Phylogenetics and Dispersal Patterns of Brassicaceae Around the Qinghai–Tibet Plateau
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Journal of Systematics JSE and Evolution doi: 10.1111/jse.12312 Research Article Phylogenetics and dispersal patterns of Brassicaceae around the Qinghai–Tibet Plateau Chaoju Qian1,2, Yong Shi1, Yuan Liu1, Xia Yan1,3*, and Xiao-Fei Ma1* 1Key Laboratory of Stress Physiology and Ecology in Cold and Arid Regions, Gansu Province, Department of Ecology and Agriculture Research, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou 730000, China 2University of Chinese Academy of Sciences, Beijing 100049, China 3Key Laboratory of Eco-hydrology of Inland River Basin, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou 730000, China *Authors for correspondence. E-mail: X-F Ma, [email protected]; X Yan, [email protected]. Received 29 September 2016; Accepted 13 March 2018; Article first published online 3 May 2018 Abstract Brassicaceae, one of the most diverse and economically valuable plant families, is distributed all over the world. Previous studies have suggested that Brassicaceae originated and diversified in the Old World. In this study, the phylogenetic relationships of 17 tribes of Brassicaceae from the Qinghai–Tibet Plateau (QTP) and adjacent areas were investigated using nuclear ribosomal internal transcribed spacer (nrITS) and chloroplast DNA sequence data (rbcL and petB-petD) with maximum likelihood, maximum parsimony, and Bayesian methods. As suggested by both the nrITS and chloroplast DNA trees, Cardaria pubescens (C.A.Mey.) Jarm. (Lepidieae) and Draba lanceolata Royle (Arabideae) should be classified in the Eutremeae and Cardamineae, respectively. Based on over 700 newly sequenced and published nrITS sequences of Brassicaceae, an up-to-date comprehensive phylogeny of the family was reconstructed using the maximum likelihood method. In the phylogenetic tree, 10 monophyletic tribes were detected. They were used to clarify the lineage diversification and dispersal patterns of the 10 tribes. The results showed that most of the monophyletic tribes may have originated in different regions of the world, and then dispersed into other regions surrounding the QTP. Rapid lineage diversification rate shifts were detected in several tribes, such as Anastaticeae, which experienced a rapid shift event 1.38 Mya, corresponding to the rapid uplift of the QTP, indicating that the recent uplift of the QTP could have promoted diversification in Brassicaceae across and adjacent to the QTP. Key words: Brassicaceae, dispersal pattern, eastern Asia, phylogenetic relationship, Qinghai-Tibet Plateau (QTP). 1 Introduction Alysseae was classified in Lineage I based on PISTILLATA first intron sequences, but it was placed in a different lineage The Brassicaceae comprise 3700 species assigned to 321 (Lineage III) based on trnS(GCU)-trnG(UUC) sequences (Liu et al., genera in 51 tribes, including 22 species in 15 genera that have 2011). Due to frequent interspecific and intergeneric hybrid- not yet been classified into any tribe (Al-Shehbaz et al., 2006, ization within Brassicaceae, whole-genome duplications, and 2014; German et al., 2014; Kiefer et al., 2014). In addition to its rapid adaptive radiation events in their early evolutionary species richness, the family is also of special interest for its history (Al-Shehbaz et al., 2006; Koch et al., 2007; Franzke high economic and scientific value, including many important et al., 2009; Couvreur et al., 2010; Tsuda et al., 2014; Huang vegetable crops (e.g., Brassica and Raphanus), sources of et al., 2016), a clear understanding of the phylogenetic industrial oils and spices (e.g., Brassica, Armoracia, and relationships within the family has not been achieved. Sinapis), several medicinal herbs (e.g., Rorippa and Erysimum), Previous studies (Lysak & Koch, 2011) have documented and the model plant Arabidopsis thaliana (L.) Heynh. The that crucifers are widely distributed in mountainous and phylogenetic relationships in the family have been the focus of alpine regions worldwide, except in Antarctica. Based on interest of numerous scholars. Starting in the early 1990s, with species diversity, it is speculated that the Brassicaceae the advancement of molecular technology and the use of originated in the Irano-Turanian region, which is one of the additional markers for classification, some genera that were major diversification centers, with approximately 900 species originally based on morphology were suggested to be non- in approximately 150 genera (Franzke et al., 2009). The level of monophyletic (Al-Shehbaz et al., 2006). Furthermore, molec- diversification is also high in the Mediterranean region of ular markers have also suggested discordant phylogenetic Europe, central and western Asia, and western