Abstract
Podocarpus latifolius [(Thunb.) R.Br. ex Mirb.], also known as real yellow wood, is a large evergreen tree with exceptionally high-quality wood. It is a member of the Podocarpaceae family, which includes many species widely grown for wood pulp as well as timber for construction. Despite its importance, studies focusing on its genetic characterization and molecular biology are limited. Therefore, this study reports the complete plastome of P. latifolius, which is a circular molecule of 134 020 base pairs (bp) in length, lacking a quadripartite structure. The P. latifolius plastome encodes 117 unique genes, consisting of 82 protein-coding genes, 31 transfer RNA genes and four ribosomal RNA genes. The analysis showed that the Podocarpaceae plastomes have experienced some intron and gene losses, inversions, and inverted repeat (IR) loss resulting in a diverse plastome organization at the species and genus levels. Therefore, to understand the extent of these genomic rearrangements, more sampling of the Podocarpaceae plastomes is necessary. A total of 149 editing sites were predicted in 28 genes, all of which were C to U conversions. Moreover, a total of 164 simple sequence repeats (SSRs) were identified in the P. latifolius plastome, the majority being mononucleotide repeat motifs with A/T sequence predominance. Overall, the data obtained in this study will be useful for population genetics, evolutionary history and phylogenetic studies of the species in this genus.
Acknowledgments
The authors are thankful to Prof. Jinming Chen for his useful comments and precious remarks on the manuscript. We also thank Dr. Oskar Faix and the anonymous reviewers for their helpful comments.
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: This work was financially supported by the Special Funds for the Young Scholars of Taxonomy of Chinese Academy of Sciences Grants to Liao Kuo (grant no. ZSBR-013) and Sino-Africa Joint Research Center (#Y323771W07 and #SAJC201322).
Employment or leadership: None declared.
Honorarium: None declared.
Conflict of interest statement: The authors declare no conflicts of interest.
References
Abdillahi, H., Stafford, G., Finnie, J., Van Staden, J. (2010) Ethnobotany, phytochemistry and pharmacology of Podocarpus sensu latissimo (sl). S. Afr. J. Bot. 76:1–24.10.1016/j.sajb.2009.09.002Search in Google Scholar
Abdillahi, H., Finnie, J., Van Staden, J. (2011) Anti-inflammatory, antioxidant, anti-tyrosinase and phenolic contents of four Podocarpus species used in traditional medicine in South Africa. J. Ethnopharmacol. 136:496–503.10.1016/j.jep.2010.07.019Search in Google Scholar PubMed
Aerts, R., Thijs, K.W., Lehouck, V., Beentje, H., Bytebier, B., Matthysen, E., Gulinck, H., Lens, L., Muys, B. (2011) Woody plant communities of isolated Afromontane cloud forests in Taita Hills, Kenya. Plant Ecol. 212:639–649.10.1007/s11258-010-9853-3Search in Google Scholar
Asaf, S., Khan, A.L., Khan, M.A., Shahzad, R., Kang, S.M., Al-Harrasi, A., Al-Rawahi, A., Lee, I.-J. (2018) Complete chloroplast genome sequence and comparative analysis of loblolly pine (Pinus taeda L.) with related species. PLoS One 13:e0192966.10.1371/journal.pone.0192966Search in Google Scholar PubMed PubMed Central
