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First reported chloroplast genome sequence of Punica granatum (cultivar Helow) from Jabal Al-Akhdar, Oman: phylogenetic comparative assortment with Lagerstroemia

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Abstract

Pomegranate (Punica granatum L.) is one of the oldest known edible fruits. It has grown in popularity and is a profitable fruit crop due to its attractive features including a bright red appearance and its biological activities. Scientific exploration of the genetics and evolution of these beneficial traits has been hampered by limited genomic information. In this study, we sequenced the complete chloroplast (cp) genome of the native P. granatum (cultivar Helow) cultivated in the mountains of Jabal Al-Akhdar, Oman. The results revealed a P. granatum cp genome length of 158,630 bp, characterized by a relatively conserved structure containing 2 inverted repeat regions of 25,466 bp, an 18,686 bp small single copy regions, and an 89,015 bp large single copy region. The 86 protein-coding genes included 37 transfer RNA genes and 8 ribosomal RNA genes. Comparison of the P. granatum whole cp genome with seven Lagerstroemia species revealed an overall high degree of sequence similarity with divergence among intergenic spacers. The location, distribution, and divergence of repeat sequences and shared genes of the Punica and Lagerstroemia species were highly similar. Analyses of nucleotide substitution, insertion/deletions, and highly variable regions in these cp genomes identified potential plastid markers for taxonomic and phylogenetic studies in Myrtales. A phylogenetic study of the cp genomes and 76 shared coding regions generated similar cladograms. The complete cp genome of P. granatum will aid in taxonomical studies of the family Lythraceae.

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References

  • Al Said F, Al-Yahyai R, Opara U (2012) Traditional cultivation of pomegranate in Oman. II All Afr Hortic Congr 1007:549–555

    Google Scholar 

  • Al-Dous EK, George B, Al-Mahmoud ME, Al-Jaber MY, Wang H, Salameh YM, Al-Azwani EK, Chaluvadi S, Pontaroli AC, DeBarry J (2011) De novo genome sequencing and comparative genomics of date palm (Phoenix dactylifera). Nat Biotechnol 29:521

    CAS  PubMed  Google Scholar 

  • Al-Rawahi AS, Edwards G, Al-Sibani M, Al-Thani G, Al-Harrasi AS, Rahman MS (2014) Phenolic constituents of pomegranate peels (Punica granatum L.) cultivated in Oman. European J Med Plants 4:315

    CAS  Google Scholar 

  • Al-Sadi AM, Al-Fahdi AR, Al-Yahyai RA, Al-Ghaithi AG, Al-Said FA, Soleiman MJ (2015) Genetic analysis suggests a shared origin of Punica granatum cultivars in Oman with cultivars from the center of origin Iran. Gen Resour Crop Evol 62:815–821

    Google Scholar 

  • Al-Yahyai R, Al-Said F, Opara L (2009) Fruit growth characteristics of four pomegranate cultivars from northern Oman. Fruits 64:335–341

    Google Scholar 

  • Asaf S, Khan AL, Khan AR, Waqas M, Kang S-M, Khan MA, Lee S-M, Lee I-J (2016) Complete chloroplast genome of Nicotiana otophora and its comparison with related species. Front Plant Sci 7:843

    PubMed  PubMed Central  Google Scholar 

  • Asaf S, Khan AL, Khan MA, Imran QM, Kang S-M, Al-Hosni K, Jeong EJ, Lee KE, Lee I-J (2017a) Comparative analysis of complete plastid genomes from wild soybean (Glycine soja) and nine other Glycine species. PloS one 12:e0182281

    PubMed  PubMed Central  Google Scholar 

  • Asaf S, Khan AL, Khan MA, Waqas M, Kang S-M, Yun B-W, Lee I-J (2017b) Chloroplast genomes of Arabidopsis halleri ssp. gemmifera and Arabidopsis lyrata ssp. petraea: structures comparative analysis. Sci Rep 7:7556

