Diversification of Rosaceae Since the Late Cretaceous Based on Plastid
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Research Diversification of Rosaceae since the Late Cretaceous based on plastid phylogenomics Shu-Dong Zhang1*, Jian-Jun Jin1,2*, Si-Yun Chen1, Mark W. Chase3,4, Douglas E. Soltis5,6,7, Hong-Tao Li1, Jun-Bo Yang1, De-Zhu Li1 and Ting-Shuang Yi1 1Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China; 2Kunming College of Life Sciences, University of Chinese Academy of Sciences, Kunming, Yunnan 650201, China; 3Science Directorate, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, UK; 4School of Plant Biology, University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia; 5Florida Museum of Natural History, University of Florida, Gainesville, FL 32611-7800, USA; 6Department of Biology, University of Florida, Gainesville, FL 32611, USA; 7Genetics Institute, University of Florida, Gainesville, FL 32608, USA Summary Authors for correspondence: Phylogenetic relationships in Rosaceae have long been problematic because of frequent De-Zhu Li hybridisation, apomixis and presumed rapid radiation, and their historical diversification has Tel: +86 871 65223503 not been clarified. Email: [email protected] With 87 genera representing all subfamilies and tribes of Rosaceae and six of the other eight Ting-Shuang Yi families of Rosales (outgroups), we analysed 130 newly sequenced plastomes together with Tel: +86 871 65223136 12 from GenBank in an attempt to reconstruct deep relationships and reveal temporal diversi- Email: [email protected] fication of this family. Received: 1 November 2016 Our results highlight the importance of improving sequence alignment and the use of Accepted: 26 December 2016 appropriate substitution models in plastid phylogenomics. Three subfamilies and 16 tribes (as previously delimited) were strongly supported as monophyletic, and their relationships were New Phytologist (2017) fully resolved and strongly supported at most nodes. Rosaceae were estimated to have origi- doi: 10.1111/nph.14461 nated during the Late Cretaceous with evidence for rapid diversification events during several geological periods. The major lineages rapidly diversified in warm and wet habits during the Late Cretaceous, and the rapid diversification of genera from the early Oligocene onwards Key words: diversification, phylogenomics, occurred in colder and drier environments. plastome, rapid radiation, Rosaceae, systematic error. Plastid phylogenomics offers new and important insights into deep phylogenetic relation- ships and the diversification history of Rosaceae. The robust phylogenetic backbone and time estimates we provide establish a framework for future comparative studies on rosaceous evolution. relationships among major clades and genera in Rosaceae have Introduction historically been a major phylogenetic challenge (Morgan et al., Phylogenomics applies genomic data to reconstruct the evolu- 1994; Potter et al., 2007), exemplifying a pattern resulting from tionary history of organisms (Eisen, 1998; Eisen & Fraser, 2003; multiple rapid radiations and reticulation events (Campbell et al., Delsuc et al., 2005) and has been applied to tackle rapidly radiat- 2007). We use plastid phylogenomics here to better resolve phy- ing clades (Hackett et al., 2008; Jian et al., 2008; Bewick et al., logenetic relationships within Rosaceae. 2012; Zhou et al., 2012; Ruhfel et al., 2014; Wickett et al., 2014) Rosaceae are one of the most diverse angiosperm families with and hybridisation events (Marcet-Houben & Gabaldon, 2015; c. 90 genera and 3000 species with a global distribution. They are Sun et al., 2015) in diverse lineages. Due to their moderate size, especially rich in the temperate and warmer regions of the North- moderate nucleotide substitution rates and freedom from prob- ern Hemisphere (Potter et al., 2007). Rosaceous species have lems of paralogy (Clegg et al., 1994), plastid DNA sequences adapted to a wide variety of environments, ranging from mesic to have been widely used for the reconstruction of plant phyloge- xeric communities and tropical forest to tundra ecosystems. nies. A plastome phylogenomics approach has been successfully Many species of Rosaceae are also economically important, as applied to resolve many enigmatic relationships within edible fruits (apples, pears, apricots, plums, cherries, peaches, angiosperms and across all green plants (Jansen et al., 2007; raspberries, loquats and strawberries), ornamentals (crab apples, Moore et al., 2007, 2010; Zhong et al., 2010; Xi et al., 2012; roses, photinias, firethorns, rowans and hawthorns) and timbers Barrett et al., 2014; Ruhfel et al., 2014). Phylogenetic (plums and pears). For this reason, in part, the entire nuclear genome has been sequenced for at least nine