Large-scale phylogenomic analysis resolves a backbone phylogeny in ferns

Abstract

BackgroundFerns, originated about 360 million years ago, are the sister group of seed plants. Despite the remarkable progress in our understanding of fern phylogeny, with conflicting molecular evidence and different morphological interpretations, relationships among major fern lineages remain controversial.ResultsWith the aim to obtain a robust fern phylogeny, we carried out a large-scale phylogenomic analysis using high-quality transcriptome sequencing data, which covered 69 fern species from 38 families and 11 orders. Both coalescent-based and concatenation-based methods were applied to both nucleotide and amino acid sequences in species tree estimation. The resulting topologies are largely congruent with each other, except for the placement of Angiopteris fokiensis, Cheiropleuria bicuspis, Diplaziopsis brunoniana, Matteuccia struthiopteris, Elaphoglossum mcclurei, and Tectaria subpedata.ConclusionsOur result confirmed that Equisetales is sister to the rest of ferns, and Dennstaedtiaceae is sister to eupolypods. Moreover, our result strongly supported some relationships different from the current view of fern phylogeny, including that Marattiaceae may be sister to the monophyletic clade of Psilotaceae and Ophioglossaceae; that Gleicheniaceae and Hymenophyllaceae form a monophyletic clade sister to Dipteridaceae; and that Aspleniaceae is sister to the rest of the groups in eupolypods II. These results were interpreted with morphological traits, especially sporangia characters, and a new evolutionary route of sporangial annulus in ferns was suggested. This backbone phylogeny in ferns sets a foundation for further studies in biology and evolution in ferns, and therefore in plants.

The complete plastid genome sequence of Trichomanes trollii (Hymenophyllaceae)

“…Likewise, several recent studies , Ruhfel et al 2014, Gitzendanner et al 2018 place Equisetum as sister of Ophioglossidae in agreement with the present results and this position appears better supported than the alternative arrangement of Equisetum as sister to all other ferns (Kuo et al 2011, Knie et al 2015, Rothfels et al 2015, Labiak and Karol 2017. However, the recent large-scale analyses using massive transcriptome data unequivocally support Equisetum as the sister of all other ferns (Qi et al 2018, Shen et al 2018.…”

“…It is noteworthy that this node remained equally poorly supported in an analysis of 25 nuclear loci with limited taxonomic sampling (Wolf et al 2018). In taxonomically better sampled analyses of much larger number of nuclear loci Hymenophyllales and Gleicheniales formed a clade, but Gleicheniales was paraphyletic with respect to Hymenophyllales (Qi et al 2018, Shen et al 2018. In contrast, the plastome analysis by Kuo et al (2018) supported, under most analyses, the monophyly of Gleicheniales, but the relationship between Hymenophyllales and Gleicheniales remained ambiguous.…”

“…Taxonomically broad molecular systematic investigations in ferns have mostly applied only a relatively few plastid markers (Schuettpelz and Pryer 2007, Lehtonen 2011, Testo and Sundue 2016, but complete plastid genomes (plastomes) have been increasingly used in recent years to verify the backbone of fern phylogeny (Gao et al 2013, Labiak and Karol 2017. Together with other high-throughput sequencing approaches (Rothfels et al 2015, Qi et al 2018, Shen et al 2018, Wolf et al 2018) these more character-rich studies have resolved and confirmed several previously uncertain nodes in the fern tree of life.…”

“…However, the exact phylogenetic relationships of some major fern lineages still remain controversial. For example, the phylogenetic position of horsetails (Equisetum) among the early fern lineages has remained elusive ever since they were first resolved as ferns (Pryer et al 2001, Wikström and Pryer 2005, Knie et al 2015, Qi et al 2018, Shen et al 2018. Filmy ferns (Hymenophyllales) represent another deep fern lineage with unclear relationships.…”

“…They clearly belong to the early diverging leptosporangiate ferns, but some studies have resolved them as sister to Gleicheniales (Pryer et al 2004, Lehtonen et al 2017 while most studies seem to resolve them as sister to all other nonosmundalean leptosporangiate ferns (Pryer et al 2001, Schuettpelz and Pryer 2007, Lehtonen 2011, Knie et al 2015, Rothfels et al 2015, Wolf et al 2018). Yet, some analyses have found Gleicheniales diverging before Hymenophyllales (Kuo et al 2011, Knie et al 2015, or Gleicheniales as a paraphyletic grade in respect to Hymenophyllales (Qi et al 2018, Shen et al 2018.…”