Complete chloroplast genome sequences of two endangered Phoebe (Lauraceae) species
© The Author(s) 2017
Received: 12 May 2017
Accepted: 20 August 2017
Published: 13 September 2017
Phoebe (Lauraceae) comprises of evergreen trees or shrubs with approximately 100 species, distributed in tropical and subtropical Asia and Neotropical America. A total of 34 species and three varieties occur in China. Despite of economic and ecological value, only limited genomic resources are available for this genus.
We sequenced the two complete chloroplast (cp) genomes of Phoebe chekiangensis and P. bournei using Illumina sequencing technology via a combined strategy of de novo and reference-guided assembly. We also performed comparative analyses with the cp genomes of P. sheareri and P. sheareri var. oineiensis previously reported. The chloroplast genomes of P. chekiangensis and P. bournei identically contain 112 genes consisting of 78 protein coding genes, 30 tRNA genes, and 4 rRNA genes, with the size of 152,849 and 152,853 bp, respectively. From the two chloroplast genomes, 131 SSRs were identified and 12 different SSRs located in five protein coding genes. The analysis showed the extremely conserved structure of chloroplast genomes with surprisingly little variations at the LSC/IR and SSC/IR boundaries. Moreover, the mean nucleotide diversity was found to be 0.162% for 77 regions, suggesting an extraordinarily low level of sequence divergence. Four highest divergent regions (trnH-psbA, rps14-trnT, petA-psbJ, ccsA-ndhD) with the percentage of nucleotide diversity higher than 0.50% were identified, which had potential use for species identification and phylogenetic studies.
This study will facilitate our understanding of population genetics, phylogenetic relationship and plant evolution of Phoebe species.
Phoebe is a genus of evergreen trees or shrubs belonging to family, Lauraceae. Phoebe comprises of approximately 100 species, distributed in tropical and subtropical Asia and neotropical America. A total of 34 species and three varieties are endemic to China (Wu et al. 2008). Phoebe species, with their high-quality wood, were widely used to make column during palace construction in the Ming and Qing dynasties and built high valuable furniture which stood for the power and status of the noble (Ding et al. 2015). The most famous and valuable Phoebe wood are called ‘wood with golden wire’, which comes from several specific and sporadically distributed rare Phoebe species, endemics to China, including Phoebe chekiangensis, Phoebe bournei, Phoebe sheareri, Phoebe zhennan, and Phoebe lichuanensis. Our target species, P. chekiangensis is distributed in Zhejiang and its adjacent areas (including Fujian, Jiangxi, and Anhui Province), whereas P. bournei is distributed in Yangtze River Basin and its south region in China. The Phoebe species have a very high economic and ecological value but with extremely limited studies on biochemical compound and population diversity (Hegde et al. 1997; Zhang et al. 2012a, b).
The chloroplast (cp) is an important organelle that plays a key role in plant photosynthesis providing energy to green plants and carbon fixation (Douglas 1990). With the rapid development of next-generation sequencing, it is now cheaper and faster to obtain genomes than by traditional Sanger sequencing. Therefore, cp genome-scale data have been increasingly used to infer phylogenetic relationships at high taxonomical levels, and even in lower taxa (Moore et al. 2007; Parks et al. 2009; Huang et al. 2014; Yang et al. 2017; Zeng et al. 2017). Although the cp genome is more conserved than the nuclear genome in plants, many mutation events in the chloroplast DNA sequence have been identified, including indels, substitutions, and inversions (Ingvarsson et al. 2003). Most angiosperm cp genomes have a quadripartite circular structure ranging from 115 to 165 kp in length, and are composed of two copies of inverted repeat (IR) regions that are separated by a large single copy (LSC) region and a small single copy (SSC) region (Wicke et al. 2011; Wang et al. 2015). Massive information for genetics, taxonomy, and phylogeny could be mined from cp genomes, because of their relatively conserved gene structure and sequence divergence between species and individuals (Parks et al. 2009; Huang et al. 2014). Furthermore, cp genomes can provide effective genetic markers for evolutionary studies from population level. In addition, analyzing the composition and structure of the cp genomes for such an important genus Phoebe can explore further genetic variations, which could improve quantitative and quality traits.
