The complete chloroplast genome of Prunus triloba var. plena and comparative analysis of Prunus species: genome structure, sequence divergence, and phylogenetic analysis

Abstract

Prunus triloba var. plena, also known as flowering plum, is a perennial deciduous shrub admired for its brilliant pink-purple blooms. Chloroplast (cp) DNA is highly conserved in structure and gene arrangement, making cp genomic data valuable resources for species delimitation and phylogenetics. The cp genome of P. triloba var. plena was de novo assembled with the aim of developing cp-derived molecular markers and deepening the understanding of phylogenetic relationship among Prunus species. The complete cp genome was 158,022 bp in length, with a GC content of 36.8%. The plastome featured a typical quadripartite structure, consisting of a pair of inverted repeat (IR) regions of 26,379 bp, separated by a large single copy (LSC) region of 86,242 bp, and a small single copy (SSC) region of 19,022 bp. The cp genome encoded 134 genes, including 87 protein-coding genes, 39 tRNA genes, and 8 rRNA genes. A total of 59 simple sequence repeat (SSR) were identified, 68% of which were located in the intergenic regions. An obvious A/T bias was observed in the majority of SSRs detected. Besides, 48 repeats in different sizes and types were detected. These repeats, together with SSRs and the divergence hotspots detected, could serve as markers facilitating species discrimination and evolutionary research in Prunus. Using plastome sequences, we re-investigated the phylogenetic relationship among 32 Prunus species. These species explicitly clustered into three monophyletic clades, among which P. triloba var. plena was closely related to species in the subgenera Amygdalus and Prunus.

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References

  1. Bankevich A et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. Bobik K, Burch-Smith TM (2015) Chloroplast signaling within, between and beyond cells. Front Plant Sci 6:781. https://doi.org/10.3389/fpls.2015.00781

    Article  PubMed  PubMed Central  Google Scholar 

  3. Bolger A, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. Bortiri E et al (2001) Phylogeny and systematics of Prunus (Rosaceae) as determined by sequence analysis of ITS and the chloroplast trnL-trnF spacer DNA. Syst Bot 26:797–807. https://doi.org/10.1043/0363-6445-26.4.797

    Article  Google Scholar 

  5. Cong X (1991) Studies of the reproduction of green branch cutting of Prunus triloba var. plena. Acta Hortic Sin 18:278–280

    Google Scholar 

  6. da Silva Oliveira EJ, Marques A, Almeida C (2019) The chloroplast genome of Hancornia speciosa Gomes: structural organization and phylogenomic studies in Rauvolfioideae (Apocynaceae). Braz J Bot 42:449–455. https://doi.org/10.1007/s40415-019-00549-8

    Article  Google Scholar 

  7. Duan Y-Z, Shen Y-H, Kang F-R, Wang J-W (2019) Characterization of the complete chloroplast genomes of the endangered shrub species Prunus mongolica and Prunus pedunculata (Rosales: rosaceae). Conserv Genet Resour 11:249–252. https://doi.org/10.1007/s12686-017-0979-7

    Article  Google Scholar 

  8. Duan C, Shen Y, Zhao G (2020) Complete chloroplast genome characteristics of Prunus triloba Lindl. Mitochondrial DNA B 5:504–505. https://doi.org/10.1080/23802359.2019.1704657

    Article  Google Scholar 

  9. Gao K, Li J, Khan WU et al (2019) Comparative genomic and phylogenetic analyses of Populus section Leuce using complete chloroplast genome sequences. Tree Genet Genomes 15:32. https://doi.org/10.1007/s11295-019-1342-9

    Article  Google Scholar 

  10. Gilman EF (1997) Trees for urban and suburban landscapes. Delmar, Albany

    Google Scholar 

  11. Greiner S, Lehwark P, Bock R (2019) OrganellarGenomeDRAW (OGDRAW) version 1.3.1: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Res 47:W59–W64. https://doi.org/10.1093/nar/gkz238

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. Haberle RC, Fourcade HM, Boore JL, Jansen RK (2008) Extensive rearrangements in the chloroplast genome of trachelium caeruleum are associated with repeats and tRNA genes. J Mol Evol 66:350–361. https://doi.org/10.1007/s00239-008-9086-4

