Systematics and Plastome Evolution in Schizaeaceae

Abstract

While the family Schizaeaceae (Schizaeales) represents only about 0.4% of the extant fern species diversity, it differs from other ferns greatly in gross morphologies, niche preferences, and life histories. One of the most notable features in this family is its mycoheterotrophic life style in the gametophytic stage, which appears to be associated with extensive losses of plastid genes. However, the limited number of sequenced plastomes, and the lack of a well-resolved phylogenetic framework of Schizaeaceae, makes it difficult to gain any further insight. Here, with a comprehensive sampling of ~77% of the species diversity of this family, we first inferred a plastid phylogeny of Schizaeaceae using three DNA regions. To resolve the deep relationships within this family, we then reconstructed a plastome-based phylogeny focusing on a selection of representatives that covered all the major clades. From this phylogenomic backbone, we traced the evolutionary histories of plastid genes and examined whether gene losses were associated with the evolution of gametophytic mycoheterotrophy. Our results reveal that extant Schizaeaceae is comprised of four major clades—Microschizaea, Actinostachys, Schizaea, and Schizaea pusilla. The loss of all plastid NADH-like dehydrogenase (ndh) genes was confirmed to have occurred in the ancestor of extant Schizaeaceae, which coincides with the evolution of mycoheterotrophy in this family. For chlorophyll biosynthesis genes (chl), the losses were interpreted as convergent in Schizaeaceae, and found not only in Actinostachys, a clade producing achlorophyllous gametophytes, but also in S. pusilla with chlorophyllous gametophytes. In addition, we discovered a previously undescribed but phylogenetically distinct species hidden in the Schizaea dichotoma complex and provided a taxonomic treatment and morphological diagnostics for this new species—Schizaea medusa. Finally, our phylogenetic results suggest that the current PPG I circumscription of Schizaea is non-monophyletic, and we therefore proposed a three-genus classification moving a subset of Schizaea species sensu PPG I to a third genus—Microschizaea.

A new species of grass fern, Schizaea erecta (Schizaeaceae), from Dinagat Island, Mindanao, Philippines

“…The sporangia of S. erecta are oblong whereas S. dichotoma has reniform sporangia (Figure 2G, H). Ke et al (2022) and Brownsey & Perrie (2014) stated that the S. dichotoma complex exhibits wide morphological and cytological variation. However, most members of this complex are poorly characterized and have been collectively lumped into "S. dichotoma", which was found to be polyphyletic in the phylogeny of Ke et al (2022).…”

“…Ke et al (2022) and Brownsey & Perrie (2014) stated that the S. dichotoma complex exhibits wide morphological and cytological variation. However, most members of this complex are poorly characterized and have been collectively lumped into "S. dichotoma", which was found to be polyphyletic in the phylogeny of Ke et al (2022). Although our new species was not included in this phylogeny, we reckon that it is morphologically so distinct that it merits treatment as a separate species, especially in anticipation of further splitting in this group.…”

“…The family Schizaeaceae (Schizaeales) represents about 0.4% of extant fern species diversity worldwide (PPG1, 2016). Its species differ from other ferns greatly in gross morphology, niche preferences, and life history (Ke et al, 2022). They can be distinguished by their simplified shape, and unique annulus among ferns.…”

“…There are about 35−40 species in the family, which are found throughout the tropical and south temperate regions of the world (PPG I, 2016;Smith et al, 2006). Schizaeaceae has been found to comprise four major clades-Microschizaea, Actinostachys, Schizaea pusilla Pursh (1814: 657), and the remaining members of Schizaea (Ke et al, 2022).…”

“…Schizaea dichotoma varies widely in morphology and cytology (Brownsey & Perrie, 2014), with various species sometimes segregated from it. Most segregates of this complex species are poorly characterized, and although collectively lumped into "S. dichotoma", have been found to resolve as polyphyletic in the DNA sequencebased phylogeny of Ke et al (2022).…”