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Phylogenetic Reconstruction and Diversification of the Triticeae

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Phylogenetic Reconstruction and Diversification of the Triticeae Biochemical Systematics and Ecology 50 (2013) 346–360 Contents lists available at SciVerse ScienceDirect Biochemical Systematics and Ecology journal homepage: www.elsevier.com/locate/biochemsyseco Phylogenetic reconstruction and diversification of the Triticeae (Poaceae) based on single-copy nuclear Acc1 and Pgk1 gene data Xing Fan a,b, Li-Na Sha a, Shuang-Bin Yu a, Dan-Dan Wu a, Xiao-Hong Chen a, Xiao-Feng Zhuo a, Hai-Qin Zhang a, Hou-Yang Kang a, Yi Wang a, You-Liang Zheng a,b, Yong-Hong Zhou a,b,* a Triticeae Research Institute, Sichuan Agricultural University, Wenjiang 611130, Sichuan, China b Key Laboratory of Crop Genetic Resources and Improvement, Ministry of Education, Sichuan Agricultural University, Yaan 625014, Sichuan, China article info abstract Article history: Two single-copy nuclear gene (Acc1 and Pgk1) sequences were used to estimate the phy- Received 23 March 2013 logeny and diversification patterns of the Triticeae. Phylogenetic analyses and diversification Accepted 18 May 2013 patterns suggested that (1) a major radiation occurring in the Triticeae about 6.1–9.2 MYA Available online might have been triggered by the late Miocene climate oscillations; (2) the Triticeae lineages from Mediterranean and Arctic-temperate regions were evolutionarily distinct; (3) the Keywords: relationship between Thinopyrum bessarabicum and Triticum/Aegilops is more closely than Triticeae that between Lophopyrum elongatum and Triticum/Aegilops;(4)Pseudoroegneria is closely Phylogeny Diversification related to Australopyrum and Lophopyrum;(5)Australopyrum might originate from coloni- Monogenomic genera zation via South-east Asia during the late Miocene; (6) Habitats, mating systems, and climate Climate oscillations oscillations may associated with the diversification rate shifts leading to the majority of Mediterranean lineage. Diversification rate shifts in Mediterranean lineage of the Triticeae not only spur the occurrence of many endemic lineages but also provide opportunity for polyploid crop origin and domestication. Ó 2013 Elsevier Ltd. All rights reserved. 1. Introduction Determining what processes have driven species diversification and diversity is a central goal of evolutionary and con- servation biologists. The forces acting on species richness may apply at different latitudes or biogeographic regions, indicating the importance of historical processes (e.g. dispersal events, and local speciation and extinction regimes) in mediating the environment–diversity relationship (Qian et al., 2009; Kisel et al., 2011). Theoretical and empirical investigation emphasized that historical climate fluctuations are a key factor promoting species diversification and distribution (Currie, 1991; Pearson and Dawson, 2003; Clarke and Gaston, 2006; Lavergne et al., 2010). Recent studies combining an effect of historical climatic variability with time-calibrated phylogenies suggested that variation in global climate determined the distribution, richness and diversity of plant clades, hence, indirectly influenced plant diversification (Egan and Crandall, 2008; Nyman et al., 2012). * Corresponding author. Triticeae Research Institute, Sichuan Agricultural University, Wenjiang 611130, Sichuan, China. E-mail address: [email protected] (Y.-H. Zhou). 0305-1978/$ – see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.bse.2013.05.010 X. Fan et al. / Biochemical Systematics and Ecology 50 (2013) 346–360 347 The wheat tribe (Poaceae: Triticeae), an economically important gene pool for genetic improvement of cereal and forage crops, includes about 450 diploid and polyploid species that distribute in a wide range of ecological habitats over the temperate and subtropical and tropic alpine regions (Dewey, 1984). In the Triticeae, 24 major basic genomes donated by diploid species have been designated and were recognized in eighteen monogenomic genera (Löve, 1984; Wang et al., 1994). Many basic genomes (e.g. A, B, D, Ns, Xm, E, St, Y, H, P, W) in various combinations (e.g. AB, ABD, NsXm, StE, StH, StY, StYH, StYP, StYW) constitute polyploid species, about 75% of the Triticeae species (Lu, 1994). Monogenomic genera have been the focus of numerous phylogenetic investigations, partly because of its economic importance (which includes barley, rye, and crested- wheat grasses), and partly because of its genome donor to the speciation of polyploid species, as well as partly because of its wide variety of species richness, morphology, ecology and distribution. It was not considered that genomic analysis can reveal a phylogeny of the monogenomic genera (Kellogg, 1989; Kellogg et al., 1996; Petersen and Seberg, 1997; Seberg and Petersen, 1998). Attempts