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

. 2019 Apr;222(2):1061-1075.

doi: 10.1111/nph.15650. Epub 2019 Jan 24.

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

Jeffrey P Mower et al. New Phytol. 2019 Apr.

Abstract

Lycophytes are a key group for understanding vascular plant evolution. Lycophyte plastomes are highly distinct, indicating a dynamic evolutionary history, but detailed evaluation is hindered by the limited availability of sequences. Eight diverse plastomes were sequenced to assess variation in structure and functional content across lycophytes. Lycopodiaceae plastomes have remained largely unchanged compared with the common ancestor of land plants, whereas plastome evolution in Isoetes and especially Selaginella is highly dynamic. Selaginella plastomes have the highest GC content and fewest genes and introns of any photosynthetic land plant. Uniquely, the canonical inverted repeat was converted into a direct repeat (DR) via large-scale inversion in some Selaginella species. Ancestral reconstruction identified additional putative transitions between an inverted and DR orientation in Selaginella and Isoetes plastomes. A DR orientation does not disrupt the activity of copy-dependent repair to suppress substitution rates within repeats. Lycophyte plastomes include the most archaic examples among vascular plants and the most reconfigured among land plants. These evolutionary trends correlate with the mitochondrial genome, suggesting shared underlying mechanisms. Copy-dependent repair for DR-localized genes indicates that recombination and gene conversion are not inhibited by the DR orientation. Gene relocation in lycophyte plastomes occurs via overlapping inversions rather than transposase/recombinase-mediated processes.

Keywords: Isoetes (quillworts); Lycopodiaceae (clubmosses); Lycopodiophyta (lycophytes); Selaginella (spikemosses); evolutionary stasis; gene loss; inversion; plastid genome (plastome).

© 2018 The Authors. New Phytologist © 2018 New Phytologist Trust.

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Figures

Figure 1

Figure 1

Functional content of lycophyte plastomes. (a) Protein‐coding genes. (b)

rRNA

genes. (c)

tRNA

genes. (d) Introns. Total counts are listed at the bottom of each functional category. Annotations for specific genes and introns that were corrected in this study are marked with a dark gray circle.

Figure 2

Figure 2

Structural evolution of Lycopodiaceae plastomes. The loss of trnT‐GGU is marked with a ψ. Inverted repeat (

IR

) expansions are denoted with red arrows, and genes affected by the

IR

expansion are listed in red text. The two genes arising from the split of ycf2 are labeled.

Figure 3

Figure 3

Structural evolution of Selaginella plastomes. Pseudogenes and lost genes are marked with a ψ and listed in black text. Inversion endpoints are marked by brown dotted lines, and the genes closest to each endpoint are listed in brown text. Inverted repeat (

IR

) expansions are denoted with red arrows, and genes affected by the

IR

expansion are listed in red text.

Figure 4

Figure 4

Structural evolution of Isoetes plastomes. Pseudogenes and lost genes are marked with a ψ and listed in black text. Inversion endpoints are marked by brown dotted lines, and the genes closest to each endpoint are listed in brown text. Inverted repeat (

IR

) expansions are denoted with red arrows, and genes affected by the

IR

expansion are listed in red text.

Figure 5

Figure 5

Substitution rate variation among lycophyte species and genes. (a) Synonymous divergence (

_d_S

) tree estimated from 51 concatenated genes that are single copy (

SC

) in all lycophytes. (b)

_d_S

tree estimated from concatenated ndhB + psbM + rps7 genes that are duplicated in Selaginella kraussiana. (c)

_d_S

tree estimated from rps4, which is duplicated in S. moellendorffii and S. tamariscina. (d) Overall divergence (d) tree estimated from four

rRNA

genes that are duplicated in all Selaginella species. Species with duplicated genes are shown in red. Terminal branch lengths for all Selaginella species are listed, and a ratio of branch lengths is given for each species in (b–d) relative to branch lengths in (a). All trees are drawn to the scale shown at bottom.

IR

, inverted repeat;

DR

, direct repeat.

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