    PubMed  PubMed Central  Google Scholar 

  • Asaf S, Waqas M, Khan AL, Khan MA, Kang S-M, Imran QM, Shahzad R, Bilal S, Yun B-W, Lee I-J (2017c) The complete chloroplast genome of wild rice (Oryza minuta) and its comparison to related species. Front Plant Sci 8:304

    PubMed  PubMed Central  Google Scholar 

  • Bassiri-Jahromi S (2018) Punica granatum (Pomegranate) activity in health promotion and cancer prevention. Oncol Rev 12:345

    PubMed  PubMed Central  Google Scholar 

  • Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brozynska M, Furtado A, Henry RJ (2016) Genomics of crop wild relatives: expanding the gene pool for crop improvement. Plant Biotechnol J 14:1070–1085

    CAS  PubMed  Google Scholar 

  • Cao J, Jiang D, Zhao Z, Yuan S, Zhang Y, Zhang T, Zhong W, Yuan Q, Huang L (2018) Development of chloroplast genomic resources in Chinese yam (Dioscorea polystachya). BioMed Res Int 2018:1–11

    Google Scholar 

  • Cavalier-Smith T (2002) Chloroplast evolution: secondary symbiogenesis and multiple losses. Curr Biol 12:R62–R64

    CAS  PubMed  Google Scholar 

  • Celik I, Temur A, Isik I (2009) Hepatoprotective role and antioxidant capacity of pomegranate (Punica granatum) flowers infusion against trichloroacetic acid-exposed in rats. Food Chem Toxicol 47:145–149

    CAS  PubMed  Google Scholar 

  • Chandra R, Babu D, Jadhav VT, da Silva JT (2010) Origin, history and domestication of pomegranate. Fruit Veg Cereal Sci Biotechnol 4:1–6

    Google Scholar 

  • Chen J, Hao Z, Xu H, Yang L, Liu G, Sheng Y, Zheng C, Zheng W, Cheng T, Shi J (2015) The complete chloroplast genome sequence of the relict woody plant Metasequoia glyptostroboides Hu. et Cheng. Front Plant Sci 6:447

    PubMed  PubMed Central  Google Scholar 

  • Clegg MT, Gaut BS, Learn GH, Morton BR (1994) Rates and patterns of chloroplast DNA evolution. Proc Natl Acad Sci 91:6795–6801

    CAS  PubMed  PubMed Central  Google Scholar 

  • Conti E, Litt A, Wilson PG, Graham SA, Briggs BG, Johnson L, Sytsma KJ (1997) Interfamilial relationships in Myrtales: molecular phylogeny and patterns of morphological evolution. Syst Bot 22:629–647

    Google Scholar 

  • Corriveau JL, Coleman AW (1988) Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperm species. Am J Bot 75:1443–1458

    Google Scholar 

  • Cronn R, Liston A, Parks M, Gernandt DS, Shen R, Mockler T (2008) Multiplex sequencing of plant chloroplast genomes using Solexa sequencing-by-synthesis technology. Nucleic Acids Res 36:e122–e122

    PubMed  PubMed Central  Google Scholar 

  • Daniell H, Chan H-T, Pasoreck EK (2016a) Vaccination via chloroplast genetics: affordable protein drugs for the prevention and treatment of inherited or infectious human diseases. Ann Rev Genet 50:595–618

    CAS  PubMed  Google Scholar 

  • Daniell H, Lin C-S, Yu M, Chang W-J (2016b) Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biol 17:134

    PubMed  PubMed Central  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Meth 9:772

    CAS  Google Scholar 

  • Diekmann K, Hodkinson TR, Barth S (2012) New chloroplast microsatellite markers suitable for assessing genetic diversity of Lolium perenne and other related grass species. Ann Bot 110:1327–1339

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dong W, Liu J, Yu J, Wang L, Zhou S (2012) Highly variable chloroplast markers for evaluating plant phylogeny at low taxonomic levels and for DNA barcoding. PloS one 7:e35071

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dong W, Xu C, Li D, Jin X, Li R, Lu Q, Suo Z (2016) Comparative analysis of the complete chloroplast genome sequences in psammophytic Haloxylon species (Amaranthaceae). PeerJ 4:e2699

