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Derived Evidence Supports Recent Polyploidization and a Major Phylogeographic Division in Trithuria Submersa (Hydatellaceae, Nymphaeales)

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Derived Evidence Supports Recent Polyploidization and a Major Phylogeographic Division in Trithuria Submersa (Hydatellaceae, Nymphaeales) Research Transcriptome-derived evidence supports recent polyploidization and a major phylogeographic division in Trithuria submersa (Hydatellaceae, Nymphaeales) Isabel Marques1,2,3*, Sean A. Montgomery1,2*, Michael S. Barker4, Terry D. Macfarlane5, John G. Conran6, Pilar Catalan3,7, Loren H. Rieseberg1, Paula J. Rudall8 and Sean W. Graham1,2 1Department of Botany, University of British Columbia, 6270 University Boulevard, Vancouver, BC V6T 1Z4, Canada; 2UBC Botanical Garden & Centre for Plant Research, University of British Columbia, 6804 Marine Drive SW, Vancouver, BC V6T 1Z4, Canada; 3Department of Agricultural and Environmental Sciences, High Polytechnic School of Huesca, University of Zaragoza, C/Carretera de Cuarte Km 1, Huesca E22071, Spain; 4Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA; 5Western Australian Herbarium, Science and Conservation Division, Department of Parks and Wildlife, Locked Bag 104, Bentley Delivery Centre, Bentley, WA 6983, Australia; 6School of Biological Sciences, Australian Centre for Evolutionary Biology and Biodiversity & Sprigg Geobiology Centre, The University of Adelaide, Benham Bldg DX 650 312, Adelaide, SA 5005, Australia; 7Department of Botany, Institute of Biology, Tomsk State University, Lenin Av. 36, Tomsk 634050, Russia; 8Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK Summary Author for correspondence: Relatively little is known about species-level genetic diversity in flowering plants outside the Isabel Marques eudicots and monocots, and it is often unclear how to interpret genetic patterns in lineages Tel: +1 604 822 4816 with whole-genome duplications. We addressed these issues in a polyploid representative of Email: [email protected] Hydatellaceae, part of the water-lily order Nymphaeales. Received: 28 June 2015 We examined a transcriptome of Trithuria submersa for evidence of recent whole-genome Accepted: 12 October 2015 duplication, and applied transcriptome-derived microsatellite (expressed-sequence tag sim- ple-sequence repeat (EST-SSR)) primers to survey genetic variation in populations across its New Phytologist (2016) 210: 310–323 range in mainland Australia. doi: 10.1111/nph.13755 A transcriptome-based Ks plot revealed at least one recent polyploidization event, consis- tent with fixed heterozygous genotypes representing underlying sets of homeologous loci. A Key words: ANA-grade, Australia, strong genetic division coincides with a trans-Nullarbor biogeographic boundary. microsatellite markers, population genetic Patterns of ‘allelic’ variation (no more than two variants per EST-SSR genotype) and diversity, transcriptome-enabled markers, recently published chromosomal evidence are consistent with the predicted polyploidization trans-Nullarbor plants, Trithuria. event and substantial homozygosity underlying fixed heterozygote SSR genotypes, which in turn reflect a selfing mating system. The Nullarbor Plain is a barrier to gene flow between two deep lineages of T. submersa that may represent cryptic species. The markers developed here should also be useful for further disentangling species relationships, and provide a first step towards future genomic studies in Trithuria. 1999; Soltis & Soltis, 2004; Saarela et al., 2007; Graham & Iles, Introduction 2009). Here we examined patterns of genetic diversity across Despite the important evolutionary role of polyploidization in most of the range of Trithuria submersa, the most widespread plants (e.g. Soltis et al., 2014; Mayrose et al., 2015), our under- member of Hydatellaceae (one of three families of Nymphaeales; standing of polyploids is still limited compared with diploids, in Angiosperm Phylogeny Group II, 2003). We also applied tran- part because of difficulties in applying standard genetic diversity scriptome-based evidence to address whether it has experienced estimators (e.g. De Silva et al., 2005; Obbard et al., 2006; polyploidization in its recent ancestry, as suggested by karyotypic Dufresne et al., 2014). Species-level genetic diversity studies of evidence (Kynast et al., 2014). polyploids are rare outside the eudicots and monocots in Relatively little is known about the evolutionary history of angiosperms, although see Quan et al. (2009) for a recent exam- Hydatellaceae (Nymphaeales), despite considerable recent atten- ple in the water lilies (Nymphaeales). The latter is an ancient tion following the family’s taxonomic realignment away from the aquatic clade that is the sister group of all other angiosperms monocots (Saarela et al., 2007; Graham & Iles, 2009). The fam- except Amborella (e.g. Mathews & Donoghue, 