The Unique Evolutionary Trajectory and Dynamic Conformations of DR and IR/DR-Coexisting Plastomes of the Early Vascular Plant Selaginellaceae (Lycophyte)
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GBE The Unique Evolutionary Trajectory and Dynamic Conformations of DR and IR/DR-Coexisting Plastomes of the Early Vascular Plant Selaginellaceae (Lycophyte) Hong-Rui Zhang1,2, Qiao-Ping Xiang1,*, and Xian-Chun Zhang1,* 1State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, The Chinese Academy of Sciences, Beijing, China 2University of Chinese Academy of Sciences, Beijing, China *Corresponding authors: E-mails: [email protected];[email protected]. Accepted: March 30, 2019 Data deposition: All the plastomes have been deposited at GenBank under accession numbers MG272483–MG272484, MH598531– MH598537, and MK156800. Abstract Both direct repeats (DR) and inverted repeats (IR) are documented in the published plastomes of Selaginella species indicating the unusual and diverse plastome structure in the family Selaginellaceae. In this study, we newly sequenced complete plastomes of seven species from five main lineages of Selaginellaceae and also resequenced three species (Selaginella tamariscina, Selaginella uncinata, and Selaginella moellendorffii) to explore the evolutionary trajectory of Selaginellaceae plastomes. Our results showed that the plastomes of Selaginellaceae vary remarkably in size, gene contents, gene order, and GC contents. Notably, both DR and IR structures existed in the plastomes of Selaginellaceae with DR structure being an ancestral state. The occurrence of DR structure was at 257 Ma and remained in most subgenera of Selaginellaceae, whereas IR structure only reoccurred in Selaginella sect. Lepidophyllae (143 Ma) and Selaginella subg. Heterostachys (19 Ma). The presence of a pair of large repeats psbK-trnQ, together with DR/IR region in Selaginella bisulcata, Selaginella pennata, S. uncinata,andSelaginella hainanensis, could frequently mediate diverse homologous recombination and create approximately equal stoichiometric isomers (IR/DR-coexisting) and subgenomes. High proportion of repeats is presumably responsible for the dynamic IR/DR-coexisting plastomes, which possess a lower synony- mous substitution rate (dS) compared with DR-possessing and IR-possessing plastomes. We propose that the occurrence of DR structure, together with few repeats, is possibly selected to keep the stability of plastomes and the IR/DR-coexisting plastomes also reached an equilibrium in plastome organization through highly efficient homologous recombination to maintain stability. Key words: gene loss, homologous recombination, DR/IR evolution, Selaginella, substitution rate, time divergence. Introduction Selaginellaceae, Selaginella tamariscina (Xu et al. 2018), Plastid genomes (plastomes) of almost all land plants are Selaginella vardei, Selaginella indica (Zhang et al. 2018), and highly conserved and present the canonical quadripartite Selaginella kraussiana (Mower et al. 2018)inlandplants.The structure with a pair of large inverted repeats (termed IRA DR structure in Selaginellaceae was explained to have oc- and IRB) separated by two single-copy regions (termed LSC curred by 50-kb fragment inversion with a complete IRB and SSC) (Mower and Vickrey 2018). Normally, the range of being included, compared with the plastome of its sister fam- the IR varies through expansion or contraction. Complete loss ily Isoetaceae (Mower et al. 2018; Zhang et al. 2018). of the IR is rare but has been observed in some species of In addition to the exceptional existence of plastomes with Fabaceae (Lavin et al. 1990; Cai et al. 2008), Geraniaceae DR structure, a salient fraction of land plants plastomes ex- (Guisinger et al. 2011; Blazier et al. 2016; Ruhlman et al. perienced significant structural rearrangements, with evi- 2017), and Cactaceae (Sanderson et al. 2015). Remarkably, dence of large inversions and loss of entire gene family, plastomes with a pair of large direct repeats (termed DRA and despite the overall conservation in structures and gene order DRB) have been documented for four species of (Mower and Vickrey 2018). A 30-kb inversion (ycf2-psbM) ß The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 1258 Genome Biol. Evol. 11(4):1258–1274. doi:10.1093/gbe/evz073 Advance Access publication April 1, 2019 DR and IR/DR-Coexisting Plastomes of the Early Vascular Plant Selaginellaceae GBE was detected in the large single copy (LSC) of ferns and seed Jansen 2014). Three major pathways of gene loss have plants plastomes relative to bryophytes and lycophytes, been detected in land plants: 1) gene transfer to the nucleus which is a strong evidence