species (with others *These authors contributed equally to this work. in progress) including apple (Velasco et al., 2010), five strawberry Ó 2017 The Authors New Phytologist (2017) 1 New Phytologist Ó 2017 New Phytologist Trust www.newphytologist.com New 2 Research Phytologist species (Shulaev et al., 2011; Hirakawa et al., 2014), peach sequenced plastomes representing all previously recognised major (Ahmad et al., 2011; International Peach Genome et al., 2013), lineages of Rosaceae, this study applies multiple phylogenetic pear (Wu et al., 2013) and mei (Sun et al., 2013). reconstruction methods in combination with appropriate models As an ecologically and economically important group, of sequence evolution to estimate phylogenetic relationships. The Rosaceae have been a particular focus of many botanists, and a major objectives of this study are to: resolve the phylogenetic rela- series of taxonomic and phylogenetic studies have been published tionships among major clades and genera of Rosaceae; test the (Potter et al., 2007). Recent molecular phylogenetic studies have utility of plastome sequence data to resolve phylogenetic relation- strongly supported the monophyly of Rosaceae and their sister ships of putatively rapidly radiating groups; and explore the tem- relationships to a clade formed by the other eight families of the poral diversification patterns of Rosaceae with respect to order Rosales (Soltis et al., 2011; Zhang et al., 2011; The palaeoenvironmental changes. Angiosperm Phylogeny Group, 2016). Previous molecular phylo- genetic studies based on a limited number of loci have greatly Materials and Methods advanced our understanding of rosaceous relationships (Morgan et al., 1994; Evans et al., 2000; Potter et al., 2002, 2007; Lo & Taxon sampling Donoghue, 2012; Chin et al., 2014). However, following the studies reviewed earlier, portions of the tree remained unresolved, We sampled 132 species from 79 genera (Supporting Informa- with weakly supported and conflicting relationships. Relation- tion Table S1) to represent all three recognised subfamilies ships among the three subfamilies (Amygdaloideae, Dryadoideae and 16 tribes of Rosaceae, and 10 species to represent six of and Rosoideae) remain contentious (Potter et al., 2007; Chin the other eight families of Rosales as outgroups. We included et al., 2014; Li et al., 2015), and those among some tribes and representatives of many genera that have been recently com- genera are also controversial and not fully resolved (Potter et al., bined with other genera or for which circumscriptions are 2007; Lo & Donoghue, 2012; Chin et al., 2014), especially those contentious. The voucher specimens were deposited in the within subfamily Dryadoideae and subtribe Malinae (formerly herbarium of Kunming Institute of Botany, Chinese Academy Pyrinae or Maloideae). of Sciences (KUN). Concomitantly, major classifications of Rosaceae based on morphology alone, or on both morphology and molecular data Plastome sequencing and data assembly do not agree regarding the delimitation of subfamilies, super- tribes, tribes, subtribes and even some genera (Hutchinson, Total genomic DNA was extracted from 100 mg of fresh leaves 1964; Schulze-Menz, 1964; Takhtajan, 1997; Kalkman, 2004; using a modified CTAB (cetrimonium bromide) method of Yang Potter et al., 2007). Homoplasy of morphological characters that et al. (2014). For most species, the plastomes were amplified in have been the basis for classifications, frequent interspecific and overlapping fragments using the long-range PCR method of even intergeneric hybridisation, apomixis and rapid radiation Yang et al. (2014), and PCR fragments were pooled together in have all created difficulties in both classification and phylogenetic roughly equal concentrations for subsequent sequencing. The reconstruction of Rosaceae (Campbell et al., 2007; Potter et al., plastomes of Kerria japonica and two Filipendula species failed to 2007; Lo & Donoghue, 2012). be amplified using this method, so 0.5 lg of total genomic DNA The large-scale evolutionary history of Rosaceae remains was directly used for sequencing. The DNA samples were sheared poorly understood, although previous dating analyses have into fragments of c. 500 bp and used to construct libraries accord- provided some insights. Most previous studies estimated a ing to the manufacturer’s manual (Illumina, San Diego, CA, stem age of Rosaceae between 90 and 80 Ma in the Late Cre- USA). Paired-end sequencing of 90 bp was conducted on an Illu- taceous (Wikstrom et al., 2001; Magallon & Castillo, 2009; mina HiSeq 2000 at BGI-Shenzhen, and > 200 Mb (> 2 Gb for Wang et al., 2009; Bell et al., 2010; Hohmann et al., 2015; K. japonica and Filipendula spp.) of sequence data for each sam- Tank et al., 2015), but 106.1 or 106.5