    PubMed  PubMed Central  Google Scholar 

  • Ercisli S, Agar G, Orhan E, Yildirim N, Hizarci Y (2007) Interspecific variability of RAPD and fatty acid composition of some pomegranate cultivars (Punica granatum L.) growing in Southern Anatolia Region in Turkey Biochemical. Syst Ecol 35:764–769

    CAS  Google Scholar 

  • Ercisli S, Kafkas E, Orhan E, Kafkas S, Dogan Y, Esitken A (2011) Genetic characterization of pomegranate (Punica granatum L.) genotypes by AFLP markers. Biol Res 44:345–350

    CAS  PubMed  Google Scholar 

  • Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I (2004) VISTA: computational tools for comparative genomics. Nucleic Acids Res 32:W273–W279. https://doi.org/10.1093/nar/gkh458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu C-N, Li H-T, Milne R, Zhang T, Ma P-F, Yang J, Li D-Z, Gao L-M (2017) Comparative analyses of plastid genomes from fourteen Cornales species: inferences for phylogenetic relationships and genome evolution. BMC Genom 18:956

    Google Scholar 

  • Gallaher SD, Fitz-Gibbon ST, Strenkert D, Purvine SO, Pellegrini M, Merchant SS (2018) High-throughput sequencing of the chloroplast and mitochondrion of Chlamydomonas reinhardtii to generate improved de novo assemblies, analyze expression patterns and transcript speciation, and evaluate diversity among laboratory strains and wild isolates. Plant J 93:545–565

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gao L, Yi X, Yang Y-X, Su Y-J, Wang T (2009) Complete chloroplast genome sequence of a tree fern Alsophila spinulosa: insights into evolutionary changes in fern chloroplast genomes. BMC Evol Biol 9:130

    PubMed  PubMed Central  Google Scholar 

  • Gates DJ, Pilson D, Smith SD (2018) Filtering of target sequence capture individuals facilitates species tree construction in the plant subtribe Iochrominae (Solanaceae). Mol Phylogenet Evol 123:26–34

    PubMed  Google Scholar 

  • Graham SA, Hall J, Sytsma K, Shi S-H (2005) Phylogenetic analysis of the Lythraceae based on four gene regions and morphology International. J Plant Sci 166:995–1017

    CAS  Google Scholar 

  • Gu C, Tembrock LR, Johnson NG, Simmons MP, Wu Z (2016) The complete plastid genome of Lagerstroemia fauriei and loss of rpl2 intron from Lagerstroemia (Lythraceae). PLoS One 11:e0150752

    PubMed  PubMed Central  Google Scholar 

  • Gu C, Tembrock LR, Zhang D, Wu Z (2017) Characterize the complete chloroplast genome of Lagerstroemia floribunda (Lythraceae), a narrow endemic crape myrtle native to Southeast Asia Conservation. Genet Resour 9:91–94

    Google Scholar 

  • Hajiahmadi Z, Talebi M, Sayed-Tabatabaei BE (2013) Studying genetic variability of Pomegranate (Punica granatum L.) based on chloroplast DNA and barcode genes. Mol Biotechnol 55:249–259

    CAS  PubMed  Google Scholar 

  • Hu TT, Pattyn P, Bakker EG, Cao J, Cheng J-F, Clark RM, Fahlgren N, Fawcett JA, Grimwood J, Gundlach H (2011a) The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet 43:476

    PubMed  PubMed Central  Google Scholar 

  • Hu TT, Pattyn P, Bakker EG, Cao J, Cheng JF, Clark RM, Fahlgren N, Fawcett JA, Grimwood J, Gundlach H, Haberer G, Hollister JD, Ossowski S, Ottilar RP, Salamov AA, Schneeberger K, Spannagl M, Wang X, Yang L, Nasrallah ME, Bergelson J, Carrington JC, Gaut BS, Schmutz J, Mayer KFX, de Peer YV, Grigoriev IV, Nordborg M, Weigel D, Guo YL (2011b) The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet 43:476–476+. https://doi.org/10.1038/ng.807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Y-l, Shi S-h (2002) Phylogenetics of Lythraceae sensu lato: a preliminary analysis based on chloroplast rbc L gene, psa A-ycf 3 spacer, and nuclear rDNA internal transcribed spacer (ITS) sequences. Int J Plant Sci 163:215–225

