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Extreme Variation in GC, Gene and Intron Content and Multiple Inversions Between a Direct and Inverted Orientation of the Rrna Repeat

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Extreme Variation in GC, Gene and Intron Content and Multiple Inversions Between a Direct and Inverted Orientation of the Rrna Repeat University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications from the Center for Plant Science Innovation Plant Science Innovation, Center for 2018 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 University of Nebraska-Lincoln, jpmower@unl.edu Peng-Fei Ma University of Nebraska - Lincoln Felix Grewe Field Museum of Natural History, fgrewe@fieldmuseum.org Alex Taylor University of Michigan-Ann Arbor Todd P. Michael J.Craig Venter Institute Follow this and additional works at: https://digitalcommons.unl.edu/plantscifacpub See next page for additional authors Part of the Plant Biology Commons, Plant Breeding and Genetics Commons, and the Plant Pathology Commons Mower, Jeffrey P.; Ma, Peng-Fei; Grewe, Felix; Taylor, Alex; Michael, Todd P.; VanBuren, Robert; and Qiu, Yin- Long, "Lycophyte plastid genomics: extreme variation in GC, gene and intron content and multiple inversions between a direct and inverted orientation of the rRNA repeat" (2018). Faculty Publications from the Center for Plant Science Innovation. 202. https://digitalcommons.unl.edu/plantscifacpub/202 This Article is brought to you for free and open access by the Plant Science Innovation, Center for at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Center for Plant Science Innovation by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Jeffrey P. Mower, Peng-Fei Ma, Felix Grewe, Alex Taylor, Todd P. Michael, Robert VanBuren, and Yin-Long Qiu This article is available at DigitalCommons@University of Nebraska - Lincoln: https://digitalcommons.unl.edu/ plantscifacpub/202 Research 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. Mower1,2 , Peng-Fei Ma1,3, Felix Grewe4, Alex Taylor5, Todd P. Michael6 , Robert VanBuren7 and Yin-Long Qiu5 1Center for Plant Science Innovation, University of Nebraska, Lincoln, NE 68588, USA; 2Department of Agronomy and Horticulture, University of Nebraska, Lincoln, NE 68583, USA; 3Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650201, China; 4Grainger Bioinformatics Center, Science and Education, Field Museum of Natural History, Chicago, IL 60605, USA; 5Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA; 6J. Craig Venter Institute, La Jolla, CA 92037, USA; 7Department of Horticulture, Michigan State University, East Lansing, MI 48824, USA Summary Author for correspondence: Lycophytes are a key group for understanding vascular plant evolution. Lycophyte plas- Jeffrey P. Mower tomes are highly distinct, indicating a dynamic evolutionary history, but detailed evaluation is Tel: +1 402 472 2130 hindered by the limited availability of sequences. Email: jpmower@unl.edu Eight diverse plastomes were sequenced to assess variation in structure and functional con- Received: 27 August 2018 tent across lycophytes. Accepted: 10 December 2018 Lycopodiaceae plastomes have remained largely unchanged compared with the common ancestor of land plants, whereas plastome evolution in Isoetes and especially Selaginella is New Phytologist (2019) 222: 1061–1075 highly dynamic. Selaginella plastomes have the highest GC content and fewest genes and doi: 10.1111/nph.15650 introns of any photosynthetic land plant. Uniquely, the canonical inverted repeat was con- verted into a direct repeat (DR) via large-scale inversion in some Selaginella species. Ancestral Key words: evolutionary stasis, gene loss, reconstruction identified additional putative transitions between an inverted and DR orienta- inversion, Isoetes (quillworts), Lycopodiaceae tion in Selaginella and Isoetes plastomes. A DR orientation does not disrupt the activity of (clubmosses), Lycopodiophyta (lycophytes), copy-dependent repair to suppress substitution rates within repeats. plastid genome (plastome), Selaginella Lycophyte plastomes include the most archaic examples among vascular plants and the (spikemosses). most reconfigured among land plants. These evolutionary trends correlate with the mitochon- drial 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. Introduction Walsh, 1992), which may be facilitated by frequent intramolecu- lar recombination between IR copies that produces two isomeric Across the diversity of land plants, the plastid genome (plastome) forms of