Barker, N., Muller, E., Mill, R. (2004) A yellowwood by any other name: molecular systematics and the taxonomy of Podocarpus and the Podocarpaceae in southern Africa. S. Afr. J. Sci. 100:629–632.Search in Google Scholar
Beentje, H.J. Kenya Trees, Shrubs and Lianas. National Museums of Kenya, Nairobi, Kenya, 1994. pp. 42–43.Search in Google Scholar
Bytebier, B. Taita Hills Biodiversity Project Report. National Museums of Kenya, Nairobi, 2001. p. 121.Search in Google Scholar
Celiński, K., Kijak, H., Barylski, J., Grabsztunowicz, M., Wojnicka-Półtorak, A., Chudzińska, E. (2017) Characterization of the complete chloroplast genome of Pinus uliginosa (Neumann) from the Pinus mugo complex. Conserv. Genet. Resour. 9:209–212.10.1007/s12686-016-0652-6Search in Google Scholar
Chaney, L., Mangelson, R., Ramaraj, T., Jellen, E.N., Maughan, P.J. (2016) The complete chloroplast genome sequences for four Amaranthus species (Amaranthaceae). Appl. Plant. Sci. 4:1600063.10.3732/apps.1600063Search in Google Scholar PubMed PubMed Central
Chen, H., Deng, L., Jiang, Y., Lu, P., Yu, J. (2011) RNA editing sites exist in protein-coding genes in the chloroplast genome of Cycas taitungensis. J. Integr. Plant Biol. 53:961–970.10.1111/j.1744-7909.2011.01082.xSearch in Google Scholar PubMed
Chen, T.-C., Liu, Y.-C., Wang, X., Wu, C.-H., Huang, C.-H., Chang, C.-C. (2017a) Whole plastid transcriptomes reveal abundant RNA editing sites and differential editing status in Phalaenopsis aphrodite subsp. formosana. Bot. Stud. 58:38.10.1186/s40529-017-0193-7Search in Google Scholar PubMed PubMed Central
Chen, C., Zheng, Y., Liu, S., Zhong, Y., Wu, Y., Li, J., Xu, L.A., Xu, M. (2017b) The complete chloroplast genome of Cinnamomum camphora and its comparison with related Lauraceae species. PeerJ. 5:e3820.10.7717/peerj.3820Search in Google Scholar PubMed PubMed Central
Chiang, Y.C., Shih, H.C., Chang, L.W., Li, W.R., Lin, H.Y., Ju, L.P. (2011) Isolation of 16 polymorphic microsatellite markers from an endangered and endemic species, Podocarpus nakaii (Podocarpaceae). Am. J. Bot. 98:e306–e309.10.3732/ajb.1100229Search in Google Scholar PubMed
Daniell, H., Lin, C.-S., Yu, M., Chang, W.-J. (2016) Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biol. 17:134.10.1186/s13059-016-1004-2Search in Google Scholar PubMed PubMed Central
Dantas, L.G., Esposito, T., de Sousa, A.C.B., Félix, L., Amorim, L.L., Benko-Iseppon, A.M., Batalha-Filho, H., Pedrosa-Harand, A. (2015) Low genetic diversity and high differentiation among relict populations of the neotropical gymnosperm Podocarpus sellowii (Klotz.) in the Atlantic Forest. Genetica 143:21–30.10.1007/s10709-014-9809-ySearch in Google Scholar PubMed
Darling, A.C., Mau, B., Blattner, F.R., Perna, N.T. (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 14:1394–1403.10.1101/gr.2289704Search in Google Scholar PubMed PubMed Central
Diekmann, K., Hodkinson, T.R., Wolfe, K.H., van den Bekerom, R., Dix, P.J., Barth, S. (2009) Complete chloroplast genome sequence of a major allogamous forage species, perennial ryegrass (Lolium perenne L.). DNA Res. 16:165–176.10.1093/dnares/dsp008Search in Google Scholar PubMed PubMed Central
Dierckxsens, N., Mardulyn, P., Smits, G. (2016) NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res. 45:e18.Search in Google Scholar