    CAS  Article  PubMed  Google Scholar 

  13. Huang J, Yang X, Zhang C, Yin X, Liu S, Li X (2015) Development of chloroplast microsatellite markers and analysis of chloroplast diversity in Chinese jujube (Ziziphus jujuba Mill.) and wild jujube (Ziziphus acidojujuba Mill.). PloS One 10:e0134519. https://doi.org/10.1371/journal.pone.0134519

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Kalkman C (1966) The old world species of Prunus subg. Laurocerasus including those formerly referred to Pygeum. Blumea Biodiv Evol Biogeogr Plants 13:1–115. https://doi.org/urn:nbn:nl:ui:19-526237

    Google Scholar 

  15. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Kearse M, Moir R, Wilson A et al (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199

    Article  PubMed  PubMed Central  Google Scholar 

  17. Kim HT, Kim JS, Lee YM et al (2018) Molecular markers for phylogenetic applications derived from comparative plastome analysis of Prunus species: novel phylogenetic markers for Prunus species. J Syst Evol 57:15–22. https://doi.org/10.1111/jse.12453

    Article  Google Scholar 

  18. Kocoń J, Muszyński S (1982) Ultrastructure of pollen grain sculpturing in several species of the Rosaceae family. Acta Soc Bot Pol 51:341–344. https://doi.org/10.5586/asbp.1982.030

    Article  Google Scholar 

  19. Krawczyk K, Nobis M, Myszczyński K, Klichowska E, Sawicki J (2018) Plastid super-barcodes as a tool for species discrimination in feather grasses (Poaceae: Stipa). Sci Rep 8:1924. https://doi.org/10.1038/s41598-018-20399-w

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  22. Lee S, Wen J (2001) A phylogenetic analysis of Prunus and the Amygdaloideae (Rosaceae) using ITS sequences of nuclear ribosomal DNA. Am J Bot 88:150–160. https://doi.org/10.2307/2657135

    CAS  Article  PubMed  Google Scholar 

  23. Lee SR, Kim K, Lee BY, Lim CE (2019) Complete chloroplast genomes of all six Hosta species occurring in Korea: molecular structures, comparative, and phylogenetic analyses. BMC Genom 20:833. https://doi.org/10.1186/s12864-019-6215-y

    CAS  Article  Google Scholar 

  24. Li B, Huang P, Guo W, Zheng Y (2020) Development of nuclear SSR and chloroplast genome markers in diverse Liriodendron chinense germplasm based on low-coverage whole genome sequencing. Biol Res 53:21. https://doi.org/10.1186/s40659-020-00289-0

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Liu X, Chang EM, Liu J et al (2019) Complete chloroplast genome sequence and phylogenetic analysis of Quercus bawanglingensis Huang, Li et Xing, a vulnerable oak tree in China. Forests 10:587. https://doi.org/10.3390/f10070587

    Article  Google Scholar 

  26. Mayor C, Brudno M, Schwartz JR et al (2000) VISTA : visualizing global DNA sequence alignments of arbitrary length. Bioinformatics 16:1046–1047. https://doi.org/10.1093/bioinformatics/16.11.1046

    CAS  Article  PubMed  Google Scholar 

  27. McKain M, Johnson M, Uribe-Convers S, Eaton D, Yang Y (2018) Practical considerations for plant phylogenomics. Appl Plant Sci 6:e1038. https://doi.org/10.1002/aps3.1038

    Article  PubMed  PubMed Central  Google Scholar 

  28. Milošević T, Milošević N (2018) Plum (Prunus spp) Breeding. In: Al-Khayri JM, Jain SM, Johnson DV (eds) Advances in plant breeding strategies: fruits, 1st edn. Springer, Switzerland, pp 165–215. https://doi.org/10.1007/978-3-319-91944-7_5

    Google Scholar 

  29. Mu X, Wang P, Du J, Gao YG, Zhang J (2018) The chloroplast genome of Cerasus humilis: Genomic characterization and phylogenetic analysis. PLoS ONE 13:e0196473. https://doi.org/10.1371/journal.pone.0196473

