Structural rearrangements of the chloroplast genome provide an important phylogenetic link in ferns.

Abstract

The chloroplast genome of most land plants is highly conserved. In contrast, physical and gene mapping studies have revealed a highly rearranged chloroplast genome in species representing four families of ferns. In all four, there has been a rare duplication of the psbA gene and the order of the psbA, 16S, and 23S rRNA genes has been inverted. Our analysis shows that the described rearrangement results from a minimum of two inversions within the inverted repeat. This chloroplast DNA structure provides unambiguous evidence that phylogenetically links families of ferns once thought to belong to different major evolutionary lineages.The chloroplast DNA (cpDNA) of most land plants is a circular molecule 120-160 kilobases (kb), which codes for 120 genes and typically contains an inverted repeat (IR). These repeated sequences range in size from 9.4 to 76 kb, code for several genes including those for 16S and 23S rRNA, and are separated by small single copy (SSC) and large single copy (LSC) regions (1-3). Gene order is remarkably similar in the cpDNAs of the fern Osmunda, the gymnosperm Ginkgo, and many angiosperms and differs from that in the bryophyte Marchantia primarily by a 30-kb inversion (4-6). This 30-kb inversion places the psbA gene close to the IR in Osmunda and in most gymnosperms and angiosperms (3, 4). The rRNA genes are part of an operon typically oriented with the 16S gene nearer to the LSC region and the 23S gene closer to the SSC region (Fig. 1A). Structural changes (such as gene duplications, gene losses, and inversions) are relatively rare and have been documented mainly in angiosperms (refs. 7-10, but see ref. 11).In this report, we describe the chloroplast genome shared by several ferns and show that it differs considerably from the typical structure detailed above. These differences provide molecular evidence about the evolutionary relationships of these ferns, which have been in dispute, and demonstrate that the chloroplast genomes of groups other than angiosperms have been markedly changed during evolution. Evidence concerning relationships at higher taxonomic levels is especially needed in ferns in which different phylogenies based on morphological characters are not concordant (12-15). Reasons for these discrepancies include (i) the use of narrative methods of phylogenetic analysis where the line of reasoning and the characters used are not made explicit, (ii) difficulties in identifying homologous parts in structurally simple organisms, and (iii) problems in determining the primitive or advanced states ofcharacters. The latter situation arises from the paucity of evidence from the fossil record (15-17) and the difficulty in choosing appropriate outgroups for many extant taxa due to the antiquity of ferns and the loss of many potential outgroups through extinction. MATERIALS AND METHODSLeaves of Polystichum acrostichoides (Michx.) Schott were collected in western Massachusetts and a voucher specimen (Sprague in 1986) was deposited at the Dean Herbarium of Indiana University. Leaves ...

Divergence of the phytochrome gene family predates angiosperm evolution and suggests that Selaginella and Equisetum arose prior to Psilotum

“…(See also Hasebe et al 1993.) Studies on structural arrangements of the chloroplast genome in ferns (Stein et al 1992) support the latter finding. Rare duplications and gene orders show that genera like Adiantum and Dryopteris belong to the same lineage.…”

The evolution of chloroplast genome structure in ferns

“…The first of these was approximately 18 kb and the second was approximately 21 kb ). Mapping studies of Polystichum acrostichoides and Cyathea furfuracea, representative of two major branches within the core leptosporangiate ferns (sensu Pryer et al 2004), indicate they share the rearranged gene order found in A. capillus-veneris (Stein et al 1992;Raubeson and Stein 1995). This suggests the core leptosporangiates all have approximately the same gene order as A. capillusveneris.…”

Deep sequencing of Ptilidium (Ptilidiaceae) suggests evolutionary stasis in liverwort plastid genome structure

“…changes in gene order, gene duplication and loss) are thought to be relatively rare. Plastid genome rearrangements have proved informative in many groups including embryophytes (Kelch et al 2004, Mishler & Kelch 2009), vascular plants (Raubeson & Jansen 1992), ferns (Stein et al 1992), Asteraceae (Jansen & Palmer 1987) and recently in mosses (Goffinet et al 2005(Goffinet et al , 2007; rearrangements in mitochondrial gene order have also provided supporting information for liverwort relationships inferred from DNA sequence data (e.g. Wahrmund et al 2008, Knoop 2010.…”