Multilocus species tree analyses resolve the ancient radiation of the subtribe Zizaniinae (Poaceae)
Graphical abstract
Introduction
Rapid radiations are ubiquitous in plants (Bell et al., 2010) and many other organisms (Amaral et al., 2012, Belfiore et al., 2008, Lee et al., 2012, Song et al., 2012, Townsend et al., 2011 and see reviews by Rokas and Carroll, 2006). The diversification of angiosperms is featured by a series of lineage radiations occurred from deep to shallow levels (Bell et al., 2010, Davies et al., 2004). Remarkable representatives of ancient rapid radiations in angiosperms include Mesangiospermae (Moore et al., 2007), Pentapetalae (Moore et al., 2010), Rosidae (Wang et al., 2009), and superasterids (Moore et al., 2010). Recent rapid radiations are also prevalent and have been extensively studied involving different plant families (e.g., Pillon et al., 2013, Richardson et al., 2001, Zou et al., 2008).
Rapid radiations pose a major challenge to molecular phylogenetic analysis. They not only hamper the reconstruction of phylogenetic relationships but also challenge the methodology of phylogenetic inference. The concatenation analysis of multiple-gene sequences has been successfully used to resolve rapid radiations (de Queiroz and Gatesy, 2007, Delsuc et al., 2005, Moore et al., 2010, Salichos and Rokas, 2013, Song et al., 2012). However, the application of the concatenation approach usually failed for recent rapid diversification where lack of monophyly of the same species and gene tree discordance among loci are prevalent (Maddison and Knowles, 2006). In recent years, several species tree approaches, which applied the multispecies coalescent to model lineage divergence process, have been developed (Heled and Drummond, 2010, Liu, 2008, Liu et al., 2009). Despite different modeling strategies, these coalescent-based species tree methods all estimate species trees by accounting for gene tree discordance (Heled and Drummond, 2010) and have been shown to be superior to traditional concatenation approaches when lineages diverged rapidly and gene trees conflicted among loci (Belfiore et al., 2008, Carstens and Knowles, 2007, Degnan and Rosenberg, 2009). Although these coalescent-based species tree methods have been proved to be successful in resolving recent species radiations (Belfiore et al., 2008, Carstens and Knowles, 2007, Cranston et al., 2009), their applications to ancient rapid radiations are still lacking.
The tribe Oryzeae is composed of 11 genera and ∼70 species and includes several economically important species such as Asian and African cultivated rice (Oryza sativa and Oryza glaberrima, respectively), some Leersia species as forage resources and the Zizania species (wild rice) as cuisine in China and North America (Johnson, 1969, Vaughan, 1994). The valuable germplasm for rice breeding in this tribe includes not only close relatives of cultivated rice (e.g., the A-genome species), but also distant relatives such as Zizania latifolia which has been utilized to generate rice introgression lines for potential breeding application (Dong et al., 2006). Furthermore, given the completion of the whole genome sequencing of three rice cultivars (Goff et al., 2002, Wang et al., 2014, Yu et al., 2002) and well established genomic resources for Oryza (Kim et al., 2008), tribe Oryzeae has become an increasingly attractive system for evolutionary genetic and genomic studies (Ai et al., 2012, Jacquemin et al., 2014, Yang et al., 2009, Zou et al., 2008). Obviously, a clear and reliable phylogenetic framework is essential to various investigations using rice and its relatives as the study system (Kellogg, 2009).
Given its economic and theoretical significance, the tribe Oryzeae has been extensively investigated in terms of evolutionary history using various data, including morphology (Martínez-y-Pérez et al., 2006, Martínez-y-Pérez et al., 2008, Terrell et al., 2001), cytology (Nayar, 1973), and molecular markers (Duvall et al., 1993, Ge et al., 2002, Guo and Ge, 2005, Zeng et al., 2012, Zhang and Second, 1989). These studies confirmed the monophyly of Oryzeae and its division of two subtribes (Oryzinae and Zizaniinae). Although the phylogeny of the subtribe Oryzinae has been well resolved (Ge et al., 2002, Guo and Ge, 2005, Tang, 2009), the phylogenetic relationship of the major lineages in the subtribe Zizaniinae has not been established reliably until Tang et al. (2010) conducted the most comprehensive phylogenetic and biogeographic analyses by sampling all the genera in this tribe. Based on the concatenation analysis of 20 chloroplast fragments, Tang et al. (2010) successfully reconstructed the Zizaniinae phylogeny and estimated that the subtribe Zizaniinae started to diverge during the early Miocene (∼21 MYA) and evolved rapidly into 5 lineages in less than 3 MY. On this basis, Tang et al. (2010) proposed that an ancient rapid radiation occurred during the early diversification of Zizaniinae, which might be responsible for low resolution in previous phylogenetic analyses (Ge et al., 2002, Guo and Ge, 2005, Terrell et al., 2001). Nevertheless, the hypothesis of rapid radiation in the subtribe Zizaniinae has not been tested by nuclear genes. In addition, the basal lineages of Zizaniinae and the systematic position of the genus Hygroryza are inconsistent among different studies and need further investigation (Guo and Ge, 2005, Tang et al., 2010).
In the present study, we sequenced 13 single-copy nuclear genes for nine species representing all seven genera of the subtribe Zizaniinae. In conjunction with the concatenated intergenic sequences of chloroplast DNA generated by Tang et al. (2010) and one additional nuclear gene GPA1 published in Guo and Ge (2005), we inferred the species tree of Zizaniinae using three recently developed species tree methods. Specifically, we aimed to address the following questions: (1) Do multiple independent nuclear genes support the ancient radiation hypothesis of the subtribe Zizaniinae as implicated by previous chloroplast analysis? (2) Could the phylogeny of Zizaniinae be fully resolved by multilocus data? (3) Would the species tree approaches achieve better resolution within Zizaniinae than traditional concatenation analysis?
Section snippets
Plant species and nuclear genes sampled
We sampled nine species representing all seven genera of the subtribe Zizaniinae including three monotypic genera endemic to a specific region, i.e., Hygroryza (Asia), Potamophila (Australia), and Rhynchoryza (South America) (Tang et al., 2010). The genus Zizania consists of four species and is distributed disjunctively in Asia and North America. One species from North America (Zizania aquatica) and one from Asia (Z. latifolia) were included. For the genus Chikusichloa, which is distributed in
Sequence characteristics
We successfully obtained the sequences of 14 nuclear genes from nine representative species of Zizaniinae and the outgroup Oryza rufipogon. The aligned length ranged from 659 base pair (bp) (R1047) to 1118 bp (O1_3), with variable sites ranging from 18.42% (Adh1,) to 44.27% (B4_4) and informative sites from 5.46% (Adh1) to 17.45% (R22) (Table1). The GC content of these loci varied between 36.7% (O1_1) and 48.6% (Adh1), without significant difference in base frequency among the Zizaniinae
Phylogenetic analyses of multiple loci confirmed the ancient rapid radiation in Zizaniinae
The individual gene trees of the subtribe Zizaniinae are characterized by widespread discordance in topologies and low resolution of short interior branches of the phylogeny (Fig. 1). Such discordance could result from various reasons, including model misspecification, insufficient variation or substitution saturation, incomplete lineage sorting, hybridization and introgression, as well as gene duplication and loss (Degnan and Rosenberg, 2009, Maddison, 1997, Nakhleh, 2013). Our additional
Acknowledgments
We acknowledge the International Rice Research Institute (Los Banos, Philippines) for providing seed and leaf samples. This work was supported by the National Natural Science Foundation of China (NSCF Grant Nos. 30990240 and 31301747).
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These authors contributed equally to this work.