showing lycophytes are located (infA, rpl22, rpl32, and accD), 2) substitution by a nuclear- as sister group of other vascular plants (Raubeson and encoded, mitochondrial targeted gene product (rps16), and Jansen 1992). The plastomes of ferns underwent two hypo- 3) substitution by a nuclear-encoded protein for a plastid gene thetical inversions (CE inversion [trnC to trnE] and DE inver- product (accD, rpl23) (Jansen and Ruhlman 2012). The mul- sion [trnD-trnY]) within rpoB-psbZ (BZ) region from the tiple independent ndh gene loss in different lineages is sup- ancestral gene order in eusporangiates to the derived gene posed to belong to the third pathway (Ruhlman et al. 2015). order in core leptosporangiates whereas the plastome struc- Selaginellaceae, one of the most ancient vascular plants tures within these two groups were generally consistent, with nearly 400 Myr of evolutionary history (Banks 2009)is respectively (Gao et al. 2011, 2013; Grewe et al. 2013). the largest family of lycophytes with 750 species classified Many other rearrangements also exist in some conifers into the only genus Selaginella (Jermy 1990; Weststrand and (Chaw et al. 2018) and several angiosperm lineages like Korall 2016b; Zhou et al. 2016). Selaginella species have Campanulaceae, Fabaceae, and Geraniaceae (Mower and highly diverse growth forms, including creeping, climbing, Vickrey 2018; Ruhlman and Jansen 2018). Inversion facili- prostrate, erect, and rosetted forms, and also inhabit an im- tated by recombination, transposition, and expansion/con- pressive range of habitats, from tropical rain forests to deserts, traction of the IR has been suggested as three different alpine, and arctic habitats (Zhang et al. 2013). Both mitochon- mechanisms that cause rearrangements in land plants drial and plastid genomes are more frequently subject to (Jansen and Ruhlman 2012). However, it is recently recog- alterations under specific environmental conditions nized that most plastomes exists as linear/concatemeric/ (Marechal and Brisson 2010). With such a high diversity in highly branched complex molecules in plants and these rear- habitat and growth forms and extremely long evolutionary rangement events are reinterpreted as result of a BIR (break- history, complex plastomes with different structures are in- induced replication) -like, recombination-dependent replica- ferred in Selaginellaceae (Tsuji et al. 2007). However, only tion mechanism between different linear plastome tem- seven species of Selaginella,viz.,Selaginella uncinata (Tsuji plates (Oldenburg and Bendich 2015). Furthermore, four et al. 2007), Selaginella moellendorffii (Smith 2009), S. tam- families of nuclear-encoded proteins (MutS homolog 1 ariscina (Xu et al. 2018), S. vardei, S. indica (Zhang et al. [MSH1], RecA-like recombinases, the organellar ssDNA- 2018), S. kraussiana,andSelaginella lepidophylla (Mower binding proteins [OSBs], and the Whirlies) have been char- et al. 2018) have been reported for their plastomes. acterized to target to both mitochondria and plastid, or Compared with the species from Lycopodiaceae and some protein members of the four families target to only Isoetaceae of lycophytes (Wolf et al. 2005; Karol et al. plastids and function as recombination surveillance machin- 2010; Guo et al. 2016; Moweretal.2018; Zhang et al. ery in plant plastids (Marechal and Brisson 2010). 2018), plastomes of Selaginella are, indeed, far less conserved Gene and intron contents are highly conserved among the in both structures and gene contents. Both S. uncinata and S. vast majority of land plants plastomes; however, numerous moellendorffii belong to subg. Stachygynandrum based on examples of gene loss or pseudogenization have been iden- both morphology-based classification (Jermy 1986)andare- tified in several angiosperm lineages (Ruhlman and Jansen cent molecular-based classification (Weststrand and Korall 2014). For example, most or all of the suite of 11 functionally 2016b). However, their plastomes show divergent variation related ndh genes have been lost independently in a small in structure. Several rearrangements, such as a 20-kb frag- assortment of taxa with diverse habitat, including the parasitic ment inversion, a 17-kb fragment transposition and gene Epifagus (Wicke et al. 2011), the mycoheterotrophic duplications, exist in these two species (Smith 2009). Rhizanthella gardneri (Delannoy et al. 2011), some members Selaginella kraussiana, belonging to subg. Gymnogynum of the carnivorous Lentibulariaceae (Wicke et al. 2014), the (sensu Weststrand and Korall 2016a), is morphologically sim- xerophytic Suguaro cactus (Sanderson et al. 2015) and gne- ilar with S. uncinata, whereas the morphology of