1999; Soltis et al., ily is now recognized as a major component of the ANITA or ANA grade (named after five of the six constituent families, or *These authors contributed equally to this work. the three component orders, Amborellales, Nymphaeales and 310 New Phytologist (2016) 210: 310–323 Ó 2015 The Authors www.newphytologist.com New Phytologist Ó 2015 New Phytologist Trust New Phytologist Research 311 Austrobaileyales), which collectively defines the deepest divisions reported (O. Hidalgo et al., unpublished; and see Iles et al., in flowering-plant phylogeny. The family comprises c. 12 species 2012). of Trithuria (the sole genus) that are restricted to Australia, New Here, we characterized the polyploid ancestry of T. submersa Zealand and India (Saarela et al., 2007; Iles et al., 2012, 2014). by looking for evidence of gene duplication peaks in the tran- Despite the ancient origin of its stem lineage, the crown clade of scriptome that correspond to whole-genome duplication the family diversified relatively recently (around the early (WGD). To provide further insights into the biogeography of Miocene), and much of its biogeographic distribution may be this species, we also characterized population genetic diversity explained by recent long-distance dispersal events (Iles et al., across mainland populations of T. submersa using microsatellite 2014). This may contrast with generally low dispersability in (expressed-sequence tag simple-sequence repeat; EST-SSR) Cabombaceae and Nymphaeaceae (L€ohne et al., 2005), the two markers that we developed from the transcriptome assembly. We water-lily families that comprise its sister group. also made an initial assessment of cross-species transferability of Most species in the family flourish in temporarily inundated the microsatellite markers in all congeners as a tool for future areas as short-lived (ephemeral) aquatics (Sokoloff et al., 2011; studies on the genetic structure in this family. Iles et al., 2014), although the family also includes several sub- merged aquatic species, at least one of which can live for several Materials and Methods years (Pledge, 1974). A remarkable diversity of reproductive sys- tems is also observed in Hydatellaceae, including dioecy, several cDNA library construction and 454 sequencing of Trithuria forms of cosexuality, autogamy and apomixis (Sokoloff et al., submersa 2008, 2011). The genus Trithuria is a candidate model-plant sys- tem for investigating the early evolution of the flowering plants, RNA extractions and preparation of normalized cDNA libraries along with other candidates in Nymphaeales (Vialette-Guiraud followed the protocol of Lai et al. (2012). Briefly, total RNA et al., 2011; Povilus et al., 2015). Species of Trithuria are a poten- from T. submersa material (Kew living accession no. 3830) grown tially attractive candidate model system because of their small in the Conservation Biotechnology Unit at the Royal Botanic habit (mature plants are a few cm tall), rapid, mostly annual life Gardens, Kew (from seeds collected by Renee Tuckett at Mersea cycle, suitability for cultivation (demonstrated at least vegeta- Road swamp, Western Australia, in 2006) was isolated using Tri- tively), and the capacity for self-fertilization in most species (Tay- zol reagent (Invitrogen) and purified with a Qiagen RNeasy mini lor et al., 2010; Sokoloff et al., 2011). They also have small column. Library construction involved selection for polyadeny- genome sizes (e.g. T. submersa,1C= c. 1.36 pg; Pellicer et al., lated (polyA+) transcripts to enrich for protein-coding mRNAs 2013), which may facilitate future genomic initiatives, and one and normalization with the Trimmer-Direct cDNA Normaliza- or more species in the family is thought to be diploid (e.g. tion Kit (Evrogen, Moscow, Russia) to improve the representa- T. australis,2n = 14; see Iles et al., 2012). We have no informa- tion of low-copy transcripts and thereby maximize gene tion on wild genotypes or the genetic structure of natural popula- discovery. Normalized cDNA was prepared for sequencing fol- tions of Trithuria, which would be useful for clarifying species lowing the genomic DNA shotgun protocol provided by 454 Life limits, particularly in a group of three closely related species of Sciences (Branford, CT, USA). Sequencing was performed using Trithuria: T. bibracteata, T. occidentalis and T. submersa a 454 GS-FLX sequencer and Titanium reagents. The 454 (Sokoloff et al., 2008; Iles et al., 2012, 2014). These three species sequences were cleaned using the program SNOWHITE (Barker appear to be intermingled or nested in gene trees based on plastid et al., 2010; Dlugosch et al., 2013), and the transcriptome was and nuclear ribosomal internal transcribed spacer region (ITS) assembled using MIRA v.3.0.5 (Chevreux et al., 2004) with default data (Iles et al., 2012, 2014), but the phylogenetic data are sug- parameters for 454 data
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