do Nascimento Vieira, L., Faoro, H., Rogalski, M., de Freitas Fraga, H.P., Cardoso, R.L.A., de Souza, E.M., de Oliveira Pedrosa, F., Nodari, R.O., Guerra, M.P. (2014) The complete chloroplast genome sequence of Podocarpus lambertii: genome structure, evolutionary aspects, gene content and SSR detection. PLoS One 9:e90618.10.1371/journal.pone.0090618Search in Google Scholar PubMed PubMed Central
do Nascimento Vieira, L., Rogalski, M., Faoro, H., de Freitas Fraga, H.P., dos Anjos, K.G., Picchi, G.F.A., Nodari, R.O., de Oliveira Pedrosa, F., de Souza, E.M., Guerra, M.P. (2016) The plastome sequence of the endemic Amazonian conifer, Retrophyllum piresii (Silba) CN Page, reveals different recombination events and plastome isoforms. Tree Genet. Genomes 12:10.10.1007/s11295-016-0968-0Search in Google Scholar
Doyle, J.J., Doyle, J.L., Palmer, J.D. (1995) Multiple independent losses of two genes and one intron from legume chloroplast genomes. Syst. Bot. 20:272–294.10.2307/2419496Search in Google Scholar
Duan, R.-Y., Yang, L.-M., Lv, T., Wu, G.-L., Huang, M.-Y. (2016) The complete chloroplast genome sequence of Pinus dabeshanensis. Conserv. Genet. Resour. 8:395–397.10.1007/s12686-016-0567-2Search in Google Scholar
Eckenwalder, J. Conifers of the World: Portland. Timber Press Portland, OR, USA, 2009.Search in Google Scholar
Fang, M.-F., Wang, Y.-J., Zu, Y.-M., Dong, W.-L., Wang, R.-N., Deng, T.-T., Li, Z.-H. (2016) The complete chloroplast genome of the Taiwan red pine Pinus taiwanensis (Pinaceae). Mitochondrial DNA Part A 27:2732–2733.10.3109/19401736.2015.1046169Search in Google Scholar PubMed
Fleischmann, T.T., Scharff, L.B., Alkatib, S., Hasdorf, S., Schöttler, M.A., Bock, R. (2011) Nonessential plastid-encoded ribosomal proteins in tobacco: a developmental role for plastid translation and implications for reductive genome evolution. Plant Cell 23:3137–3155.10.1105/tpc.111.088906Search in Google Scholar PubMed PubMed Central
Guo, X., Castillo-Ramírez, S., González, V., Bustos, P., Fernández-Vázquez, J.L., Santamaría, R.I., Arellano, J., Cevallos, M.A., Dávila, G. (2007) Rapid evolutionary change of common bean (Phaseolus vulgaris L) plastome, and the genomic diversification of legume chloroplasts. BMC Genomics 8:228.10.1186/1471-2164-8-228Search in Google Scholar
Guo, W., Grewe, F., Cobo-Clark, A., Fan, W., Duan, Z., Adams, R.P., Schwarzbach, A.E., Mower, J.P. (2014) Predominant and substoichiometric isomers of the plastid genome coexist within Juniperus plants and have shifted multiple times during cupressophyte evolution. Genome Biol. Evol. 6:580–590.10.1093/gbe/evu046Search in Google Scholar
Hansen, D.R., Dastidar, S.G., Cai, Z., Penaflor, C., Kuehl, J.V., Boore, J.L., Jansen, R.K. (2007) Phylogenetic and evolutionary implications of complete chloroplast genome sequences of four early-diverging angiosperms: Buxus (Buxaceae), Chloranthus (Chloranthaceae), Dioscorea (Dioscoreaceae), and Illicium (Schisandraceae). Mol. Phylogenet. Evol. 45:547–563.10.1016/j.ympev.2007.06.004Search in Google Scholar
He, P., Huang, S., Xiao, G., Zhang, Y., Yu, J. (2016) Abundant RNA editing sites of chloroplast protein-coding genes in Ginkgo biloba and an evolutionary pattern analysis. BMC Plant Biol. 16:257.10.1186/s12870-016-0944-8Search in Google Scholar