the plastome (Bohnert & Loffelhardt, 1982; Palmer, is distinguished by its overall conservation in size, structure and 1983). content. Plastomes of photoautotrophic land plants typically Comparative analysis of plastome structures from diverse land range from 120 to 160 kb in length, with c. 80 protein-coding plant representatives demonstrated that inversions and IR bound- genes, four rRNAs, and c. 30 tRNAs arranged into a structure ary shifts (via expansion or contraction) are the primary processes that usually includes large and small single-copy (SC) regions of structural rearrangements, with varying frequency among lin- (termed LSC and SSC) separated by a large inverted repeat (IR) eages (reviewed in Mower & Vickrey, 2018). More rarely, a third in two copies (Wicke et al., 2011; Jansen & Ruhlman, 2012; type of rearrangement (variously termed transposition or translo- Mower & Vickrey, 2018). One of the most notable effects of this cation) has been invoked to explain the intramolecular relocation genomic structure is that substitution rates are several times lower of one or more genes within the plastome (e.g., Milligan et al., in the IR relative to SC regions (Wolfe et al., 1987; Perry & 1989; Cosner et al., 1997, 2004; Chumley et al., 2006; Tsuji Wolfe, 2002; Li et al., 2016; Zhu et al., 2016). This reduction in et al., 2007; Karol et al., 2010; Knox, 2014). Nearly all such IR substitution rates has been attributed to a copy-dependent examples come from more rearranged plastomes, making it diffi- repair mechanism such as biased gene conversion (Birky & cult to reconstruct whether the relocation was direct (implying Ó 2018 The Authors New Phytologist (2019) 222: 1061–1075 1061 New Phytologist Ó 2018 New Phytologist Trust www.newphytologist.com This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. New 1062 Research Phytologist the involvement of a translocase or site-specific recombinase) or nonvascular plant plastomes, implying a plesiomorphic retention the indirect result of some combination of overlapping inversions of gene order from the land plant ancestor (Wolf et al., 2005; and/or differential IR expansions/contractions. Mower & Vickrey, 2018). By contrast, Isoetes and Selaginella har- Among nonvascular land plants, plastomic rearrangements are bor plastomes that are more rearranged (Tsuji et al., 2007; Smith, rare, with just a few examples of inversions and IR boundary 2009; Karol et al., 2010; Xu et al., 2018). The plastome from shifts and no putative cases of transposition/translocation. Isoetes flaccida exhibits two diagnostic changes, including an inver- Indeed, plastomes from most species are fully collinear, including sion affecting chlL and chlN and a putative translocation of ycf2 duplications of four ribosomal RNAs (rRNAs) and five transfer from the LSC to the SSC (Karol et al., 2010). Plastomes from RNAs (tRNAs) within the IR (Grosche et al., 2012; Bell et al., three Selaginella species (S. moellendorffii, S. tamariscina,and 2014; Villarreal et al., 2018), indicating that this structural S. uncinata) are more diverse due to multiple inversions, putative arrangement was stably inherited from the common ancestor of translocations, and gene losses (Tsuji et al., 2007; Smith, 2009; all land plants (Mower & Vickrey, 2018). The rare exceptions of Xu et al., 2018). The IR has evolved differently in all three genera, structural change involve a c. 70 kb inversion that characterizes exemplified by minor expansions in Huperzia that captured por- mosses within the Funariidae (Sugiura et al., 2003; Goffinet tions of ndhF and exon 2 of rps12 (Wolf et al., 2005; Karol et al., et al., 2007), a 1 kb inversion unique to the parasitic liverwort 2010), by an independent and slightly larger IR expansion in Aneura mirabilis (Wickett et al., 2008), and a c. 7 kb IR expan- Isoetes that assimilated rps7 and exons 2 and 3 of rps12 (Karol sion that is specific to hornworts in Anthocerotaceae (Villarreal et al., 2010), and by distinct IR expansions in different Selaginella et al., 2013). species accompanied by multiple losses of tRNA genes (Tsuji By contrast, inversions and IR boundary shifts are recurrent et al., 2007; Smith, 2009; Xu et al., 2018). themes in the evolution of euphyllophyte (i.e., angiosperm, gym- The variable nature of plastome sequences among lycophytes nosperm, and fern) plastomes (Zhu et al., 2016; Mower & Vick- indicates that multiple evolutionary events must have occurred, rey, 2018). For example, a c. 35 kb inversion is shared
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