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Mulligan BO (1941) Manual of cultivated trees and shrubs hardy in North America. Nature 148:7. https://doi.org/10.1038/148007a0

    Article  Google Scholar 

  31. Palmer J (1990) Plastid chromosomes: structure and evolution. In: Lawrence B, Indra KV (eds) The molecular biology of plastids: cell culture and somatic cell genetics of plants, 1st edn. Academic Press, San Diego, pp 5–53

    Google Scholar 

  32. Pervaiz T, Sun X, Zhang Y, Tao R, Zhang J, Fang J (2015) Association between chloroplast and mitochondrial DNA sequences in Chinese Prunus genotypes (Prunus persica, Prunus domestica, and Prunus avium). BMC Plant Biol 15:4. https://doi.org/10.1186/s12870-014-0402-4

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256. https://doi.org/10.1093/molbev/msn083

    CAS  Article  PubMed  Google Scholar 

  34. Raubeson L, Jansen R (2005) Chloroplast genomes of plants. In: Henry RJ (ed) Plant diversity and evolution: genotypic and phenotypic variation in higher plants, 1st edn. CABI Publishing, Oxon, pp 45–68

    Google Scholar 

  35. Roston RL, Jouhet J, Yu F, Gao H (2018) Editorial: structure and function of chloroplasts. Front Plant Sci 9:1656. https://doi.org/10.3389/fpls.2018.01656

    Article  PubMed  PubMed Central  Google Scholar 

  36. Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sanchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248

    CAS  Article  PubMed  Google Scholar 

  37. Shi L, Chen H, Jiang M, Wang L, Wu X, Huang L, Liu C (2019) CPGAVAS2, an integrated plastome sequence annotator and analyzer. Nucl Acids Res 47:W65–W73. https://doi.org/10.1093/nar/gkz345

    CAS  Article  PubMed  Google Scholar 

  38. Smartt J, Simmonds NW (1995) Evolution of crop plants. Wiley, New York

    Google Scholar 

  39. Tillich M, Lehwark P, Pellizzer T, Ulbricht-Jones E, Fischer A, Bock R, Greiner S (2017) GeSeq: versatile and accurate annotation of organelle genomes. Nucl Acids Res 45:W6–W11. https://doi.org/10.1093/nar/gkx391

    CAS  Article  PubMed  Google Scholar 

  40. Turmel M, Otis C, Lemieux C (2015) Dynamic evolution of the chloroplast genome in the green algal classes Pedinophyceae and Trebouxiophyceae. Genome Biol Evol 7:2062–2082. https://doi.org/10.1093/gbe/evv130

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Vieira M-L, Santini L, Lima Diniz A, Munhoz C (2016) Microsatellite markers: what they mean and why they are so useful. Genet Mol Biol 39:312–328. https://doi.org/10.1590/1678-4685-GMB-2016-0027

    Article  PubMed  PubMed Central  Google Scholar 

  42. Walker BJ, Abeel T, Shea T et al (2014) Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9:e112963. https://doi.org/10.1371/journal.pone.0112963

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. Wang L, Liang J, Shang Q, Sa W, Wang L (2020) The complete plastome of Sorbaria kirilowii: genome structure, comparative analysis, and phylogenetic implications. Mol Biol Rep. https://doi.org/10.1007/s11033-020-05976-5

    Article  PubMed  PubMed Central  Google Scholar 

  44. Wellington Santos M (2009) WebSat: a web software for microsatellite marker development. Bioinformation 3:282–283. https://doi.org/10.6026/97320630003282

    Article  Google Scholar 

  45. Wen J et al (2008) Phylogenetic inferences in Prunus (Rosaceae) using chloroplast ndhF and ribosomal ITS sequences. J Syst Evol 46:322–332. https://doi.org/10.3724/SP.J.1002.2008.08050

    Article  Google Scholar 

  46. Wicke S, Schneeweiss GM, dePamphilis CW, Müller KF, Quandt D (2011) The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Mol Biol 76:273–297. https://doi.org/10.1007/s11103-011-9762-4