In this study, we reported the complete and annotated DNA sequences for the cp genomes of P. chekiangensis and P. bournei using next-generation sequencing platform, which is also the first comprehensive analysis on cp genomes for Phoebe combining the cp genomes of P. sheareri and P. sheareri var. oineiensis previously reported (Song et al. 2016). The specific aims of the present study were to: (1) present the complete chloroplast genome sequences and investigate global structural patterns of P. chekiangensis and P. bournei; (2) examine variations of repeat sequences and simple sequence repeats (SSRs) among the two Phoebe chloroplast genomes; (3) screen sequence divergence hotspot regions in the four Phoebe chloroplast genomes.
Plant material and DNA extraction
Young leaves of P. chekiangensis and P. bournei were sampled from single seedlings growing in the nursery located at 30.21N, 120.02E, of Zhejiang Academy of Forestry. The provenance was Hangzhou, Zhejiang Province and Mingxi, Fujian Province, PR China, which was the primary distribution area of P. chekiangensis and P. bournei, respectively. Total genomic DNA per species was extracted from 30 mg of the silica-dried leaf using the modified CTAB method (Porebski et al. 1997). The quality and concentration of the genomic DNA were assessed using agarose gel electrophoresis and an Agilent BioAnalyzer 2100 (Agilent Technologies).
Chloroplast genome illumina sequencing, assembly and annotation
Genomic DNA was used to generate short-insert (500 bp) paired-end sequencing libraries according to the Illumina standard protocol. Genomic DNA from each species was sequenced using a HiSeq™ 2000 analyzer (Illumina, San Diego, California, USA) at Beijing Genomics Institute (BGI, Shenzhen, China).The raw reads (20,777,674 and 20,787,108 bp for P. chekiangensis and P. bournei) were generated with 125 bp length and assembled into whole chloroplast genomes in a multi-step approach employing a modified pipeline that involved a combination of both reference guided and de novo assembly approaches. First, paired-end sequence reads were trimmed to remove low-quality bases (Q <20, 0.01 probability error) and adapter sequences using CLC-quality trim tool (quality_trim software included in CLC ASSEMBLY CELL package, http://www.clcbio.com/products/clc-assembly-cell/) before undertaking sequence assembly. Second, the contigs were assembled using CLC de novo assembler with the following optimized parameters: bubble size of 98, minimum contig length of 200, mismatch cost of two, deletion and insertion costs of three, length fraction of 0.9, and similarity fraction of 0.8. Third, all the contigs were aligned to the reference chloroplast genome of Machilus yunnanensis (NC028073) using BLAST (http://blast.ncbi.nlm.nih.gov/), and aligned contigs (≥90% similarity and query coverage) were ordered according to the reference chloroplast genome. Then, contigs were aligned with the reference genome to construct the draft chloroplast genome of each species in Geneious 9.0.5 software (http://www.geneious.com). Finally, clean reads were re-mapped to the draft cp genomes of two Phoebe species, and the mapping ratio were 3.41% for P. chekiangensis and 2.15% for P. bournei, and average coverage depth were 578.2 and 367.1 for P. chekiangensis and P. bournei, respectively. Using the Dual Organellar Genome Annotator (DOGMA) program (Wyman et al. 2004), the two Phoebe chloroplast genomes were annotated. Protein-coding genes were identified by using the plastid/bacterial genetic code. Intron/exon boundaries were further determined using MAFFT v7 with those of the M. yunnanensis chloroplast genomes as a reference (Katoh and Standley 2013). Using the program tRNAscan-SEwith default settings (Schattner et al. 2005), tRNA boundaries were verified. The circular chloroplast genome maps of the Phoebe were drawn using the Organellar Genome DRAW (OGDRAW) software, with subsequent manual editing (Lohse et al. 2007).