    CAS  Google Scholar 

  • Huang H, Shi C, Liu Y, Mao S-Y, Gao L-Z (2014) Thirteen Camellia chloroplast genome sequences determined by high-throughput sequencing: genome structure and phylogenetic relationships. BMC Evol Biol 14:151

    PubMed  PubMed Central  Google Scholar 

  • Huotari T, Korpelainen H (2012) Complete chloroplast genome sequence of Elodea canadensis and comparative analyses with other monocot plastid genomes. Gene 508:96–105

    CAS  PubMed  Google Scholar 

  • Jbir R, Hasnaoui N, Mars M, Marrakchi M, Trifi M (2008) Characterization of Tunisian pomegranate (Punica granatum L.) cultivars using amplified fragment length polymorphism analysis. Scientia Horticulturae 115:231–237

    CAS  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    CAS  PubMed  PubMed Central  Google Scholar 

  • Khan A, Khan IA, Heinze B, Azim MK (2012) The chloroplast genome sequence of date palm (Phoenix dactylifera L. cv.‘Aseel’). Plant Mol Biol Rep 30:666–678

    CAS  Google Scholar 

  • Khan AL, Al-Harrasi A, Asaf S, Park CE, Park G-S, Khan AR, Lee I-J, Al-Rawahi A, Shin J-H (2017) The first chloroplast genome sequence of Boswellia sacra, a resin-producing plant in Oman. PloS one 12:e0169794

    PubMed  PubMed Central  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

    CAS  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    CAS  PubMed  Google Scholar 

  • Kode V, Mudd EA, Iamtham S, Day A (2005) The tobacco plastid accD gene is essential and is required for leaf development. Plant J 44:237–244

    CAS  PubMed  Google Scholar 

  • Kolodner R, Tewari K (1979) Inverted repeats in chloroplast DNA from higher plants. Proc Natl Acad Sci 76:41–45

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kraemer L, Beszteri B, Gäbler-Schwarz S, Held C, Leese F, Mayer C, Pöhlmann K, Frickenhaus S (2009) STAMP: extensions to the STADEN sequence analysis package for high throughput interactive microsatellite marker design. BMC Bioinform 10:41. https://doi.org/10.1186/1471-2105-10-41

    Article  CAS  Google Scholar 

  • Kuang D-Y, Wu H, Wang Y-L, Gao L-M, Zhang S-Z, Lu L (2011) Complete chloroplast genome sequence of Magnolia kwangsiensis (Magnoliaceae): implication for DNA barcoding and population genetics. Genome 54:663–673

    PubMed  Google Scholar 

  • Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299–306. https://doi.org/10.1093/bib/bbn017

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Hahn FM, McMahan CM, Cornish K, Whalen MC (2009) Comparative analysis of the complete sequence of the plastid genome of Parthenium argentatum and identification of DNA barcodes to differentiate Parthenium species and lines. BMC Plant Biol 9:131

    PubMed  PubMed Central  Google Scholar 

  • Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R (2001) REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res 29:4633–4642 doi. https://doi.org/10.1093/nar/29.22.4633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lansky EP, Newman RA (2007) Punica granatum (pomegranate) and its potential for prevention and treatment of inflammation and cancer. J Ethnopharmacol 109:177–206

    CAS  PubMed  Google Scholar 

  • Lee C, Wen J (2004) Phylogeny of Panax using chloroplast trnC–trnD intergenic region and the utility of trnC–trnD in interspecific studies of plants. Mol Phylogen Evol 31:894–903

    CAS  Google Scholar 

  • Levin GM (2006) Pomegranate roads: a Soviet botanist’s exile from Eden, 1st edn. Floreant Press, Forestville, California, pp 15–183

    Google Scholar 

  • 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. https://doi.org/10.1007/s00294-007-0161-y

