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Gradual Evolution of Allopolyploidy in Arabidopsis Suecica ARTICLES https://doi.org/10.1038/s41559-021-01525-w Gradual evolution of allopolyploidy in Arabidopsis suecica Robin Burns 1, Terezie Mandáková2, Joanna Gunis 1, Luz Mayela Soto-Jiménez 1, Chang Liu3, Martin A. Lysak 2, Polina Yu. Novikova 4,5 ✉ and Magnus Nordborg 1 ✉ Most diploid organisms have polyploid ancestors. The evolutionary process of polyploidization is poorly understood but has frequently been conjectured to involve some form of ‘genome shock’, such as genome reorganization and subgenome expres- sion dominance. Here we study polyploidization in Arabidopsis suecica, a post-glacial allopolyploid species formed via hybrid- ization of Arabidopsis thaliana and Arabidopsis arenosa. We generated a chromosome-level genome assembly of A. suecica and complemented it with polymorphism and transcriptome data from all species. Despite a divergence around 6 million years ago (Ma) between the ancestral species and differences in their genome composition, we see no evidence of a genome shock: the A. suecica genome is colinear with the ancestral genomes; there is no subgenome dominance in expression; and transposon dynamics appear stable. However, we find changes suggesting gradual adaptation to polyploidy. In particular, the A. thaliana subgenome shows upregulation of meiosis-related genes, possibly to prevent aneuploidy and undesirable homeologous exchanges that are observed in synthetic A. suecica, and the A. arenosa subgenome shows upregulation of cyto-nuclear pro- cesses, possibly in response to the new cytoplasmic environment of A. suecica, with plastids maternally inherited from A. thaliana. These changes are not seen in synthetic hybrids, and thus are likely to represent subsequent evolution. ncient polyploidization or whole-genome duplication is a Genomic changes have also been reported in natural allopoly- hallmark of most higher-organism genomes1,2, including ploids such as Tragopogon miscellus66,67, Mimulus pergrinus17 and Aour own3,4. While most of these organisms are now diploid Spartina anglica68; however, these examples resemble resynthe- and show only traces of polyploidy, there are many examples of sized allopolyploids in being extremely recent (around 100 years). recent polyploidization, especially among flowering plants5–9. These More-established allopolyploids generally do not show signs of examples are important because they allow us to study the process genomic changes12–14,16,69–71. of polyploidization. Here, we focus on an allopolyploid comparable in age to these Widespread naturally occurring polyploid hybrids (that is, allo- examples: the highly selfing72 A. suecica, which was formed through polyploids) show that natural polyploid species can quickly become the hybridization of A. thaliana and A. arenosa around 16 thousand successful10–18 and even invasive19. However, new allopolyploid species years ago, during the Last Glacial Maximum20, and which is cur- face numerous challenges such as population bottlenecks13,20, compe- rently found in northern Fennoscandia (Fig. 1a). The ancestral spe- tition with their diploid progenitors21, chromosome segregation22–24, cies diverged around 6 Ma (ref. 73), and based on organelle sequences, changes to genome structure25 and genome regulation26,27—poten- A. thaliana is the maternal and A. arenosa is the paternal parent74. tially leading to a ‘genome shock’28. In agreement with this, genomic This scenario is supported by A. arenosa being a ploidy-variable spe- and transcriptomic changes tied to the hybridization of diverged cies, such that A. suecica could readily be generated by the fusion of genomes have been reported in resynthesized polyploids of wheat29–35, an unreduced A. thaliana egg cell and an autotetraploid A. arenosa Brassica napus36–38 and cotton39–42, although exceptions exist43. sperm cell20,75. Despite a severe genetic bottleneck20, most of the The long-term importance of such changes is unclear. Evidence genetic variation in A. suecica is shared with the ancestral species, of the transcription and mobilization of transposable elements (TEs) ruling out a unique origin. To study genomic change in A. suecica, we in resynthesized wheat33,44–46 is not observed in cultivated wheat47. used long-read sequencing to generate a chromosome-level genome However, other cultivated crop genomes, like cotton, show evidence sequence, complemented by a partial assembly of a tetraploid consistent with dramatic changes following allopolyploidy5,48–53. A. arenosa, and by short-read genome and transcriptome sequenc- Strawberry6, peanut8 and the mesopolyploids Brassica rapa54 and ing data from populations of all three species—including ‘synthetic’ maize55 show evidence of subgenome dominance, whereas wheat56, A. suecica. Our main goal was to look for evidence of genome cotton51 and B. napus57 do not. The reasons for these differences are changes (particularly the kind of dramatic changes discussed above) not understood. in A. suecica relative to the ancestral species. Whether allopolyploid crops are representative of natural poly- ploidization is unclear. Domestication is frequently associated with Results and analysis very strong ‘artificial’ selection, which can markedly alter the fitness The genome is conserved. We assembled a reference genome landscape58–62, and structural variants have been linked to favour- from a naturally inbred20,72 A. suecica accession (ASS3), using able agronomic traits63–65. In addition, polyploid crops are generally 50× long-read PacBio sequencing (PacBio RSII). The absence of het- evolutionarily recent. erozygosity and the substantial (around 11.6%) divergence between 1Gregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter, Vienna, Austria. 