A recurring syndrome of accelerated plastid genome evolution in the angiosperm tribe Sileneae (Caryophyllaceae)

• Multiple species in the angiosperm tribe Sileneae harbor divergent plastid genomes.
• At least three lineages exhibit parallel increases in the rate of genome evolution.
• These lineages have elevated substitution rates in the same subset of plastid genes.
• Independent lineages also share identical inversions and intron losses.
• Multiple mechanisms are likely responsible for this repeated evolutionary pattern.

In flowering plants, plastid genomes are generally conserved, exhibiting slower rates of sequence evolution than the nucleus and little or no change in structural organization. However, accelerated plastid genome evolution has occurred in scattered angiosperm lineages. For example, some species within the genus Silene have experienced a suite of recent changes to their plastid genomes, including inversions, shifts in inverted repeat boundaries, large indels, intron losses, and rapid rates of amino acid sequence evolution in a subset of protein genes, with the most extreme divergence occurring in the protease gene clpP. To investigate the relationship between the rates of sequence and structural evolution, we sequenced complete plastid genomes from three species (Silene conoidea, S. paradoxa, and Lychnis chalcedonica), representing independent lineages within the tribe Sileneae that were previously shown to have accelerated rates of clpP evolution. We found a high degree of parallel evolution. Elevated rates of amino acid substitution have occurred repeatedly in the same subset of plastid genes and have been accompanied by a recurring pattern of structural change, including cases of identical inversions and intron loss. This “syndrome” of changes was not observed in the closely related outgroup Agrostemma githago or in the more slowly evolving Silene species that were sequenced previously. Although no single mechanism has yet been identified to explain the correlated suite of changes in plastid genome sequence and structure that has occurred repeatedly in angiosperm evolution, we discuss a possible mixture of adaptive and non-adaptive forces that may be responsible.

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