Are the genomes of royal ferns really frozen in time? Evidence for coinciding genome stability and limited evolvability in the royal ferns

Schneider, Harald; Li, Hongmei; Clark, James W.; Hidalgo, Oriane; Pellicer, Jaume; Zhang, Shouzhou; Kelly, Laura J.; Fay, Michael F.; Leitch, Ilia J.

doi:10.1111/nph.13330

Cited by 28 publications

(27 citation statements)

References 35 publications

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“…Evidence so far supports the hypothesis that polyploid fern genomes are probably diploidized despite retaining polyploid chromosome numbers (Haufler, 1987;Clark et al, 2016). This argument appears to be consistent with the relative scarcity of documented dysploid events in the phylogeny of fern lineages (Lovis, 1977;Bellefroid et al, 2010;Hennequin et al, 2010;Wang et al, 2010;Wolf et al, 2015), and the recent report of static genome size for more than 180 million years in royal ferns (Bomfleur et al, 2014;Schneider et al, 2015).…”

Section: Introductionsupporting

confidence: 77%

Neo‐ and Paleopolyploidy contribute to the species diversity of Asplenium—the most species‐rich genus of ferns

Schneider

Chang

et al. 2017

J of Sytematics Evolution

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Polyploidy is widely considered as a major process in the evolution of plants but the accumulation of polyploid species diversity is still controversial. Some recent studies proposed increased extinction risk in neopolyploids compared with their diploid ancestors. The high proportion of polyploid ferns is expected to be formed mainly by neopolyploids, whereas paleopolyploid species are predicted to be clustered in clades founded by whole genome duplications. Here, we test this prediction by exploring the evolution of polyploidy in the derived fern family Aspleniaceae. The family has a global distribution and shows the highest frequency of polyploid taxa among all ferns. To test the hypothesis, we obtained a comprehensive phylogeny using chloroplast DNA sequences of 883 specimens representing 292 species. All published chromosome counts were mapped onto this phylogenetic framework in order to explore the evolution of polyploids. We recovered evidence for several whole genome duplications in the history of Aspleniaceae. Phylogenetic relationships of polyploids exceeding the tetraploid level suggest that tetraploid Asplenium species may have replaced their diploid ancestors as the main evolutionary players in some clades of this family.

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Section: Introductionsupporting

confidence: 77%

Neo‐ and Paleopolyploidy contribute to the species diversity of Asplenium—the most species‐rich genus of ferns

Schneider

Chang

et al. 2017

J of Sytematics Evolution

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“…Nevertheless, these broad‐scale differences in the response to WGD do not exclude a role for other genomic processes, such as changes in repeat composition and dynamics, impacting the evolution of particular fern lineages (Dodsworth et al, ; Wolf et al, ). For example, genome size variation in royal ferns (Osmundaceae) is not correlated with chromosome number (Schneider et al, ), and the genome size of the apomictic fern Asplenium monanthes L . complex and relatives cannot be explained solely by polyploidy (Dyer et al, ).…”

Section: Introductionmentioning

confidence: 99%

Polyploidy does not control all: Lineage‐specific average chromosome length constrains genome size evolution in ferns

Liu

Ekrt

Koutecký

et al. 2019

J of Sytematics Evolution

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Recent studies investigating the evolution of genome size diversity in ferns have shown that they have a distinctive genome profile compared with other land plants. Ferns are typically characterized by possessing medium‐sized genomes, although a few lineages have evolved very large genomes. Ferns are different from other vascular plant lineages as they are the only group to show evidence for a correlation between genome size and chromosome number. In this study, we aim to explore whether the evolution of fern genome sizes is not only shaped by chromosome number changes arising from polyploidy but also by constraints on the average amount of DNA per chromosome. We selected the genus Asplenium L. as a model genus to study the question because of the unique combination of a highly conserved base chromosome number and a high frequency of polyploidy. New genome size data for Asplenium taxa were combined with existing data and analyzed within a phylogenetic framework. Genome size varied substantially between diploid species, resulting in overlapping genome sizes among diploid and tetraploid spleenworts. The observed additive pattern indicates the absence of genome downsizing following polyploidy. The genome size of diploids varied non‐randomly and we found evidence for clade‐specific trends towards larger or smaller genomes. The 578‐fold range of fern genome sizes have arisen not only from repeated cycles of polyploidy but also through clade‐specific constraints governing accumulation and/or elimination of DNA.

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“…'static genomes' in the royal ferns (Bomfleur et al, 2014;Schneider et al, 2015) and arguments suggesting that chromosome size expansion via accumulation of repeats plays only a minor role in the evolution of fern genomes compared with seed plants (Wagner & Wagner, 1980; but see Dyer et al, 2013). The prediction is also consistent with the relatively small number of studies providing evidence for single chromosome gains and losses in ferns (Lovis, 1977), including recent studies that have incorporated phylogenetic evidence in their analyses, for example Hymenophyllum (Hennequin et al, 2010), Lepisorus (Wang et al, 2010) and the Loxoscaphe complex in Asplenium (Bellefroid et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Genome evolution of ferns: evidence for relative stasis of genome size across the fern phylogeny

et al. 2016

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Summary The genome evolution of ferns has been considered to be relatively static compared with angiosperms. In this study, we analyse genome size data and chromosome numbers in a phylogenetic framework to explore three hypotheses: the correlation of genome size and chromosome number, the origin of modern ferns from ancestors with high chromosome numbers, and the occurrence of several whole‐genome duplications during the evolution of ferns. To achieve this, we generated new genome size data, increasing the percentage of fern species with genome sizes estimated to 2.8% of extant diversity, and ensuring a comprehensive phylogenetic coverage including at least three species from each fern order. Genome size was correlated with chromosome number across all ferns despite some substantial variation in both traits. We observed a trend towards conservation of the amount of DNA per chromosome, although Osmundaceae and Psilotaceae have substantially larger chromosomes. Reconstruction of the ancestral genome traits suggested that the earliest ferns were already characterized by possessing high chromosome numbers and that the earliest divergences in ferns were correlated with substantial karyological changes. Evidence for repeated whole‐genome duplications was found across the phylogeny. Fern genomes tend to evolve slowly, albeit genome rearrangements occur in some clades.

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Are the genomes of royal ferns really frozen in time? Evidence for coinciding genome stability and limited evolvability in the royal ferns

Cited by 28 publications

References 35 publications

Neo‐ and Paleopolyploidy contribute to the species diversity of Asplenium—the most species‐rich genus of ferns

Neo‐ and Paleopolyploidy contribute to the species diversity of Asplenium—the most species‐rich genus of ferns

Polyploidy does not control all: Lineage‐specific average chromosome length constrains genome size evolution in ferns

Genome evolution of ferns: evidence for relative stasis of genome size across the fern phylogeny

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