to sort out the phylogenetic details of the monogenomic genera, phylogenetic reconstructions were carried out based on morphological characteristics (Seberg and Frederiksen, 2001), chloroplast genes (Mason-Gamer et al., 2002), internal transcribed spacers (ITS) sequences (Hsiao et al., 1995), highly repetitive nuclear DNA (Kellogg and Appels, 1995), single-copy nuclear genes (Petersen and Seberg, 1997; Helfgott and Mason-Gamer, 2004; Mason-Gamer, 2005), and multiple gene combined data (Escobar et al., 2011). No consensual definition of clades, however, has been received due to either phylogenetic tree inferred from a limited number of genes (Petersen and Seberg, 1997; Hsiao et al., 1995; Kellogg and Appels, 1995; Helfgott and Mason-Gamer, 2004; Mason-Gamer, 2005) or limited sample (Kellogg and Appels, 1995; Escobar et al., 2011) or introgression events and/or incomplete lineage sorting of ancestral polymorphisms (Mason-Gamer, 2005; Escobar et al., 2011). With the data accumulating on members of the Triticeae, the origin and diversification of the tribe have received attention. Data from natural distribution speculated that the tribe originated about in the middle of the Tertiary period (20–30 MYA), and the first step of phylogenetic diversification in the Triticeae was occurred at the diploid level (Sakamoto, 1973). Morphological analyses presumed that the general evolution of the Triticeae has been defined by divergence at the diploid level from a common diploid ancestor (West et al., 1988). Kellogg et al. (1996) hypothesized that the common ancestor of the Triticeae had a spicate inflorescence with three spikelets per node and gave rise to lineages leading to present-day Psa- thyrostachys and Hordeum. Molecular dating suggested that the divergence between Aegilops/Triticum lineage and barley range from 15 to 10 MYA (million years ago) (Gaut, 2002; Huang et al., 2002; Dvorak and Akhunov, 2005), and the diploid Triticum and Aegilops progenitors of the A, B, D, G and S genomes all radiated about 4.5 MYA (Huang et al., 2002). While these studies add to our understanding of origin of the Triticeae, little is known about the processes driving species diversification and diversity within the Triticeae. Moreover, a complete picture of evolutionary history within the tribe is needed. In this study, we carried out phylogenetic reconstructions and molecular dating using two unlinked nuclear gene (Acc1 and Pgk1) sequences for 31 species of 17 monogenomic genera within the Triticeae. Chromosome mapping indicate that a single copy of the Acc1 gene is present in each of the group 2 homoeologous chromosomes in hexaploid wheat (Gornicki et al., 1997). Analysis of the Pgk1 gene showed that it is present as a single copy per diploid chromosome in grass, and a single copy of the Pgk1 gene is present in each of the group 3 homoeologous chromosomes in hexaploid wheat (Huang et al., 2002). The objectives were: (1) to reconstruct the phylogeny of the Triticeae, especially the time-calibrated phylogeny of the tribe; (2) to document the divergence history within this tribe; (3) to estimate the diversification pattern and process of the Triticeae species. 2. Materials and methods 2.1. Taxon sampling A total of 31 diploid taxa representing 18 basic genomes are used in this study. While generic definitions within the Triticeae have been extremely variable (Barkworth, 2000), this sample represents nearly all of the monogenomic genera accepted in genome-based classifications of the tribe. Acc1 and Pgk1 sequences of Aegilops/Triticum group, Secale, and Hor- deum vulgare were obtained from the data reported by Huang et al. (2002). The remaining sequences of the Triticeae, along with Bromus inermis were obtained from our published data (Fan et al., 2009, 2012). Plant material with sample information and GenBank identification numbers are listed in Table S1. 2.2. Data analysis The Acc1 and Pgk1 sequences were edited using SeqMan (DNASTAR package, Inc. Madison, Wisconsin) and adjusted manually where necessary. The basic sequence statistics, including nucleotides frequencies, transition/transversion ratio and variability in different regions of the sequences were examined by MEGA3 (Kumar et al., 2004). The partition homogeneity test, implemented in the program PAUP*4.0b10 (Swofford D L, Sinauer Associates, http://www.sinauer.com) was used to determine whether the Acc1 and Pgk1 genes contained significantly different signals. The partition homogeneity test can generate significant results if one gene has experienced many multiple substitutions or contains random information. The result of the partition homogeneity test showed that the sequence data sets for the Acc1 and Pgk1 loci were congruent (P ¼ 0.1000) and could therefore be combined for purposes of estimating the phylogeny and diversification pattern of the Triticeae. 348 X. Fan
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