Hirao, T., Watanabe, A., Kurita, M., Kondo, T., Takata, K. (2008) Complete nucleotide sequence of the Cryptomeria japonica D. Don. chloroplast genome and comparative chloroplast genomics: diversified genomic structure of coniferous species. BMC Plant Biol. 8:70.10.1186/1471-2229-8-70Search in Google Scholar
Jansen, R.K., Raubeson, L.A., Boore, J.L., dePamphilis, C.W., Chumley, T.W., Haberle, R.C., Wyman, S.K., Alverson, A.J., Peery, R., Herman, S.J., Fourcade, H.M., Kuehl, J.V., McNeal, J.R., Leebens-Mack, J., Cui, L. (2005) Methods for obtaining and analyzing whole chloroplast genome sequences. Methods Enzymol. 395:348–384.10.1016/S0076-6879(05)95020-9Search in Google Scholar
Jansen, R.K., Cai, Z., Raubeson, L.A., Daniell, H., Leebens-Mack, J., Müller, K.F., Guisinger-Bellian, M., Haberle, R.C., Hansen, A.K., Chumley, T.W. (2007) Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc. Natl. Acad. Sci. USA 104:19369–19374.10.1073/pnas.0709121104Search in Google Scholar PubMed PubMed Central
Jansen, R.K., Wojciechowski, M.F., Sanniyasi, E., Lee, S.-B., Daniell, H. (2008) Complete plastid genome sequence of the chickpea (Cicer arietinum) and the phylogenetic distribution of rps12 and clpP intron losses among legumes (Leguminosae). Mol. Phylogenet. Evol. 48:1204–1217.10.1016/j.ympev.2008.06.013Search in Google Scholar PubMed PubMed Central
Jiang, M., Chen, H., He, S., Wang, L., Chen, A.J., Liu, C. (2018) Sequencing, characterization, and comparative analyses of the plastome of Caragana rosea var. rosea. Int. J. Mol. Sci. 19:1419.10.3390/ijms19051419Search in Google Scholar PubMed PubMed Central
Jobson, R.W., Qiu, Y.-L. (2008) Did RNA editing in plant organellar genomes originate under natural selection or through genetic drift? Biol. Direct. 3:43.10.1186/1745-6150-3-43Search in Google Scholar PubMed PubMed Central
Karcher, D., Bock, R. (2002) The amino acid sequence of a plastid protein is developmentally regulated by RNA editing. J. Biol. Chem. 277:5570–5574.10.1074/jbc.M107074200Search in Google Scholar PubMed
Keller, J., Rousseau-Gueutin, M., Martin, G.E., Morice, J., Boutte, J., Coissac, E., Ourari, M., Aïnouche, M., Salmon, A., Cabello-Hurtado, F. (2017) The evolutionary fate of the chloroplast and nuclear rps16 genes as revealed through the sequencing and comparative analyses of four novel legume chloroplast genomes from Lupinus. DNA Res. 24:343–358.10.1093/dnares/dsx006Search in Google Scholar PubMed PubMed Central
Khadivi-Khub, A., Zamani, Z., Fattahi, R., Wünsch, A. (2014) Genetic variation in wild Prunus L. subgen. Cerasus germplasm from Iran characterized by nuclear and chloroplast SSR markers. Trees 28:471–485.10.1007/s00468-013-0964-zSearch in Google Scholar
Kim, K.-J., Lee, H.-L. (2004) Complete chloroplast genome sequences from Korean ginseng (Panax schinseng Nees) and comparative analysis of sequence evolution among 17 vascular plants. DNA Res. 11:247–261.10.1093/dnares/11.4.247Search in Google Scholar PubMed
Kumbhar, F., Nie, X., Xing, G., Zhao, X., Lin, Y., Wang, S., Weining, S. (2018) Identification and characterisation of rna editing sites in chloroplast transcripts of einkorn wheat (Triticum monococcum). Ann. Appl. Biol. 172:197–207.10.1111/aab.12412Search in Google Scholar
Langmead, B., Trapnell, C., Pop, M., Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25.10.1186/gb-2009-10-3-r25Search in Google Scholar PubMed PubMed Central