    Article  CAS  PubMed  Google Scholar 

  • Ngamriabsakul C, Techaprasan J (2006) The phylogeny of Thai Boesenbergia (Zingiberaceae) based on petA-psbJ spacer (chloroplast DNA). J Sci Technol 28:49–57

    Google Scholar 

  • Nie X, Lv S, Zhang Y, Du X, Wang L, Biradar SS, Tan X, Wan F, Weining S (2012) Complete chloroplast genome sequence of a major invasive species, crofton weed (Ageratina adenophora). PloS one 7:e36869

    CAS  PubMed  PubMed Central  Google Scholar 

  • Noormohammadi Z, Fasihee A, Homaee-Rashidpoor S, Sheidai M, Baraki SG, Mazooji A, Tabatabaee-Ardakani SZ (2012) Genetic variation among Iranian pomegranates (‘Punica granatum’ L.) using RAPD, ISSR and SSR markers Australian. J Crop Sci 6:268

    CAS  Google Scholar 

  • Norouzi M, Talebi M, Sayed-Tabatabaei B-E (2012) Chloroplast microsatellite diversity and population genetic structure of Iranian pomegranate (Punica granatum L.) genotypes. Scientia Horticulturae 137:114–120

    CAS  Google Scholar 

  • Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast. DNA Nat 322:572–574

    CAS  Google Scholar 

  • Opara U, Mahdoury AA, Al-Ani MR, Al-Said FA, Al-Yahyai RA, Al-Kindi H, Al-Shuaibi Y (2008) Physiological responses and changes in postharvest quality attributes of ‘Helow’pomegranate variety (Punica granatum L.) during refrigerated storage. In: International Conference of Agricultural Engineering, 31 August–4 September 2008. International Commission of Agricultural Engineering (CIGR), Institut fur Landtechnik, Iguassu Falls City, Brazil. Bonn, Germany

  • Parvaresh M, Talebi M, Sayed-Tabatabaei B-E (2012) Molecular diversity and genetic relationship of pomegranate (Punica granatum L.) genotypes using microsatellite markers. Scientia Horticulturae 138:244–252

    CAS  Google Scholar 

  • Perdereau A, Klaas M, Barth S, Hodkinson TR (2017) Plastid genome sequencing reveals biogeographical structure and extensive population genetic variation in wild populations of Phalaris arundinacea L. in north-western. Europe Gcb Bioenergy 9:46–56

    CAS  Google Scholar 

  • Powell W, Morgante M, McDevitt R, Vendramin G, Rafalski J (1995) Polymorphic simple sequence repeat regions in chloroplast genomes: applications to the population genetics of pines. Proc Natl Acad Sci 92:7759–7763

    CAS  PubMed  PubMed Central  Google Scholar 

  • Provan J, Corbett G, Powell W, McNicol J (1997) Chloroplast DNA variability in wild and cultivated rice (Oryza spp.) revealed by polymorphic chloroplast simple sequence repeats. Genome 40:104–110

    CAS  PubMed  Google Scholar 

  • Provan J, Powell W, Hollingsworth PM (2001) Chloroplast microsatellites: new tools for studies in plant ecology and evolution. Trends Ecol Evol 16:142–147

    CAS  PubMed  Google Scholar 

  • Qian J, Song J, Gao H, Zhu Y, Xu J, Pang X, Yao H, Sun C, Li X, Li C (2013) The complete chloroplast genome sequence of the medicinal plant Salvia miltiorrhiza. PloS one 8:e57607

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raime K, Remm M (2018) Method for the identification of taxon-specific k-mers from chloroplast genome: a case study on tomato plant (Solanum lycopersicum). Front Plant Sci 9:6

    PubMed  PubMed Central  Google Scholar 

  • Raubeson LA, Peery R, Chumley TW, Dziubek C, Fourcade HM, Boore JL, Jansen RK (2007) Comparative chloroplast genomics: analyses including new sequences from the angiosperms Nuphar advena and Ranunculus macranthus. BMC Genom 8:174

    Google Scholar 

  • Ravi V, Khurana J, Tyagi A, Khurana P (2008) An update on chloroplast genomes. Plant Syst Evol 271:101–122

    CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180

    Article  CAS  PubMed  Google Scholar 

  • Rose O, Falush D (1998) A threshold size for microsatellite expansion. Mol Biol Evol 15:613–615

    CAS  PubMed  Google Scholar 

  • Rymon D (2011) Mapping features of the global pomegranate market. Acta Hortic 890:599–602

    Google Scholar 

  • Saski C, Lee S-B, Fjellheim S, Guda C, Jansen RK, Luo H, Tomkins J, Rognli OA, Daniell H, Clarke JL (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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schattner P, Brooks AN, Lowe TM (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33:W686–W689. https://doi.org/10.1093/nar/gki366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seeram NP, Adams LS, Henning SM, Niu Y, Zhang Y, Nair MG, Heber D (2005) In vitro antiproliferative, apoptotic and antioxidant activities of punicalagin, ellagic acid and a total pomegranate tannin extract are enhanced in combination with other polyphenols as found in pomegranate juice. J Nutr Biochem 16:360–367

    CAS  PubMed  Google Scholar 

  • Sharma J, Maity A (2010) Pomegranate phytochemicals: Nutraceutical and therapeutic values. Fruit Veg Cereal Sci Biotechnol 4:56–76

    Google Scholar 

  • Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043

    CAS  PubMed  PubMed Central  Google Scholar 

  • Soleimani MH, Talebi M, Sayed-Tabatabaei BE (2012) Use of SRAP markers to assess genetic diversity and population structure of wild, cultivated, and ornamental pomegranates (Punica granatum L.) in different regions of Iran. Plant Syst Evol 298:1141–1149

    Google Scholar 

  • Soriano JM, Zuriaga E, Rubio P, Llácer G, Infante R, Badenes ML (2011) Development and characterization of microsatellite markers in pomegranate (Punica granatum L.). Mol Breed 27:119–128

    Google Scholar 

  • Steele PR, Friar LM, Gilbert LE, Jansen RK (2010) Molecular systematics of the neotropical genus Psiguria (Cucurbitaceae): Implications for phylogeny and species identification American. J Bot 97:156–173

    CAS  Google Scholar 

  • Suo Z, Zhang C, Zheng Y, He L, Jin X, Hou B, Li J (2012) Revealing genetic diversity of tree peonies at micro-evolution level with hyper-variable chloroplast markers and floral traits. Plant Cell Rep 31:2199–2213

    CAS  PubMed  Google Scholar 

  • Suo Z, Chen L, Pei D, Jin X, Zhang H (2015) A new nuclear DNA marker from ubiquitin ligase gene region for genetic diversity detection of walnut germplasm resources. Biotechnol Rep 5:40–45

    Google Scholar 

  • Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), Version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Talebi BM, Bahar M, Sharifnabi B, Yamchi A (2011) Evaluation of genetic diversity among Iranian pomegranate (Punica granatum L.) cultivars, using ISSR and RAPD markers. Taxon Biosyst 8:35–44

    Google Scholar 

  • Tangphatsornruang S, Sangsrakru D, Chanprasert J, Uthaipaisanwong P, Yoocha T, Jomchai N, Tragoonrung S (2009) The chloroplast genome sequence of mungbean (Vigna radiata) determined by high-throughput pyrosequencing: structural organization and phylogenetic relationships. DNA Res 17:11–22

    PubMed  PubMed Central  Google Scholar 

  • Timme RE, Kuehl JV, Boore JL, Jansen RK (2007) A comparative analysis of the Lactuca and Helianthus (Asteraceae) plastid genomes: identification of divergent regions and categorization of shared repeats American. J Bot 94:302–312

    CAS  Google Scholar 

  • Wambugu PW, Brozynska M, Furtado A, Waters DL, Henry RJ (2015) Relationships of wild and domesticated rices (Oryza AA genome species) based upon whole chloroplast genome sequences. Sci Rep 5:13957

    PubMed  PubMed Central  Google Scholar 

  • Wolfe KH, Li W-H, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci 84:9054–9058

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu Z (2016) The whole chloroplast genome of shrub willows (Salix suchowensis). Mitochondrial DNA Part A 27:2153–2154