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Xia X (2018) DAMBE7: new and improved tools for data analysis in molecular biology and evolution. Mol Biol Evol 35:1550–1552. https://doi.org/10.1093/molbev/msy073

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. Xu Y, Ma R, Xie H, Liu J-T, Cao M-Q (2005) Development of SSR markers for the phylogenetic analysis of almond trees from China and the Mediterranean region. Genome 47:1091–1104. https://doi.org/10.1139/g04-058

    Article  Google Scholar 

  49. Xu JH, Liu Q, Hu W, Wang T, Xue Q, Messing J (2015) Dynamics of chloroplast genomes in green plants. Genomics 106:221–231. https://doi.org/10.1016/j.ygeno.2015.07.004

    CAS  Article  PubMed  Google Scholar 

  50. Xu X, Wen J, Wang W, Zheng W (2018) The complete chloroplast genome of the threatened Prunus cerasoides, a rare winter blooming cherry in the Himalayan region. Conserv Genet Resour 10:499–502. https://doi.org/10.1007/s12686-017-0859-1

    Article  Google Scholar 

  51. Xue S, Shi T, Luo WJ et al (2019) Comparative analysis of the complete chloroplast genome among Prunus mume, P. armeniaca, and P. salicina. Hortic Res 6:89. https://doi.org/10.1038/s41438-019-0171-1

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. Zang M et al (2019) Complete chloroplast genome of Fokienia hodginsii (Dunn) Henry et Thomas: insights into repeat regions variation and phylogenetic relationships in Cupressophyta. Forests 10:528. https://doi.org/10.3390/f10070528

    Article  Google Scholar 

  53. Zhang Y, Du L, Liu A et al (2016) The complete chloroplast genome sequences of five epimedium species: lights into phylogenetic and taxonomic analyses. Front Plant Sci 7:306. https://doi.org/10.3389/fpls.2016.00306

    Article  PubMed  PubMed Central  Google Scholar 

  54. Zhang X, Rong C, Qin L, Mo C, Fan L, Yan J, Zhang M (2018a) Complete chloroplast genome sequence of Malus hupehensis: genome structure, comparative analysis, and phylogenetic relationships. Molecules 23:2917. https://doi.org/10.3390/molecules23112917

    CAS  Article  PubMed Central  Google Scholar 

  55. Zhang X, Yan J, Ling Q, Fan L, Zhang M (2018b) Complete chloroplast genome sequence of Prunus davidiana (Rosaceae). Mitochondrial DNA B 3:888–889. https://doi.org/10.1080/23802359.2018.1501325

    Article  Google Scholar 

  56. Zhao X, Yan M, Ding Y, Huo Y, Yuan Z (2019) Characterization and comparative analysis of the complete chloroplast genome sequence from Prunus avium ‘Summit’. PeerJ 7:e8210. https://doi.org/10.7717/peerj.8210

    Article  PubMed  PubMed Central  Google Scholar 

  57. Zoschke R, Bock R (2018) Chloroplast translation: structural and functional organization, operational control, and regulation. Plant Cell 30:745. https://doi.org/10.1105/tpc.18.00016

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This research was supported by Science and Technology Project of Qinghai Province (2019-ZJ-962Q; 2017-NK-151; 2016-ZJ-Y01), The Open Project of State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University (2019-ZZ-05), and The Youth Foundation of Qinghai University (2019-QNY-2).

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Conceptualization: LW; Data Curation: LW, LW and QS; Formal Analysis: WS and ZG; Resources: LW; Writing-Original Draft Preparation: LW; Writing-Review and Editing: LW; Funding Acquisition: LW, WS, and QS.

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Correspondence to Le Wang.

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Wang, L., Guo, Z., Shang, Q. et al. The complete chloroplast genome of Prunus triloba var. plena and comparative analysis of Prunus species: genome structure, sequence divergence, and phylogenetic analysis. Braz. J. Bot 44, 85–95 (2021). https://doi.org/10.1007/s40415-020-00685-6

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Keywords

  • Comparative genomics
  • Molecular marker
  • Phylogenomics
  • Plastome assembly