Characterization of repeat sequences and SSRs
REPuter was used to visualize both forward, palindrome, reverse and complement repeats, with a minimum repeat size of 30 bp and a sequence identity greater than 90% with hamming distance equal to 3 in P. chekiangensis and P. bournei (Kurtz and Schleiermacher 1999). The SSRs, which usually have a higher mutation rate, are easily genotyped using PCR, used as markers for phylogenetic analysis and in marker-assisted breeding when located on nuclear chromosomes. Microsatellites, or simple sequence repeats (SSRs) were detected using MISA perl script with thresholds of ten repeat units for mononucleotide SSRs, five repeat units for dinucleotide SSRs, four repeat units for trinucleotide SSRs, and three repeat units for tetra-, penta-, and hexanucleotide SSRs (Thiel et al. 2003).
Divergence hotspot identification
The four complete chloroplast genome sequences (P. chekiangensis, P. bournei, P. sheareri, and P. sheareri var. oineiensis) were aligned,using the chloroplast genome of M. yunnanensis as a reference by mVISTA program (Frazer et al. 2004). Default parameters were utilized to align the chloroplast genomes in Shuffle-LAGAN mode and a sequence conservation profile was visualized in an mVISTA plot. To discover the divergence hotspot regions in Phoebe, protein coding gene, intron, and intergenic spacer region were evaluated with DnaSP 5.10 (Librado and Rozas 2009). All the regions were sequentially extracted under the following criteria: (1) total number of mutation (Eta) >0; (2) an aligned length >200 bp. Any large structural events, such as gene order rearrangements and IR expansions/contractions, were recorded.
Chloroplast genomes organization of P. chekiangensis and P. bournei
The basic characteristics of the sequencing data for P. chekiangensis and P. bournei
Average read length
Total cpDNA size (bp)
Length of large single copy (LSC) region
Length of inverted repeat (IR) region
Length of small single copy (SSC) region
Total CDS length
Total tRNA length
Total rRNA length
Total GC content (%)
Total number of genes
SSR and repeat sequences analysis
Inverted repeats (IRs) contraction and expansion of four Phoebe species
Divergence sequence hotspots in Phoebe species
Results from this study showed the GC content of P. chekiangensis and P. bournei chloroplast genomes is close to that reported in other Lauraceae chloroplast genomes (Song et al. 2015, 2016). Although the GC percentage in the IR regions (44.4%) of the two Pheobe was higher than that of Nicotiana otophora (43%) (Asaf et al. 2016), the presence of rRNA in Pheobe (four) was lower than that of N. otophora (eight). The results in this study were incompatible to previous report which suggested that a high GC percentage in the IR regions could be due to the presence of rRNA (Qian et al. 2013). Similarly, 112 different genes, including 78 protein-coding genes (47 genes encoding photosynthesis-related proteins, four DNA dependent RNA polymerases, 20 ribosomal proteins, one translation initiation factor, four genes encoding other proteins, and two genes of unknown function), 30 tRNA genes, and four rRNA genes were annotated in P. chekiangensis and P. bournei chloroplast genomes (Fig. 1; Additional file 4). The pattern of protein coding genes was similar to that of Persea americana (Song et al. 2016). Among all the protein-coding genes, ten genes possessed a single intron, two genes (ycf3 and clpP) contain two introns, whereas six tRNA genes contain a single intron (Additional file 4).
Overall, a total of 71 repeats, including 36.6% forward repeats (26), 40.8% palindromic repeats (29), 16.9% reverse repeats (12), and 5.7% complement repeats (4), were detected in P. chekiangensis and P. bournei chloroplast genomes. About 61.07% of these repeats were distributed in intergenic spacer. The result was comparable to chloroplast genomes of most angiosperm plant (Uthaipaisanwong et al. 2012; Yao et al. 2015). Previous studies suggested that the presence of these repeats indicates that the region is a crucial hotspot for genome reconfiguration (Gao et al. 2009). One 30 bp forward repeat occurred in the ndhC-trnV intergenic spacer and one 30 bp palindromic repeat in Ψycf1 were unique to P. chekiangensis. In contrast, one 31 bp forward repeat occurred in the ndhC-trnV intergenic spacer were only contained by P. bournei (Additional file 1). Apart from the above three repeats, the others were shared between two Phoebe species. SSRs in the chloroplast with high polymorphism in copy numbers have been recognized as one of the main sources of molecular markers, and extensively used for population genetics and phylogenetic investigation (Pauwels et al. 2012; Zhang et al. 2012a, b; Zhao et al. 2015).