2CEITEC - Central European Institute of Technology, and Faculty of Science, Masaryk University, Brno, Czech Republic. 3Institute of Biology, University of Hohenheim, Stuttgart, Germany. 4VIB-UGent Center for Plant Systems Biology, Ghent, Belgium. 5Department of Chromosome Biology, Max Planck Institute for Plant Breeding Research, Cologne, Germany. ✉e-mail: [email protected]; [email protected] NatURE EcOLOgy & EVOLUTION | VOL 5 | October 2021 | 1367–1381 | www.nature.com/natecolevol 1367 ARTICLES NATURE ECOLOGY & EVOLUTION a b A. thaliana subgenome Chr3 10 Mb 20 Mb ~6–8 Ma Chr4 10 Mb Chr2 ~16 ka 10 Mb A. thaliana A. suecica A. arenosa 10 Mb 2n = 10 2n = 4x = 26 2n = 2x(4x) = 16(32) Chr5 Selfing Selfing Outcrossing 20 Mb 20 Mb ♀ multiple origins ♂ Chr1 10 Mb 70 10 Mb 10 65 Chr13 10 Mb Chr6 20 Mb 60 Latitude (°) 10 Mb Chr12 10 Mb 55 Chr7 10 Mb 10 Mb Chr11 50 Chr8 10 Mb 10 Mb 10 20 30 40 Chr9 Chr10 Longitude (°) A. arenosa subgenome c d A. thaliana genome A. lyrata genome Chr3 Chr4 20 Mb Chr5 10 Mb 20 Mb 10 Mb 10 Mb 20 Mb Chr2 Chr320 Mb Chr4 10 Mb 10 Mb 10 Mb Chr6 10 Mb 20 Mb 30 Mb Chr2 10 Mb 10 Mb Chr7 10 Mb 20 Mb 20 Mb Chr1 Chr5 30 Mb 20 Mb 10 Mb Chr1 20 Mb 10 Mb Chr8 10 Mb Mb 20 10 Mb 20 Mb Chr1 10 Mb Chr5 20 Mb 10 Mb Chr13 10 Mb Chr6 20 Mb 10 Mb Chr7 10 Mb Chr12 10 Mb 10 Mb Chr2 Chr4 10 Mb 10 Mb Chr8 Chr11 10 Mb 20 Mb 10 Mb 10 Mb Chr3 Chr9 Chr10 A. thaliana subgenome of A. suecica A. arenosa subgenome of A. suecica Synteny block: Colinear Inversion Translocation Misassembly in A. lyrata Fig. 1 | The genome of A. suecica is largely colinear with the ancestral genomes. a, Schematic depicting the origin of A. suecica and its current distribution in relation to the ice cover at the Last Glacial Maximum. ka, thousand years ago. Ice cover data are from Natural Resource Canada (https://open.canada.ca/ data/en/dataset/a384bada-a787-5b49-9799-f5d589e97bd3). b, Chromosome-level assembly of the A. suecica genome with inner links depicting syntenic blocks between the A. thaliana and A. arenosa subgenomes of A. suecica. Histograms show the distribution of TEs (in blue) and protein-coding genes (in green) along the chromosomes. c, Synteny of the A. thaliana subgenome of A. suecica to the A. thaliana TAIR10 reference. In total 13 colinear synteny blocks were found. d, Synteny of the A. arenosa subgenome to A. lyrata. In total 40 synteny blocks were found, 33 of which were colinear. Of the remaining seven blocks, five represent inversions in the A. arenosa subgenome of A. suecica relative to A. lyrata, one is a translocation and one corresponds to a previously reported misassembly in the A. lyrata genome77. Orange bars show the density of missing regions (‘N’ bases) in the A. lyrata genome. 1368 NatURE EcOLOgy & EVOLUTION | VOL 5 | October 2021 | 1367–1381 | www.nature.com/natecolevol NATURE ECOLOGY & EVOLUTION ARTICLES the subgenomes facilitated the assembly. By contrast, assembling and structural changes associated with these clusters were A. arenosa is complicated by high heterozygosity (around 3.5% also suggested88. nucleotide diversity76) and high repeat content. Our assembly of Given this, we examined the composition and transcription of a tetraploid A. arenosa individual, included in this study, is frag- 45S rDNA repeats. Although the large and highly repetitive 45S mented: 3,629 contigs; N50 of 331 kb. The A. suecica assembly, how- rDNA clusters are missing from the genome assembly, we can ever, has an N50 contig size of 9.02 Mb. Contigs totalled 276 Mb measure the copy number of A. thaliana and A. arenosa 45S rRNA (around 90% and around 88% of genome size estimated by flow genes using sequencing coverage (see Methods). We find that cytometry and k-mer analysis, respectively; see Extended Data Fig. 1 three accessions have experienced massive loss of the A. thaliana and Methods). Contigs were placed into scaffolds using chromatin rDNA loci (Fig. 2a), which was confirmed for one of the acces- conformation capture (Hi-C) data and using the reference genomes sions (AS90a) by fluorescence in situ hybridization (FISH) analy- of A. thaliana and Arabidopsis lyrata (as substitute for A. arenosa) as sis (Fig. 2b,c). However, there is massive copy number variation guides. This resulted in 13 chromosome-scale scaffolds (Extended for 45S rRNA genes in A.
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