Genome-wide analyses of Geraniaceae plastid DNA reveal unprecedented patterns of increased nucleotide substitutions

Guisinger, Mary M.; Kuehl, Jennifer V.; Boore, Jeffrey L.; Jansen, Robert K.

doi:10.1073/pnas.0806759105

Cited by 149 publications

(184 citation statements)

References 51 publications

(58 reference statements)

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“…In numerous angiosperm lineages, a subset of plastid genes, including clpP1 and accD, display accelerated evolutionary rates, but the causes of this recurring phenomenon have remained unclear (Jansen et al 2007;Erixon and Oxelman 2008;Greiner et al 2008b;Guisinger et al 2008Guisinger et al , 2010Guisinger et al , 2011Straub et al 2011;Sloan et al 2012aSloan et al , 2014aBarnard-Kubow et al 2014;Weng et al 2014;Dugas et al 2015;Williams et al 2015;Blazier et al 2016;Zhang et al 2016). We investigated the nuclear genes that contribute to the multisubunit complexes that include ClpP1 and AccD, and incorporated population genetic and structural data to distinguish between relaxed purifying selection and positive selection as drivers of elevated d N /d S values.…”

Section: Discussionmentioning

confidence: 99%

“…Within angiosperms, most plastid genomes are highly conserved in sequence and structure (Jansen et al 2007;Wicke et al 2011), but multiple independent lineages have experienced accelerated rates of aa substitution in similar subsets of nonphotosynthetic genes (Jansen et al 2007;Erixon and Oxelman 2008;Greiner et al 2008b;Guisinger et al 2008Guisinger et al , 2010Guisinger et al , 2011Straub et al 2011;Sloan et al 2012aSloan et al , 2014aBarnard-Kubow et al 2014;Weng et al 2014;Dugas et al 2015;Williams et al 2015;Zhang et al 2016). Several mechanisms have been hypothesized to explain these repeated accelerations including positive selection, reduced effective population size (N e ), altered DNA repair, changes in gene expression, and pseudogenization following gene transfer to the nucleus (see above citations).…”

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confidence: 99%

“…In many cases of extreme plastid genome evolution, accelerations have disproportionately affected nonsynonymous sites, resulting in elevated ratios of nonsynonymous to synonymous substitution rates (d N /d S ) (e.g., Erixon and Oxelman 2008;Guisinger et al 2008;Barnard-Kubow et al 2014;Sloan et al 2014a), which indicates that changes in selection are likely involved. In addition, recent studies showed correlated increases in d N /d S between nuclear-and plastidencoded subunits in ribosomal (Sloan et al 2014b;Weng et al 2016) and RNA polymerase complexes (Zhang et al 2015), providing further evidence for changes in selection pressures.…”

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confidence: 99%

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Positive Selection in Rapidly Evolving Plastid–Nuclear Enzyme Complexes

et al. 2016

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Rates of sequence evolution in plastid genomes are generally low, but numerous angiosperm lineages exhibit accelerated evolutionary rates in similar subsets of plastid genes. These genes include clpP1 and accD, which encode components of the caseinolytic protease (CLP) and acetyl-coA carboxylase (ACCase) complexes, respectively. Whether these extreme and repeated accelerations in rates of plastid genome evolution result from adaptive change in proteins (i.e., positive selection) or simply a loss of functional constraint (i.e., relaxed purifying selection) is a source of ongoing controversy. To address this, we have taken advantage of the multiple independent accelerations that have occurred within the genus Silene (Caryophyllaceae) by examining phylogenetic and population genetic variation in the nuclear genes that encode subunits of the CLP and ACCase complexes. We found that, in species with accelerated plastid genome evolution, the nuclear-encoded subunits in the CLP and ACCase complexes are also evolving rapidly, especially those involved in direct physical interactions with plastid-encoded proteins. A massive excess of nonsynonymous substitutions between species relative to levels of intraspecific polymorphism indicated a history of strong positive selection (particularly in CLP genes). Interestingly, however, some species are likely undergoing loss of the native (heteromeric) plastid ACCase and putative functional replacement by a duplicated cytosolic (homomeric) ACCase. Overall, the patterns of molecular evolution in these plastidnuclear complexes are unusual for anciently conserved enzymes. They instead resemble cases of antagonistic coevolution between pathogens and host immune genes. We discuss a possible role of plastid-nuclear conflict as a novel cause of accelerated evolution.

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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Positive Selection in Rapidly Evolving Plastid–Nuclear Enzyme Complexes

et al. 2016

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“…Third, substitution rates calculated based on phylogenetic data suggest a lower mutation rate in chloroplast genomes than in plant nuclear genomes (Wolfe et al, 1987;Drouin et al, 2008). However, it is also known that organellar mutation rates can vary significantly in different lineages of seed plant evolution, even within a genus (Cho et al, 2004;Guisinger et al, 2008;Sloan et al, 2009). Last, it should be noted that three of the mutations in the O. glazioviana lines are associated with large repetitive elements repeats.…”

Section: Mutation Rates In the Chloroplast Genomementioning

confidence: 99%

Spontaneous Chloroplast Mutants Mostly Occur by Replication Slippage and Show a Biased Pattern in the Plastome of Oenothera

et al. 2016

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Spontaneous plastome mutants have been used as a research tool since the beginning of genetics. However, technical restrictions have severely limited their contributions to research in physiology and molecular biology. Here, we used full plastome sequencing to systematically characterize a collection of 51 spontaneous chloroplast mutants in Oenothera (evening primrose). Most mutants carry only a single mutation. Unexpectedly, the vast majority of mutations do not represent single nucleotide polymorphisms but are insertions/deletions originating from DNA replication slippage events. Only very few mutations appear to be caused by imprecise double-strand break repair, nucleotide misincorporation during replication, or incorrect nucleotide excision repair following oxidative damage. U-turn inversions were not detected. Replication slippage is induced at repetitive sequences that can be very small and tend to have high A/T content. Interestingly, the mutations are not distributed randomly in the genome. The underrepresentation of mutations caused by faulty double-strand break repair might explain the high structural conservation of seed plant plastomes throughout evolution. In addition to providing a fully characterized mutant collection for future research on plastid genetics, gene expression, and photosynthesis, our work identified the spectrum of spontaneous mutations in plastids and reveals that this spectrum is very different from that in the nucleus.

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“…Detail information about Sarlun-specific bands is listed in Table 3 (Strittmauer and Kossel, 1984, Alexandrov et al, 2009, Wu et al, 2009 was identified. Moreover, BLAST search result of band S4 protein sequence showed that ATP synthase CF0 subunit III of many eudicotyledons such as Geranium carolinianum and Erodium texanum (Guisinger et al, 2008) was identified. For BLAST search result of band S8 nucleotide sequence, the most likely candidate was a hypothetical protein of Sorghum bicolor (Paterson et al, 2009).…”

Section: Wwwintechopencommentioning

confidence: 99%