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Abstract The large size and complexity of most fern genomes have hampered efforts to elucidate fundamental aspects of fern biology and land plant evolution through genome-enabled research. Here we present a chromosomal genome assembly and associated methylome, transcriptome and metabolome analyses for the model fern species Ceratopteris richardii . The assembly reveals a history of remarkably dynamic genome evolution including rapid changes in genome content and structure following the most recent whole-genome duplication approximately 60 million years ago. These changes include massive gene loss, rampant tandem duplications and multiple horizontal gene transfers from bacteria, contributing to the diversification of defence-related gene families. The insertion of transposable elements into introns has led to the large size of the Ceratopteris genome and to exceptionally long genes relative to other plants. Gene family analyses indicate that genes directing seed development were co-opted from those controlling the development of fern sporangia, providing insights into seed plant evolution. Our findings and annotated genome assembly extend the utility of Ceratopteris as a model for investigating and teaching plant biology. 

The mechanisms controlling chromosome number, size, and shape, and the relationship of these traits to genome size, remain some of the least understood aspects of genome evolution. Across vascular plants, there is a striking disparity in chromosome number between homosporous and heterosporous lineages. Homosporous plants (comprising most ferns and some lycophytes) have high chromosome numbers compared to heterosporous lineages (some ferns and lycophytes and all seed plants). Many studies have investigated why homosporous plants have so many chromosomes. However, homospory is the ancestral condition from which heterospory has been derived several times. Following this phylogenetic perspective, a more appropriate question to ask is why heterosporous plants have so few chromosomes. Here, we review life history differences between heterosporous and homosporous plants, previous work on chromosome number and genome size in each lineage, known mechanisms of genome downsizing and chromosomal rearrangements, and conclude with future prospects for comparative research. 

Plants are more tolerant of changes in their chromosome number than animals. Even dramatic changes, such as doubling of the entire genome, sometimes leads to beneficial outcomes. Though a history of genome doubling is common in most plants, the chromosome number in many plants does not reflect this. Complex genome downsizing processes help these plants shed extra genetic information, but are poorly understood. Through comparisons with ferns – a group with high chromosome numbers – Dr Paul Wolf from the University of Alabama in Huntsville aims to shed light on genome downsizing.