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Total Duplication of the Small Single Copy Region in the Angiosperm Plastome: Rearrangement and Inverted Repeat Instability in Asarum

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Total Duplication of the Small Single Copy Region in the Angiosperm Plastome: Rearrangement and Inverted Repeat Instability in Asarum See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/323136699 Total duplication of the small single copy region in the angiosperm plastome: Rearrangement and inverted repeat instability in Asarum Article in American Journal of Botany · February 2018 DOI: 10.1002/ajb2.1001 CITATIONS READS 24 150 4 authors, including: Brandon T. Sinn Otterbein University 26 PUBLICATIONS 286 CITATIONS SEE PROFILE Some of the authors of this publication are also working on these related projects: Planteome Project View project All content following this page was uploaded by Brandon T. Sinn on 06 December 2019. The user has requested enhancement of the downloaded file. RESEARCH ARTICLE Total duplication of the small single copy region in the angiosperm plastome: Rearrangement and inverted repeat instability in Asarum Brandon T. Sinn1,3,4 , Dylan D. Sedmak1, Lawrence M. Kelly2, and John V. Freudenstein1 Manuscript received 29 August 2017; revision accepted 27 PREMISE OF THE STUDY: As more plastomes are assembled, it is evident that rearrangements, November 2017. losses, intergenic spacer expansion and contraction, and syntenic breaks within otherwise 1 The Ohio State University Museum of Biological Diversi- functioning plastids are more common than was thought previously, and such changes have ty, Department of Evolution, Ecology, and Organismal Biology, developed independently in disparate lineages. However, to date, the magnoliids remain Columbus, Ohio 43212, USA characterized by their highly conserved plastid genomes (plastomes). 2 New York Botanical Garden, Bronx, New York 10458-5126, USA 3 West Virginia University, Department of Biology, Morgantown, METHODS: Illumina HiSeq and MiSeq platforms were used to sequence the plastomes of West Virginia 26505, USA Saruma henryi and those of representative species from each of the six taxonomic sections 4 Author for correspondence (e-mail: [email protected]) of Asarum. Sequenced plastomes were compared in a phylogenetic context provided Citation: Sinn, B. T., D. D. Sedmak, L. M. Kelly, and J. V. Freuden- by maximum likelihood and parsimony inferences made using an additional 18 publicly stein. 2018. Total duplication of the small single copy region in available plastomes from early- diverging angiosperm lineages. the angiosperm plastome: Rearrangement and inverted repeat instability in Asarum. American Journal of Botany 105(1): 71–84. KEY RESULTS: In contrast to previously published magnoliid plastomes and the newly doi: 10.1002/ajb2.1001 sequenced Saruma henryi plastome published here, Asarum plastomes have undergone extensive disruption and contain extremely lengthy AT- repeat regions. The entirety of the small single copy region (SSC) of A. canadense and A. sieboldii var. sieboldii has been incorporated into the inverted repeat regions (IR), and the SSC of A. delavayi is only 14 bp long. All sampled Asarum plastomes share an inversion of a large portion of the large single copy region (LSC) such that trnE- UUC is adjacent to the LSC- IR boundary. CONCLUSIONS: Plastome divergence in Asarum appears to be consistent with trends seen in highly rearranged plastomes of the monocots and eudicots. We propose that plastome instability in Asarum is due to repetitive motifs that serve as recombinatory substrates and reduce genome stability. KEY WORDS Aristolochiaceae; Asarum; cruciform DNA; inverted repeat region; magnoliid; phylogenomics; plastid genome; plastome; small single copy region The majority of sequenced angiosperm plastid genomes (plas- et al., 2010; Guisinger et al., 2011; Ruhlman and Jansen, 2014; Sloan tomes) are highly conserved with respect to gene content, gene et al., 2014). However, syntenically disrupted and otherwise diver- order (synteny), length, and GC content (Guisinger et al., 2011; gent plastomes have only recently been reported in the magnoli- Wicke et al., 2011; Ruhlman and Jansen, 2014). Nearly all angio- ids (Blazier et al., 2016b; Naumann et al., 2016), an early-diverging sperm plastomes are functionally tripartite due to the presence angiosperm clade that comprises approximately 10,000 species in of two coevolving, expansive inverted repeat (IR) regions that 20 families (Stevens, 2001) and four orders (Cai et al., 2006; APG separate large (LSC) and small single copy (SSC) regions. The IR IV, 2016). Here, we characterize widespread plastome disruption regions have long been hypothesized to lend stability to the genome and its putative causes in one magnoliid lineage, and we present (Palmer, 1983; Knox, 2014). With the advent of massively parallel evidence for the first