    CAS  Google Scholar 

  • Wu ZQ, Tembrock LR, Ge S (2015) Are differences in genomic data sets due to true biological variants or errors in genome assembly: an example from two chloroplast genomes. Plos One. https://doi.org/10.1371/journal.pone.0118019

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu Z, Gu C, Tembrock LR, Zhang D, Ge S (2017) Characterization of the whole chloroplast genome of Chikusichloa mutica and its comparison with other rice tribe (Oryzeae) species. PloS one 12:e0177553

    PubMed  PubMed Central  Google Scholar 

  • Wyman SK, Jansen RK, Boore JL (2004) Automatic annotation of organellar genomes with. DOGMA Bioinform 20:3252–3255. https://doi.org/10.1093/bioinformatics/bth352

    Article  CAS  Google Scholar 

  • Xiang XG, Zhang JB, Lu AM, Li RQ (2011) Molecular identification of species in Juglandaceae: a tiered method. J Syst Evol 49:252–260

    Google Scholar 

  • Xu J, Feng D, Song G, Wei X, Chen L, Wu X, Li X, Zhu Z (2003) The first intron of rice EPSP synthase enhances expression of foreign gene. Sci China Ser C Life Sci 46:561

    CAS  Google Scholar 

  • Xu C, Dong W, Li W, Lu Y, Xie X, Jin X, Shi J, He K, Suo Z (2017) Comparative analysis of six Lagerstroemia complete chloroplast genomes. Front Plant Sci 8:15

    PubMed  PubMed Central  Google Scholar 

  • Yang M, Zhang X, Liu G, Yin Y, Chen K, Yun Q, Zhao D, Al-Mssallem IS, Yu J (2010) The complete chloroplast genome sequence of date palm (Phoenix dactylifera L.). PloS one 5:e12762

    PubMed  PubMed Central  Google Scholar 

  • Yao X, Tang P, Li Z, Li D, Liu Y, Huang H (2015) The first complete chloroplast genome sequences in Actinidiaceae: genome structure and comparative analysis. PloS one 10:e0129347

    PubMed  PubMed Central  Google Scholar 

  • Yao X, Tan Y-H, Liu Y-Y, Song Y, Yang J-B, Corlett RT (2016) Chloroplast genome structure in Ilex (Aquifoliaceae). Sci Rep 6:28559

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yi X, Gao L, Wang B, Su Y-J, Wang T (2013) The complete chloroplast genome sequence of Cephalotaxus 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

    PubMed  PubMed Central  Google Scholar 

  • Yuan Z, Fang Y, Zhang T, Fei Z, Han F, Liu C, Liu M, Xiao W, Zhang W, Wu S (2018) The pomegranate (Punica granatum L.) genome provides insights into fruit quality and ovule developmental biology. Plant Biotechnol J 16:1363–1374 doi. https://doi.org/10.1111/pbi.12875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Q, Liu Y (2003) Examination of the cytoplasmic DNA in male reproductive cells to determine the potential for cytoplasmic inheritance in 295 angiosperm species. Plant Cell Physiol 44:941–951

    CAS  PubMed  Google Scholar 

  • Zhang Y-J, Ma P-F, Li D-Z (2011) High-throughput sequencing of six bamboo chloroplast genomes: phylogenetic implications for temperate woody bamboos (Poaceae:Bambusoideae. PloS one 6:e20596

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Iaffaldano BJ, Zhuang X, Cardina J, Cornish K (2017) Chloroplast genome resources and molecular markers differentiate rubber dandelion species from weedy relatives. BMC Plant Biol 17:34

    PubMed  PubMed Central  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

    PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by the Oman Research Council (EBR/15/007). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Author notes

  1. Abdul Latif Khan and Sajjad Asaf equally contributed to the work.

Authors and Affiliations

  1. Natural and Medical Sciences Research Center, University of Nizwa, 616, Nizwa, Oman

    Abdul Latif Khan, Sajjad Asaf, Ahmed Al-Harrasi & Ahmed Al-Rawahi

  2. School of Applied Biosciences, Kyungpook National University, Daegu, 41566, Republic of Korea

    In-Jung Lee

Authors
  1. Abdul Latif Khan
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  2. Sajjad Asaf
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  3. In-Jung Lee
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  4. Ahmed Al-Harrasi
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  5. Ahmed Al-Rawahi
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Corresponding author

Correspondence to Ahmed Al-Harrasi.