Laslett, D., Canback, B. (2004) ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res. 32:11–16.10.1093/nar/gkh152Search in Google Scholar PubMed PubMed Central
Lin, C.P., Huang, J.P., Wu, C.S., Hsu, C.Y., Chaw, S.M. (2010) Comparative chloroplast genomics reveals the evolution of Pinaceae genera and subfamilies. Genome Biol. Evol. 2:504–517.10.1093/gbe/evq036Search in Google Scholar PubMed PubMed Central
Lin, C.-P., Wu, C.-S., Huang, Y.-Y., Chaw, S.-M. (2012) The complete chloroplast genome of Ginkgo biloba reveals the mechanism of inverted repeat contraction. Genome Biol. Evol. 4:374–381.10.1093/gbe/evs021Search in Google Scholar PubMed PubMed Central
Liu, C., Shi, L., Zhu, Y., Chen, H., Zhang, J., Lin, X., Guan, X. (2012) CpGAVAS, an integrated web server for the annotation, visualization, analysis, and GenBank submission of completely sequenced chloroplast genome sequences. BMC Genomics 13:715.10.1186/1471-2164-13-715Search in Google Scholar PubMed PubMed Central
Lohse, M., Drechsel, O., Bock, R. (2007) OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Curr. Genet. 52:267–274.10.1007/s00294-007-0161-ySearch in Google Scholar PubMed
Masika, P.J., Afolayan, A.J. (2003) An ethnobotanical study of plants used for the treatment of livestock diseases in Eastern Cape Province, South Africa. Pharm Biol. 41:16–21.10.1076/phbi.41.1.16.14694Search in Google Scholar
Mbuthia, K.W. Ecological and ethnobotanical analyses for forest restoration in the Taita Hills, Kenya, 2004.Search in Google Scholar
Mower, J.P. (2009) The PREP suite: predictive RNA editors for plant mitochondrial genes, chloroplast genes and user-defined alignments. Nucleic Acids Res. 37:W253–W259.10.1093/nar/gkp337Search in Google Scholar PubMed PubMed Central
Murray, B.G. (2013) Karyotype variation and evolution in Gymnosperms. In: Plant Genome Diversity. Eds. Leitch, I.J., Dolezel, J., Greilhuber, J., Volume 2, Springer, Vienna. pp. 231–243.10.1007/978-3-7091-1160-4_14Search in Google Scholar
Nie, X., Lv, S., Zhang, Y., Du, X., Wang, L., Biradar, S.S., Tan, X., Wan, F., Weining, S. (2012) Complete chloroplast genome sequence of a major invasive species, crofton weed (Ageratina adenophora). PLoS One 7:e36869.10.1371/journal.pone.0036869Search in Google Scholar PubMed PubMed Central
Quiroga, M.P., Premoli, A.C. (2007) Genetic patterns in Podocarpus parlatorei reveal the long-term persistence of cold-tolerant elements in the southern Yungas. J. Biogeogr. 34:447–455.10.1111/j.1365-2699.2006.01613.xSearch in Google Scholar
Quiroga, M., Premoli, A. (2010) Genetic structure of Podocarpus nubigena (Podocarpaceae) provides evidence of Quaternary and ancient historical events. Palaeogeogr. Palaeoclimatol. Palaeoecol. 285:186–193.10.1016/j.palaeo.2009.11.010Search in Google Scholar
Quiroga, M.P., Mathiasen, P., Iglesias, A., Mill, R.R., Premoli, A.C. (2016) Molecular and fossil evidence disentangle the biogeographical history of Podocarpus, a key genus in plant geography. J. Biogeogr. 43:372–383.10.1111/jbi.12630Search in Google Scholar
Raman, G., Park, V., Kwak, M., Lee, B., Park, S. (2017) Characterization of the complete chloroplast genome of Arabis stellari and comparisons with related species. PLoS One 12:e0183197.10.1371/journal.pone.0183197Search in Google Scholar PubMed PubMed Central