North America relationships within the Brassicaceae (Couvreur et al., 2010; (Al-Shehbaz, 2011). As a major biodiversity hotspot, with Liu et al., 2011; Huang et al., 2016). For example, the tribe approximately 180 species of Brassicaceae in 76 genera, the © 2018 Institute of Botany, Chinese Academy of Sciences May 2018 | Volume 56 | Issue 3 | 202–217 Dispersal of Brassicaceae around QTP 203 Qinghai–Tibet Plateau (QTP) has also been considered to be TTT; petD-R, GGTTCACCAATCATTGATGGTTC; and ITS1, TCCG another distribution center (Zhou et al., 1987; Wang et al., TAGGTGAACCTGCGG; ITS4, TCCTCCGCTTATTGATATGC. The 2006). Numerous studies have reported that the uplift of the polymerase chain reaction (PCR) was carried out using 2 QTP played an important role in the rapid diversification and Taq Plus high-fidelity PCR Master Mix (Tiangen Biotech) in a biogeographic histories of many plant genera (Liu et al., 2006; Gene-Amp PCR system 9700 DNA Thermal Cycler (PE Applied Wen et al., 2014; Yu et al., 2014a; Zhang et al., 2014). Although Biosystems, Norwalk, CT, USA) with initial denaturation at the phylogenetic relationships among the Brassicaceae in 95 °C for 4 min, followed by 35 cycles of 95 °C for 30 s, 56– China have been investigated (Liu et al., 2011), most of the 60 °C for 1 min, 72 °C for 1 min, and a final extension of 72 °C for samples were collected in Yunnan and Xinjiang provinces. 10 min. The DNA products were purified using TIANquick Midi They may not reflect how the uplift of the QTP influenced the Purification Kits (Tiangen Biotech) and were subsequently dispersal and diversification of the Brassicaceae. sequenced with the corresponding forward and reverse In our study, we aimed to better understand the primers on an ABI 3130xl Genetic Analyzer (PE Applied phylogenetic relationships and dispersal patterns within the Biosystems) using the ABI Prism BigDye Terminator Cycle Brassicaceae and to determine the role played by the uplift of version 3.1 (PE Applied Biosystems). the QTP based on samples collected in this and previous studies. Using DNA sequence variation of two maternally 2.3 Sequence analysis inherited plastid DNA markers (Corriveau & Coleman, 1988) All DNA sequences were manually verified with BioEdit version and a bi-parentally inherited nuclear ribosomal internal 7.1.3 (Hall, 1999) after alignment using muscle (available transcribed spacer (nrITS) region, we tried to reconstruct a online: http://www.ebi.ac.uk/Tools/msa/muscle/). The chloro- more complete phylogenetic tree of the Brassicaceae around plast supergene was concatenated from the two chloroplast the QTP region with increased taxon sampling. Using DNA (cpDNA) fragments using DnaSP version 5.10.01 (Librado phylogeny as the basis and beast version 1.8.0 (Drummond & Rozas, 2009). The heterozygous sites of the nrITS & Rambaut, 2007) and rasp (Yu et al., 2014b), we inferred the sequences (Aguilar & Feliner, 2003) were separated with divergence time and dispersal pattern for each monophyletic phase (Stephens et al., 2001), which was integrated in DnaSP. tribe, not only in the QTP region, but also in neighboring To facilitate further analysis, all the indels were coded by regions. By analyzing the divergence and dispersal patterns of GapCoder (Young & Heal, 2003). The newly obtained the monophyletic tribes of Brassicaceae, we hoped to sequences were deposited in GenBank with accession determine whether the pattern of lineage diversification numbers KX824451–KX824660. and spread was correlated with the uplift of the QTP. 2.4 Phylogenetic analysis and phylogenetic network Two datasets, nrITS and the cpDNA supergene, were analyzed 2 Material and Methods using maximum likelihood (ML), maximum parsimony (MP) and Bayesian inference (BI) methods, with the genera Cleome L. and 2.1 Material sampling Capparis L. as outgroups. The best-fit models for the nucleotide Sixty-eight accessions, including samples from 24 genera dataset were identified with jModelTest version 0.1.1 (Posada, (31.6% of all samples distributed around the QTP) of 17 tribes 2008) based on Akaike Information Criterion values, and the (Alysseae, Lepidieae, Anchonieae, Arabideae, Brassiceae, SYM þ G model and the GTR þ G model were chosen for nrITS Euclidieae, Camelineae, Cardamineae, Chorisporeae, Descur- and cpDNA, respectively. The ML analysis for these two ainieae, Dontostemoneae, Erysimeae, Eutremeae, Anastati- datasets was carried out using PhyML version 3.0 (Guindon & ceae, Stevenieae, Sisymbrieae, and Thlaspideae; Table 1) of Gascuel, 2003), with 500 bootstraps under the best-fit model. Brassicaceae were collected from eight provinces (Gansu, The MP analysis was also carried out in paupà version 4.0b10 Xinjiang, Yunnan, Hebei, Neimenggu, Qinghai, Ningxia, and (Swofford, 2001) for both datasets. A heuristic search was Shanxi)