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

Homosporous lycophytes (Lycopodiaceae) are a deeply diverged lineage in the plant tree of life, having split from heterosporous lycophytes (Selaginella and Isoetes) ~400 Mya. Compared to the heterosporous lineage, Lycopodiaceae has markedly larger genome sizes and remains the last major plant clade for which no chromosome-level assembly 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 intragenomic 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 highlight a potentially meaningful genomic contrast between homosporous and heterosporous species.

Population genomics of the Isoetes appalachiana (Isoetaceae) complex supports a 'diploids-first' approach to conservation.

BACKGROUND AND AIMS: Allopolyploidy is an important driver of diversification and a key contributor to genetic novelty across the tree of life. However, many studies have questioned the importance of extant polyploid lineages, suggesting that the vast majority may constitute evolutionary 'dead ends'. This has important implications for conservation efforts where polyploids and diploid progenitors often compete for wildlife management resources. Isoetes appalachiana is an allotetraploid that is broadly distributed throughout the eastern USA alongside its diploid progenitors, I. valida and I. engelmannii. As such, this species complex provides an excellent opportunity to investigate the processes that underpin the formation and survival of allopolyploid lineages. METHODS: Here we utilized RADseq and whole-chloroplast sequencing to unravel the demographic and evolutionary history of hybridization in this widespread species complex. We developed a modified protocol for phasing RADseq loci from an allopolyploid in order to examine each progenitor's genetic contribution independently in a phylogenetic context. Additionally, we conducted population-level analyses to examine genetic diversity and evidence of gene flow within species. KEY RESULTS: Isoetes appalachiana is the product of multiple phylogenetic origins, suggesting that formation and establishment of allopolyploids are common in this group. Hybridization appears to be unidirectional, with I. engelmannii consistently being the maternal progenitor. Additionally, we find that polyploid lineages are genetically isolated, rarely if ever experiencing gene flow between geographically distinct populations. CONCLUSIONS: Allopolyploid lineages of I. appalachiana appear to form frequently and experience a high degree of genetic isolation following formation. Thus, our results appear to corroborate the hypothesis that the vast majority of recently formed polyploids may represent evolutionary dead ends. However, this does not necessarily lessen the evolutionary importance or ecological impact of polyploidy per se. Accordingly, we propose a conservation strategy that prioritizes diploid taxa, thus preserving downstream processes that recurrently generate allopolyploid diversity.

The flying spider-monkey tree fern genome provides insights into fern evolution and arborescence.

To date, little is known about the evolution of fern genomes, with only two small genomes published from the heterosporous Salviniales. Here we assembled the genome of Alsophila spinulosa, known as the flying spider-monkey tree fern, onto 69 pseudochromosomes. The remarkable preservation of synteny, despite resulting from an ancient whole-genome duplication over 100 million years ago, is unprecedented in plants and probably speaks to the uniqueness of tree ferns. Our detailed investigations into stem anatomy and lignin biosynthesis shed new light on the evolution of stem formation in tree ferns. We identified a phenolic compound, alsophilin, that is abundant in xylem, and we provided the molecular basis for its biosynthesis. Finally, analysis of demographic history revealed two genetic bottlenecks, resulting in rapid demographic declines of A. spinulosa. The A. spinulosa genome fills a crucial gap in the plant genomic landscape and helps elucidate many unique aspects of tree fern biology.

Underwater CAM photosynthesis elucidated by Isoetes genome.

To conserve water in arid environments, numerous plant lineages have independently evolved Crassulacean Acid Metabolism (CAM). Interestingly, Isoetes, an aquatic lycophyte, can also perform CAM as an adaptation to low CO2 availability underwater. However, little is known about the evolution of CAM in aquatic plants and the lack of genomic data has hindered comparison between aquatic and terrestrial CAM. Here, we investigate underwater CAM in Isoetes taiwanensis by generating a high-quality genome assembly and RNA-seq time course. Despite broad similarities between CAM in Isoetes and terrestrial angiosperms, we identify several key differences. Notably, Isoetes may have recruited the lesser-known 'bacterial-type' PEPC, along with the 'plant-type' exclusively used in other CAM and C4 plants for carboxylation of PEP. Furthermore, we find that circadian control of key CAM pathway genes has diverged considerably in Isoetes relative to flowering plants. This suggests the existence of more evolutionary paths to CAM than previously recognized.

On the evolutionary significance of horizontal gene transfers in plants.

Horizontal gene transfer (HGT) has long been seen as a crucial process in the evolution of prokaryotic species, but until recently it was thought to have little, if any, effect on the evolution of eukaryotic life forms. Detecting and describing HGT events in eukaryotes is difficult, making this phenomenon at times controversial. However, modern advances in genomics and bioinformatics have radically altered our view of HGT in eukaryotes, especially in plants. It now appears that HGT to and from plant lineages is more common than previously suspected. Importantly, the transfer of functional nuclear genes with adaptive significance has been reported in numerous taxa. Here we review several recent studies that have found evidence of the horizontal transfer of nuclear genes, and argue that HGT has undoubtedly had profound impacts on plant evolution as a whole.

Can asexuality confer a short-term advantage? Investigating apparent biogeographic success in the apomictic triploid fern Myriopteris gracilis.

PREMISE OF THE STUDY: Although asexual taxa are generally seen as evolutionary dead ends, asexuality appears to provide a short-term benefit in some taxa, including a wider geographic distribution compared to sexual relatives. However, this may be an illusion created by multiple, morphologically cryptic, asexual lineages, each occupying a relatively small area. In this study we investigate the role of multiple lineages in the biogeography of Myriopteris gracilis Fée (Pteridaceae), a North American apomictic triploid fern species with a particularly large range. METHODS: Range-wide asexuality was assessed by counting spores/sporangium in 606 Myriopteris gracilis specimens from across the species range, and lineage structure was assessed with both plastid DNA sequence and Genotyping By Sequencing (GBS) SNP datasets. KEY RESULTS: Spore counting of >600 specimens identified no sexual populations, establishing that Myriopteris gracilis is exclusively asexual. The plastid data estimated the crown age of M. gracilis at ca. 2.5 mya and identified two lineages, each largely confined to the eastern or western portions of the range. These groups were further subdivided by the GBS data, revealing at least seven asexual lineages of varying geographic distributions, each occupying a relatively small portion of the total range of M. gracilis. CONCLUSIONS: Although maintained exclusively through asexual reproduction, the broad distribution of Myriopteris gracilis is a compilation of numerous, independently formed asexual lineages. Since no single asexual lineage occupies the full extent of the species distribution, recurrent lineage formation should be considered when evaluating the short-term benefit of asexuality in this taxon and others.