Saski, C., Lee, S.B., Fjellheim, S., Guda, C., Jansen, R.K., Luo, H., Tomkins, J., Rognli, O.A., Daniell, H., Clarke, J.L. (2007) Complete chloroplast genome sequences of Hordeum vulgare, Sorghum bicolor and Agrostis stolonifera, and comparative analyses with other grass genomes. Theor. Appl. Genet. 115:571–590.10.1007/s00122-007-0567-4Search in Google Scholar PubMed PubMed Central
Schattner, P., Brooks, A.N., Lowe, T.M. (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res. 33:W686–W689.10.1093/nar/gki366Search in Google Scholar PubMed PubMed Central
Schmieder, R., Edwards, R. (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863–864.10.1093/bioinformatics/btr026Search in Google Scholar PubMed PubMed Central
Schwarz, E.N., Ruhlman, T.A., Sabir, J.S., Hajrah, N.H., Alharbi, N.S., Al-Malki, A.L., Bailey, C.D., Jansen, R.K. (2015) Plastid genome sequences of legumes reveal parallel inversions and multiple losses of rps16 in papilionoids. J. Syst. Evol. 53:458–468.10.1111/jse.12179Search in Google Scholar
Strauss, S.H., Palmer, J.D., Howe, G.T., Doerksen, A.H. (1988) Chloroplast genomes of two conifers lack a large inverted repeat and are extensively rearranged. Proc. Natl. Acad. Sci. USA 85:3898–3902.10.1073/pnas.85.11.3898Search in Google Scholar PubMed PubMed Central
Sugiura, C., Sugita, M. (2004) Plastid transformation reveals that moss tRNAArg-CCG is not essential for plastid function. Plant J. 40:314–321.10.1111/j.1365-313X.2004.02202.xSearch in Google Scholar PubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731–2739.10.1093/molbev/msr121Search in Google Scholar PubMed PubMed Central
Thiel, T., Michalek, W., Varshney, R., Graner, A. (2003) Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor. Appl. Genet. 106:411–422.10.1007/s00122-002-1031-0Search in Google Scholar PubMed
Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B.C., Remm, M., Rozen, S.G. (2012) Primer3-new capabilities and interfaces. Nucleic Acids Res. 40:e115.10.1093/nar/gks596Search in Google Scholar PubMed PubMed Central
Wakasugi, T., Tsudzuki, J., Ito, S., Nakashima, K., Tsudzuki, T., Sugiura, M. (1994) Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. Proc. Natl. Acad. Sci. USA 91:9794–9798.10.1073/pnas.91.21.9794Search in Google Scholar PubMed PubMed Central
Wakasugi, T., Hirose, T., Horihata, M., Tsudzuki, T., Kössel, H., Sugiura, M. (1996) Creation of a novel protein-coding region at the RNA level in black pine chloroplasts: the pattern of RNA editing in the Gymnosperm chloroplast is different from that in angiosperms. Proc. Natl. Acad. Sci. USA 93:8766–8770.10.1073/pnas.93.16.8766Search in Google Scholar PubMed PubMed Central
Wu, C.S., Chaw, S.M. (2014) Highly rearranged and size-variable chloroplast genomes in conifers II clade (cupressophytes): evolution towards shorter intergenic spacers. Plant Biotechnol. J. 12:344–353.10.1111/pbi.12141Search in Google Scholar PubMed
Wu, C.-S., Chaw, S.-M. (2016) Large-scale comparative analysis reveals the mechanisms driving plastomic compaction, reduction, and inversions in conifers II (cupressophytes). Genome Biol. Evol. 8:3740–3750.10.1093/gbe/evw278Search in Google Scholar PubMed PubMed Central
