The Aquilegia genome provides insight into adaptive radiation and reveals an extraordinarily polymorphic chromosome with a unique history
Abstract
The columbine genus Aquilegia is a classic example of an adaptive radiation, involving a wide variety of pollinators and habitats. Here we present the genome assembly of A. coerulea 'Goldsmith', complemented by high-coverage sequencing data from 10 wild species covering the world-wide distribution. Our analyses reveal extensive allele sharing among species, and demonstrate that introgression and selection played a role in the Aquilegia radiation. We also present the remarkable discovery that the evolutionary history of an entire chromosome differs from that of the rest of the genome - a phenomenon which we do not fully understand, but which highlights the need to consider chromosomes in an evolutionary context.
Data availability
Species resequencingA. barnebyi (SRR7965809), A. aurea (SRR405095), A. vulgaris (SRR404349), A. sibirica (SRR405090), A. formosa (SRR408554), A. japonica (SRR413499), A. oxysepala (SRR413921), A. longissima (SRR7965810), A. chrysantha (SRR408559), A. pubescens (SRR7943924) are available in the Short Read Archive(https://www.ncbi.nlm.nih.gov/sra).Whole genome Aquilegia coerulea 'Goldsmith'Sanger sequences used for genome assembly are available in the NCBI Trace Archive (https://www.ncbi.nlm.nih.gov/Traces).Aquilegia coerulea 'Goldsmith' ESTsAvailable in the NCBI Short Read Archive (SRR505574-SRR505578)Aquilegia formosa 412 ESTsAvailable in the NCBI dbEST (https://www.ncbi.nlm.nih.gov/dbEST/)Aquilegia coerulea 'Goldsmith' X Aquilegia chrysantha mapping populationAvailable in the NCBI Short Read Archive (SRR8000449-SRR8000976)Aquilegia formosa x Aquilegia pubescens mapping populationAvailable in the NCBI Short Read Archive (Bioproject PRJNA489508).grandparentspub.1 (SRR7943925), pub.2 (SRR7943924), form.1 (SRR7790646), form.2 (SRR408554)F1sF1.1 (SRR7943926), F1.2 (SRR7943927)F2sSRR7814612-SRR7814614, SRR7814616-SRR7814619, SRR7814622, SRR7814624-SRR7814686, SRR7826362- SRR7826624RNAseqAvailable in the NCBI Short Read Archive: see Supplementary Table 5 for more details.Other filesA vcf containing biallelic SNPs called in all ten Aquilegia species and Semiaquilegia (AQ.Semi.all.biallelic.SNPs.vcf.gz) and text files of genomic positions passing filtration (AQ.only.kept.positions.txt.gz and AQ.Semi.kept.positions.txt.gz) are available for download at Dryad (doi:10.5061/dryad.j4j12v0).URLsThe A. coerulea 'Goldsmith' v3.1 genome release is available at: https://phytozome.jgi.doe.gov/
-
Data from: The Aquilegi a genome provides insight into adaptive radiation and reveals an extraordinarily polymorphic chromosome with a unique historyAvailable at Dryad Digital Repository under a CC0 Public Domain Dedication.
Article and author information
Author details
Funding
Czech Science Foundation (P501/12/G090)
- Martin A Lysak
CEITEC 2020 (LQ1601)
- Martin A Lysak
National Program of Sustainability I (LO1204)
- Miroslava Karafiátová
Austrian Science Funds (FWF DK W1225-B20)
- Gökçe Aköz
University of California, Santa Barbara (Harvey L. Karp Discovery Award)
- Evangeline S Ballerini
National Institutes of Health (Ruth L. Kirschstein National Research Service Award F32GM103154)
- Evangeline S Ballerini
National Science Foundation (IOS 1456317)
- Scott A Hodges
National Science Foundation (DEB 1311390)
- Nathan J Derieg
- Scott A Hodges
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Gil McVean, Oxford University, United Kingdom
Publication history
- Received: March 6, 2018
- Accepted: September 17, 2018
- Accepted Manuscript published: October 16, 2018 (version 1)
- Version of Record published: November 26, 2018 (version 2)
Copyright
© 2018, Filiault et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 5,628
- Page views
-
- 902
- Downloads
-
- 56
- Citations
Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Chromosomes and Gene Expression
- Structural Biology and Molecular Biophysics
One-dimensional (1D) target search is a well-characterized phenomenon for many DNA-binding proteins but is poorly understood for chromatin remodelers. Herein, we characterize the 1D scanning properties of SWR1, a conserved yeast chromatin remodeler that performs histone exchange on +1 nucleosomes adjacent to a nucleosome-depleted region (NDR) at gene promoters. We demonstrate that SWR1 has a kinetic binding preference for DNA of NDR length as opposed to gene-body linker length DNA. Using single and dual color single-particle tracking on DNA stretched with optical tweezers, we directly observe SWR1 diffusion on DNA. We found that various factors impact SWR1 scanning, including ATP which promotes diffusion through nucleotide binding rather than ATP hydrolysis. A DNA-binding subunit, Swc2, plays an important role in the overall diffusive behavior of the complex, as the subunit in isolation retains similar, although faster, scanning properties as the whole remodeler. ATP-bound SWR1 slides until it encounters a protein roadblock, of which we tested dCas9 and nucleosomes. The median diffusion coefficient, 0.024 μm2/s, in the regime of helical sliding, would mediate rapid encounter of NDR-flanking nucleosomes at length scales found in cellular chromatin.
-
- Cancer Biology
- Chromosomes and Gene Expression
The transformation of normal to malignant cells is accompanied by substantial changes in gene expression programs through diverse mechanisms. Here, we examined the changes in the landscape of transcription start sites and alternative promoter (AP) usage and their impact on the translatome in TCL1-driven chronic lymphocytic leukemia (CLL). Our findings revealed a marked elevation of APs in CLL B cells from Eµ-Tcl1 transgenic mice, which are particularly enriched with intra-genic promoters that generate N-terminally truncated or modified proteins. Intra-genic promoter activation is mediated by (1) loss of function of ‘closed chromatin’ epigenetic regulators due to the generation of inactive N-terminally modified isoforms or reduced expression; (2) upregulation of transcription factors, including c-Myc, targeting the intra-genic promoters and their associated enhancers. Exogenous expression of Tcl1 in MEFs is sufficient to induce intra-genic promoters of epigenetic regulators and promote c-Myc expression. We further found a dramatic translation downregulation of transcripts bearing CNY cap-proximal trinucleotides, reminiscent of cells undergoing metabolic stress. These findings uncovered the role of Tcl1 oncogenic function in altering promoter usage and mRNA translation in leukemogenesis.