Abstract
Ferns are notorious for possessing large genomes and numerous chromosomes. Despite decades of speculation, the processes underlying the expansive genomes of ferns are unclear, largely due to the absence of a sequenced homosporous fern genome. The lack of this crucial resource has not only hindered investigations of evolutionary processes responsible for the unusual genome characteristics of homosporous ferns, but also impeded synthesis of genome evolution across land plants. Here, we used the model fern species Ceratopteris richardii to address the processes (e.g., polyploidy, spread of repeat elements) by which the large genomes and high chromosome numbers typical of homosporous ferns may have evolved and have been maintained. We directly compared repeat compositions in species spanning the green plant tree of life and a diversity of genome sizes, as well as both short- and long-read-based assemblies of Ceratopteris. We found evidence consistent with a single ancient polyploidy event in the evolutionary history of Ceratopteris based on both genomic and cytogenetic data, and on repeat proportions similar to those found in large flowering plant genomes. This study provides a major stepping-stone in the understanding of land plant evolutionary genomics by providing the first homosporous fern reference genome, as well as insights into the processes underlying the formation of these massive genomes.
Highlights
There are estimated to be over 400,000 species of extant land plants[1], encompassing an enormous array of morphological, physiological, and ecological diversity
Most extant fern diversity arose within the last 40–60 million years during the Cenozoic Era following the rise to dominance of the angiosperms[69,70]. Despite their substantial morphological diversity, sister relationship to seed plants, and lengthy evolutionary history, ferns represent the final frontier of land plant genomics
The diploid signal localizations of our bacterial artificial chromosomes (BACs)-fluorescent in situ hybridization (FISH) approach refute any recent whole-genome duplication (WGD) events that may have been ambiguous in the paralog-age distribution analyses
Summary
There are estimated to be over 400,000 species of extant land plants[1], encompassing an enormous array of morphological, physiological, and ecological diversity. While repeated episodes of WGD followed by extensive silencing and rearrangement cannot be discounted as an explanation for the paradoxical genomic, genetic, and chromosomal composition of ferns[21], alternative processes underlying their large genomes and high chromosome numbers must be explored. Most notable among these alternative explanations for the large genomes of ferns is the impact of transposable elements (TEs) on genome size, as TEs make up the majority of genome space in a variety of eukaryotic lineages. Aneuploidy or chromosomal fission are possible explanations for the high chromosomal complement of most ferns[22,26,43]
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