Extraordinary preservation of gene collinearity over three hundred million years revealed in homosporous lycophytes

Abstract

Homosporous lycophytes (Lycopodiaceae) are a deeply diverged lineage in the plant tree of life, having split from heterosporous lycophytes (Selaginella and Isoetes) ~400 million years ago (MYA). Compared to the heterosporous lineage, Lycopodiaceae has markedly larger genome sizes and remains the last major plant clade for which no genomic data has been available. Here, we present chromosomal genome assemblies for two homosporous lycophyte species, the allotetraploid Huperzia asiatica and the diploid Diphasiastrum complanatum. Remarkably, despite that the two species diverged ~350 MYA, around 30% of the genes are still in syntenic blocks. Furthermore, both genomes had undergone independent whole genome duplications and the resulting intra-genomic syntenies have likewise been preserved relatively well. Such slow genome evolution over deep time is in stark contrast to heterosporous lycophytes and is correlated with a decelerated rate of nucleotide substitution. Together, the genomes of H. asiatica and D. complanatum not only fill a crucial gap in the plant genomic landscape, but also uncover a possibly unique genomic contrast between homosporous and heterosporous species.

Subgenome evolutionary dynamics in allotetraploid ferns: insights from the gene expression patterns in the allotetraploid species Phegopteris decursivepinnata (Thelypteridacea, Polypodiales)

“…Therefore, the observed absence of subgenome dominance in Phegopteris decursivepinnata is consistent with the slow genome downsizing in ferns and could partially explain the process of post-polyploid evolution seen in the broad range of homosporous ferns. Also in homosporous lycophyte, a lineage of land plants considered to exhibit a similar genome evolution as homosporous ferns ( Sessa and Der, 2016 ), a recent finding from ancient allotetraploid Huperzia showed a limited subgenome dominance and slow genome evolution following polyploidization ( Li et al., 2023 ), which support our prediction. To test the validity of our prediction, we still need to examine transcriptomic change and the pattern of genomic differentiation including TE abundance in more diverse allopolyploid fern species.…”

“…Polyploidy, or whole genome duplication, is pervasive in eukaryotes ( Van De Peer et al., 2017 ). It is especially common in plants ( Wood et al., 2009 ), and ancient polyploidization has occurred in most lineages of land plants including mosses ( Gao et al., 2022 ), lycophytes ( Xia et al., 2022 ; Li et al., 2023 ), ferns ( Huang et al., 2020 ; Pelosi et al., 2022 ; Chen et al., 2023 ), gymnosperms ( Li et al., 2015 ), and angiosperms (e.g. Landis et al., 2018 ).…”