reported incorporation of the entirety of the sequencing, our sampling and understanding of plastome diversity SSC region into the IR. across the angiosperm phylogeny have greatly improved (Ruhlman The magnoliids represent the largest clade of basal angiosperms, and Jansen, 2014), and the discovery of nonstandard plastomes has yet the plastome sequences of only 46 representative taxa have been become increasingly common among the monocots and eudicots published (Cai et al., 2006; Kuang et al., 2011; Li et al., 2013; Bla- (Chumley et al., 2006; Cai et al., 2008; Haberle et al., 2008; Magee zier et al., 2016b; Zhou et al., 2017). Relative to other angiosperm American Journal of Botany 105(1): 71–84, 2018; http://www.wileyonlinelibrary.com/journal/AJB © 2018 Botanical Society of America • 71 72 • American Journal of Botany lineages, magnoliid plastomes have generated comparatively little plastome rearrangement be inferred from our data using a phylo- interest aside from their use in phylogenetic studies (Jansen et al., genetic framework? 2007; Moore et al., 2010; Soltis et al., 2011; Li et al., 2013; Logacheva Through the comparison of the disrupted plastomes of Asa- et al., 2014; Ruhfel et al., 2014); those sequenced to date are unre- rum with the canonically ordered Saruma plastome, we found that arranged and highly conserved in length, and gene and GC content reduction in intergenic spacer complexity, coupled with length- (Cai et al., 2006; Li et al., 2013; Song et al., 2016), with the excep- ening of AT-rich motifs, corresponds to a reduction in syntenic tion of a six-gene inversion and IR expansion in Annona cherimola conservatism. Specifically, we found that the development and (Annonaceae; Blazier et al., 2016b) and the highly degraded plas- extension of tandem repeats are associated with syntenic breaks tome of the parasitic Hydnora visseri (Hydnoraceae; Naumann and that differential resolution of recombinatory events involving et al., 2016). Of the more than 1000 land-plant plastomes databased cruciform DNA is likely responsible for the variable presence of the by the National Center for Biotechnology Information (Ruhlman SSC region in Asarum plastomes. Our results provide further evi- et al., 2017), less than 1% are from the approximately 10,000 mag- dence that the control of replication fidelity and recombination may noliid species. Currently, the plastomes of Magnolia are perhaps together underlie a generalizable mechanism of syntenic disruption best characterized, with 18 of the 46 completely sequenced magno- of angiosperm plastomes. liid plastomes available on GenBank from this woody, slowly evolv- ing group (Kim et al., 2001). To date, only two syntenically disrupted magnoliid plastomes MATERIALS AND METHODS have been published. The plastome of Annona cherimola (Blazier et al., 2016b) has undergone marked IR expansion and contains DNA extraction and library preparation an SSC region comprising only two genes, whereas the plastome of the holoparasitic Hydnora visseri (Naumann et al., 2016) is Total DNA was extracted from 1 g of leaf material per sampled spe- extremely short and gene- sparse. Our discovery of highly variable, cies using the CTAB method (Doyle and Doyle, 1987; see Appen- lengthy AT- rich repetitive regions in Asarum plastomes (Sinn dix 1 for sample voucher information). To reduce the concentra- et al., 2015a) as part of a phylogenetic project led us to investigate tion of residual proteins and RNase, phenol–chloroform–isoamyl whether currently available magnoliid plastomes provide an accu- alcohol (25:24:1) extractions were used. DNA concentration and rate account of the presumed conservative nature of these organ- purity were quantified using a Nanodrop 2000 spectrophotometer ellar genomes. To assess the synteny and repeat content of Asarum (Thermo Scientific; Waltham, MA, USA). plastomes, we sequenced whole plastomes, surveying each taxo- nomic section of Asarum as well as the sole extant member of the DNA sequencing and data handling lineage that is sister to Asarum, Saruma henryi. We found that the plastome of S. henryi is syntenically similar to other plastomes Massively parallel sequencing of all species was accomplished by reported from the magnoliids, yet is dissimilar from these plas- multiplexing samples on multiple Illumina (San Diego, CA, USA) tomes due to the development of short AT- rich tandem repeats HiSeq and MiSeq lanes. MiSeq runs used version 3 chemistry to throughout the genome. Furthermore, the plastomes of Asarum achieve paired- end reads up to 300 bp long, and HiSeq sequencing are syntenically disrupted with respect to that of Saruma, and produced 100- bp paired- end reads with an average insert size of some have experienced shifts in IR boundaries that have resulted 560 bp. Library preparation and DNA sequencing were done at the in the heretofore unreported incorporation of the entirety of the
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