The Aquilegia genome provides insight into adaptive radiation and reveals an extraordinarily polymorphic chromosome with a unique history
- Austrian Academy of Sciences, Austria
- University of California, Santa Barbara, United States
- Masaryk University, Czech Republic
- Department of Energy, United States
- Centre of the Region Haná for Biotechnological and Agricultural Research, Czech Republic
- Harvard University, United States
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/
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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.
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.
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The Aquilegia genome provides insight into adaptive radiation and reveals an extraordinarily polymorphic chromosome with a unique history
eLife 7:e36426.
https://doi.org/10.7554/eLife.36426
Further reading
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Gene regulation is essential for life and controlled by regulatory DNA. Mutations can modify the activity of regulatory DNA, and also create new regulatory DNA, a process called regulatory emergence. Non-regulatory and regulatory DNA contain motifs to which transcription factors may bind. In prokaryotes, gene expression requires a stretch of DNA called a promoter, which contains two motifs called –10 and –35 boxes. However, these motifs may occur in both promoters and non-promoter DNA in multiple copies. They have been implicated in some studies to improve promoter activity, and in others to repress it. Here, we ask whether the presence of such motifs in different genetic sequences influences promoter evolution and emergence. To understand whether and how promoter motifs influence promoter emergence and evolution, we start from 50 ‘promoter islands’, DNA sequences enriched with –10 and –35 boxes. We mutagenize these starting ‘parent’ sequences, and measure gene expression driven by 240,000 of the resulting mutants. We find that the probability that mutations create an active promoter varies more than 200-fold, and is not correlated with the number of promoter motifs. For parent sequences without promoter activity, mutations created over 1500 new –10 and –35 boxes at unique positions in the library, but only ~0.3% of these resulted in de-novo promoter activity. Only ~13% of all –10 and –35 boxes contribute to de-novo promoter activity. For parent sequences with promoter activity, mutations created new –10 and –35 boxes in 11 specific positions that partially overlap with preexisting ones to modulate expression. We also find that –10 and –35 boxes do not repress promoter activity. Overall, our work demonstrates how promoter motifs influence promoter emergence and evolution. It has implications for predicting and understanding regulatory evolution, de novo genes, and phenotypic evolution.