Wu, C.-S., Wang, Y.-N., Liu, S.-M., Chaw, S.-M. (2007) Chloroplast genome (cpDNA) of Cycas taitungensis and 56 cp protein-coding genes of Gnetum parvifolium: insights into cpDNA evolution and phylogeny of extant seed plants. Mol. Biol. Evol. 24:1366–1379.10.1093/molbev/msm059Search in Google Scholar PubMed
Wu, C.-S., Lai, Y.-T., Lin, C.-P., Wang, Y.-N., Chaw, S.-M. (2009) Evolution of reduced and compact chloroplast genomes (cpDNAs) in gnetophytes: selection toward a lower-cost strategy. Mol. Phylogenet. Evol. 52:115–124.10.1016/j.ympev.2008.12.026Search in Google Scholar PubMed
Wu, C.-S., Lin, C.-P., Hsu, C.-Y., Wang, R.-J., Chaw, S.-M. (2011a) Comparative chloroplast genomes of Pinaceae: insights into the mechanism of diversified genomic organizations. Genome Biol. Evol. 3:309–319.10.1093/gbe/evr026Search in Google Scholar PubMed PubMed Central
Wu, C.-S., Wang, Y.-N., Hsu, C.-Y., Lin, C.-P., Chaw, S.-M. (2011b) Loss of different inverted repeat copies from the chloroplast genomes of Pinaceae and cupressophytes and influence of heterotachy on the evaluation of Gymnosperm phylogeny. Genome Biol. Evol. 3:1284–1295.10.1093/gbe/evr095Search in Google Scholar PubMed PubMed Central
Wu, C.-C., Chu, F.-H., Ho, C.-K., Sung, C.-H., Chang, S.-H. (2017) Comparative analysis of the complete chloroplast genomic sequence and chemical components of Cinnamomum micranthum and Cinnamomum kanehirae. Holzforschung 71:189–197.10.1515/hf-2016-0133Search in Google Scholar
Wyman, S.K., Jansen, R.K., Boore, J.L. (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20:3252–3255.10.1093/bioinformatics/bth352Search in Google Scholar PubMed
Yap, J.-Y.S., Rohner, T., Greenfield, A., Van Der Merwe, M., McPherson, H., Glenn, W., Kornfeld, G., Marendy, E., Pan, A.Y., Wilton, A. (2015) Complete chloroplast genome of the wollemi pine (Wollemia nobilis): structure and evolution. PLoS One 10:e0128126.10.1371/journal.pone.0128126Search in Google Scholar PubMed PubMed Central
Yi, X., Gao, L., Wang, B., Su, Y.-J., Wang, T. (2013) The complete chloroplast genome sequence of C. oliveri (Cephalotaxaceae): evolutionary comparison of Cephalotaxus chloroplast DNAs and insights into the loss of inverted repeat copies in Gymnosperms. Genome Biol. Evol. 5:688–698.10.1093/gbe/evt042Search in Google Scholar PubMed PubMed Central
Yura, K., Go, M. (2008) Correlation between amino acid residues converted by RNA editing and functional residues in protein three-dimensional structures in plant organelles. BMC Plant Biol. 8:79.10.1186/1471-2229-8-79Search in Google Scholar PubMed PubMed Central
Zhang, Y., Li, L., Yan, T.L., Liu, Q. (2014) Complete chloroplast genome sequences of Praxelis (Eupatorium catarium Veldkamp), an important invasive species. Gene 549:58–69.10.1016/j.gene.2014.07.041Search in Google Scholar PubMed
Zhao, J., Qi, B., Ding, L., Tang, X. (2010) Based on RSCU and QRSCU research codon bias of F/10 and G/11 Xylanase. Food Sci. Biotechnol. 29:755–764.Search in Google Scholar
Zhao, Y., Yin, J., Guo, H., Zhang, Y., Xiao, W., Sun, C., Wu, J., Qu, X., Yu, J., Wang, X. (2015) The complete chloroplast genome provides insight into the evolution and polymorphism of Panax ginseng. Front. Plant Sci. 5:696.10.3389/fpls.2014.00696Search in Google Scholar PubMed PubMed Central
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