the Yucca-Agave bimodal karyotype. Methods: Illumina RNA-seq data were generated for phylogenetically strategic species in Agavoideae. Paleopolyploidy was inferred in analyses of frequency plots for synonymous substitutions per synonymous site (K-s) between Hosta, Agave, and Chlorophytum paralogous and orthologous gene pairs. Phylogenies of gene families including paralogous genes for these species and outgroup species were estimated to place inferred paleopolyploid events on a species tree. Key results: K-s frequency plots suggested paleopolyploid events in the history of the genera Agave, Hosta, and Chlorophytum. Phylogenetic analyses of gene families estimated from transcriptome data revealed two polyploid events: one predating the last common ancestor of Agave and Hosta and one within the lineage leading to Chlorophytum. Conclusions: We found that polyploidy and the origin of the Yucca-Agave bimodal karyotype co-occur on the same lineage consistent with the hypothesis that the bimodal karyotype is a consequence of allopolyploidy. We discuss this and alternative mechanisms for the formation of the Yucca-Agave bimodal karyotype. More generally, we illustrate how the use of next-generation sequencing technology is a cost-efficient means for assessing genome evolution in nonmodel species

Single-molecule sequencing and optical mapping yields an improved genome of woodland strawberry (Fragaria vesca) with chromosome-scale contiguity

Background: Although draft genomes are available for most agronomically important plant species, the majority are incomplete, highly fragmented, and often riddled with assembly and scaffolding errors. These assembly issues hinder advances in tool development for functional genomics and systems biology. Findings: Here we utilized a robust, cost-effective approach to produce high-quality reference genomes. We report a near-complete genome of diploid woodland strawberry (Fragaria vesca) using single-molecule real-time sequencing from Pacific Biosciences (PacBio). This assembly has a contig N50 length of similar to 7.9 million base pairs (Mb), representing a similar to 300-fold improvement of the previous version. The vast majority (>99.8%) of the assembly was anchored to 7 pseudomolecules using 2 sets of optical maps from Bionano Genomics. We obtained similar to 24.96 Mb of sequence not present in the previous version of the F. vesca genome and produced an improved annotation that includes 1496 new genes. Comparative syntenic analyses uncovered numerous, large-scale scaffolding errors present in each chromosome in the previously published version of the F. vesca genome. Conclusions: Our results highlight the need to improve existing short-read based reference genomes. Furthermore, we demonstrate how genome quality impacts commonly used analyses for addressing both fundamental and applied biological questions.Peer reviewe

Single-molecule sequencing and optical mapping yields an improved genome of woodland strawberry (\u3ci\u3eFragaria vesca\u3c/i\u3e) with chromosome-scale contiguity

Background: Although draft genomes are available for most agronomically important plant species, the majority are incomplete, highly fragmented, and often riddled with assembly and scaffolding errors. These assembly issues hinder advances in tool development for functional genomics and systems biology. Findings: Here we utilized a robust, cost-effective approach to produce high-quality reference genomes.We report a near-complete genome of diploid woodland strawberry (Fragaria vesca) using single-molecule real-time sequencing from Pacific Biosciences (PacBio). This assembly has a contig N50 length of ~7.9 million base pairs (Mb), representing a ~300-fold improvement of the previous version. The vast majority (\u3e99.8%) of the assembly was anchored to 7 pseudomolecules using 2 sets of optical maps from Bionano Genomics. We obtained ~24.96 Mb of sequence not present in the previous version of the F. vesca genome and produced an improved annotation that includes 1496 new genes. Comparative syntenic analyses uncovered numerous, large-scale scaffolding errors present in each chromosome in the previously published version of the F. vesca genome. Conclusions: Our results highlight the need to improve existing short-read based reference genomes. Furthermore, we demonstrate how genome quality impacts commonly used analyses for addressing both fundamental and applied biological questions