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Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Data archiving statement

The complete chloroplast genome sequence data of Punica granatum cultivar Helow has been submitted to GenBank of NCBI with accession number MG878386. The data will be available publically after the acceptance of the manuscript. The accession numbers for Lagerstroemia species used in this study are provided in Table 1.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10709_2018_37_MOESM1_ESM.tiff

Figure S1. Analysis of repeat sequences in P. granatum L. (cultivar Helow) genomes. A: Total of 3 inverted repeat (IR) types; B: Frequency of palindromic repeats by length; C: Frequency of forward repeats by length; and D: Frequency of tandem repeats by length. ND: not determined. (TIFF 1709 KB)

10709_2018_37_MOESM2_ESM.tif

Figure S2. Alignment of the P. granatum L. (cultivar Helow) chloroplast genome sequences. VISTA-based identity plot showing sequence identity among the 4 species using Punica granatum L. (cultivar Helow) as a reference. The vertical scale indicates percent identity, ranging from 50–100%. The horizontal axis indicates the coordinates within the chloroplast genome. Arrows indicate the annotated genes and their transcription direction. The thick black lines show the inverted repeats (IRs). (TIF 3262 KB)

Figure S3. Pairwise distance of 76 genes from P. granatum L. (cultivar Helow) and 9 other cp genomes (TIF 1900 KB)

10709_2018_37_MOESM4_ESM.tif

Figure S4. Sliding window analysis of the whole chloroplast genomes (A) Two P. granatum species and (B) P. granatum species with other 8 species from family Lythraceae (including P. granatum (window length: 600 bp, stepsize: 200 bp)). X-axis is the position of the midpoint of a window and the Y-axis is the nucleotide diversity of each window. (TIF 1564 KB)

10709_2018_37_MOESM5_ESM.tif

Figure S5. Phylogenetic trees for 27 species from the order Myrtales using 4 different methods The data from the complete chloroplast genomes were analyzed with 4 different methods: Neighbor-joining (NJ), maximum parsimony (MP), maximum likelihood (ML), and Bayesian inference (BI). The numbers above the branches are the bootstrap values from the NJ, MP, and ML methods and the posterior probabilities of BI. The black dot represents the positions of Punica granatum L. (cultivar Helow). (TIF 732 KB)

Table S1. Genes in the sequenced Punica granatum (cultivar Helow) chloroplast genome (DOCX 14 KB)

Table S2. Genes with introns in the P. granatum chloroplast genome and the length of exons and introns (DOCX 15 KB)

Table S3. Codon-anticodon recognition pattern and codon usage for the P. granatum chloroplast genome (DOCX 18 KB)

Table S4. Repeat sequences in the P. granatum chloroplast genome (DOCX 17 KB)

Table S5. Tandem repeat sequences in the P. granatum chloroplast genome (DOCX 23 KB)

Table S6. Simple sequence repeats (SSRs) in the P. granatum chloroplast genome (DOCX 15 KB)

10709_2018_37_MOESM12_ESM.xls

Table S7. Average pairwise sequence distance of P. granatum L. (cultivar Helow) with P. granatum and other 7 Lythraceae species cp genome (XLS 30 KB)

Table S8. Indels and SNP analysis of P. granatum in comparison with related 8 species cp genomes (XLSX 9 KB)

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Khan, A.L., Asaf, S., Lee, IJ. et al. First reported chloroplast genome sequence of Punica granatum (cultivar Helow) from Jabal Al-Akhdar, Oman: phylogenetic comparative assortment with Lagerstroemia. Genetica 146, 461–474 (2018). https://doi.org/10.1007/s10709-018-0037-8

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  • DOI: https://doi.org/10.1007/s10709-018-0037-8

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