Among 131 SSRs longer than 10 bp, almost all mononucleotide was composed of A/T (97.7%), and majority of dinucleotides was composed of AT (60.0%). The AT richness in SSRs of the two Pheobe genome was similar to previous reports suggesting that SSRs found in the chloroplast genome were generally composed of polythymine (T) or polyadenine (A) repeats, and infrequently contained tandem cytosine (C) and guanine (G) repeats (Kuang et al. 2011; Qian et al. 2013; Chen et al. 2015). The SSRs identified in the two Phoebe species might be used in future population genetic studies as well as similar studies of other species, such as Panax ginseng (Kim and Lee 2004), Cucumis sativus (Kim et al. 2006), Vigna radiate (Tangphatsornruang et al. 2010), and Pyrus pyrifolia (Terakami et al. 2012).
Based on the analysis of inverted repeats contraction and expansion, a conclusion could be drawn that chloroplast genomes of four Phoebe species exhibited comparatively little difference at the IR/LSC and IR/SSC boundary regions, which was similar in Veroniceae (Choi et al. 2016). The genetic divergence within Lauraceaeis surprisingly low (Rohwer 2000; Song et al. 2016). The mean nucleotide diversity of the complete chloroplast genome of the four Phoebe species was only 0.162%, lower than that of two Panax species (0.40%) (Dong et al. 2014), three Veroniceae species (0.40%) (Choi et al. 2016), and nine Gossypium species (0.62%) (Xu et al. 2012), and extremely lower than that of five Epimedium species (3.97%) (Zhang et al. 2016). Molecular markers with nucleotide diversity over 1.5% have been reported before as highly variable regions and could be used to promote the further phylogenetic analysis and species identification in other seed plants (Särkinen and George 2013; Korotkova et al. 2014; Huang et al. 2014). However, due to the relative conservative of chloroplast genomes of Phoebe species, the quantity of the regions with nucleotide diversity exceeding 0.5% was only four, whereas in Nicotiana (Asaf et al. 2016), the quantity of the regions with nucleotide diversity over 0.7% was 15, and in Machilus (Song et al. 2015), the quantity of the regions with nucleotide diversity over 0.8% was 7. In this study, the highest nucleotide diversity was 1.389% (ccsA-ndhD), followed by 0.887% (petA-psbJ), 0.716% (rps4-trnT), and 0.506% (trnH-psbA). Therefore, only the above four regions with nucleotide diversity higher than 0.5% probably had the potential use for phylogeographic analyses and plant identification of Phoebe species.
The 77 repeat sequences were identified in the Phoebe chloroplast genomes. The analysis showed the extremely conserved structure of chloroplast genomes, the mean nucleotide diversity was found to be 0.162% for 77 regions, suggesting an extraordinarily low level of sequence divergence. Four highest divergent regions (trnH-psbA, rps14-trnT, petA-psbJ, ccsA-ndhD) were also identified, which might be useful in species identification and phylogenetic studies. Overall, this study will facilitate our understanding of population genetics, phylogenetic relationship and plant evolution of Phoebe species.
LYG, XWQ and LXH conceived and designed the experiment; ZWT and JDY contributed to the sampling; XWQ and LYG performed the experiment and analyzed the data. The manuscript was written by LYG. All authors read and approved the final manuscript.
We thank Yingxiong Qiu, Ruisen Lu, Shanshan Zhu of Zhejiang University for providing experiment design and laboratory support.
The authors declare that they have no competing interests.
Availability of data and materials
All data are deposited in NCBI.
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This work was supported by the Major Science and Technology Program (No. 2010C12009), Key Research & Development Program (No. 2017C02028) of Zhejiang Province, and National Key Research & Development Program (No. 2016YFD0600603) of China.
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