Mobile Elements Shape Plastome Evolution in Ferns

Abstract

Plastid genomes display remarkable organizational stability over evolutionary time. From green algae to angiosperms, most plastid genomes are largely collinear, with only a few cases of inversion, gene loss, or, in extremely rare cases, gene addition. These plastome insertions are mostly clade-specific and are typically of nuclear or mitochondrial origin. Here, we expand on these findings and present the first family-level survey of plastome evolution in ferns, revealing a novel suite of dynamic mobile elements. Comparative plastome analyses of the Pteridaceae expose several mobile open reading frames that vary in sequence length, insertion site, and configuration among sampled taxa. Even between close relatives, the presence and location of these elements is widely variable when viewed in a phylogenetic context. We characterize these elements and refer to them collectively as Mobile Open Reading Frames in Fern Organelles (MORFFO). We further note that the presence of MORFFO is not restricted to Pteridaceae, but is found across ferns and other plant clades. MORFFO elements are regularly associated with inversions, intergenic expansions, and changes to the inverted repeats. They likewise appear to be present in mitochondrial and nuclear genomes of ferns, indicating that they can move between genomic compartments with relative ease. The origins and functions of these mobile elements are unknown, but MORFFO appears to be a major driver of structural genome evolution in the plastomes of ferns, and possibly other groups of plants.

Peer Review #3 of "Plastome of mycoheterotrophic Burmannia itoana Mak. (Burmanniaceae) exhibits extensive degradation and distinct rearrangements (v0.1)"

“…The two translocations (Trans1/Trans2), which are typically located in the junction of IRs and SSC, are translocated into IRs of B. itoana plastome. It was hypothesized that MORFFO (Mobile Open Reading Frames in Fern Organelles) elements are regularly associated with inversions and changes to the inverted repeats (Robison et al 2018). In our study, the patterns of these rearrangements are analogous to those of rearrangements in several plastomes of ferns (Robison et al 2018).…”

“…It was hypothesized that MORFFO (Mobile Open Reading Frames in Fern Organelles) elements are regularly associated with inversions and changes to the inverted repeats (Robison et al 2018). In our study, the patterns of these rearrangements are analogous to those of rearrangements in several plastomes of ferns (Robison et al 2018). However, there is no unusual open reading frames (ORF) in the B. itoana plastome, while unusual ORF was identified in the ferns plastomes.…”

Lycophyte plastid genomics: extreme variation in GC, gene and intron content and multiple inversions between a direct and inverted orientation of the rRNA repeat

“…The status of infA is uncertain in some Selaginella species; an intact but highly divergent copy exists in S. uncinata, which was tentatively scored as functional in this study, whereas it has probably become a pseudogene in S. moellendorffii (due to the presence of two internal stop codons which cannot be eliminated because U-to-C RNA editing is absent from S. moellendorffii). In ferns, particular MORFFO mobile elements have led to structural rearrangements (Robison et al, 2018); however, no homology to any morffo-like genes was detected in any of the 14 lycophyte plastomes.…”

“…The relocation of several genes from the LSC to the IR of most leptosporangiate ferns was inferred to result from two overlapping inversions Stein et al, 1992;Raubeson & Stein, 1995). Other structural changes among fern plastomes may have been facilitated by the presence of mobile elements, termed MORFFO, within the plastome (Robison et al, 2018).…”

The first complete chloroplast genome of a mangrove fern, Acrostichum speciosum

“…Plastid genomes display remarkable conservation in sequence and stability in gene organization, making them ideal molecules to study plant phylogeny (Daniell et al 2016). Unlike the well-studied seed plants, chloroplast genome investigations of ferns are limited (Robison et al 2018). To the aspect of mangrove ferns, chloroplast genes were used as the molecular marker for hybrid identification (Zhang et al 2013).…”