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Chloroplast genome sequence of Begonia asteropyrifolia and comparative analysis with other related species

  • Genetics & Evolutionary Biology - Original Article
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Abstract

Begonia L. is the only species-rich genus in the Begoniaceae family, comprising more than recorded 2,000 species. However, most of the species in this genus are narrowly distributed, and the phylogenetic relationships of some Begonia sections are still unresolved. Begonia asteropyrifolia Y.M. Shui & W.H. Chen which belongs to the Begonia Sect. Coelocentrum has been listed as an endangered species in China. Due to a shortage of studies on the chloroplast genome of B. asteropyrifolia, studies of comparison and phylogeny with other related species were still scarce. Here, we sequenced the chloroplast genome of B. asteropyrifolia via the Illumina NovaSeq 6000 platform. The complete chloroplast genome of B. asteropyrifolia was 169,512 bp long with a typical circular quadripartite structure, containing a large single-copy (LSC) region (76,310 bp), a small single-copy (SSC) region (18,058 bp) and two inverted repeats (IR) regions (37,572 bp each). The chloroplast genome encoded 113 unique genes, containing 79 protein-coding genes, 30 tRNA genes, and four rRNA genes. The basic structure, gene content and organizations, and number of long repeats in B. asteropyrifolia are similar to previously reported congeneric species. A total of 5,759 (range 144 to 205) SSRs, 1,568 (49 each) long repeats, and 25 highly divergent regions (Pi > 0.03) were detected as candidate molecular markers for further population genetic study and species identification. Moreover, the phylogenetic analysis based on the chloroplast genomes strongly supported the division of 32 Begonia species into six groups related to geographical distribution, and the B. asteropyrifolia, Begonia ferox C.-I Peng & Yan Liu, Begonia gulongshanensis Y.M. Shui & W.H. Chen and Begonia arachnoidea C.-I Peng, Yan Liu & S.M. Ku are closely related and form one clade (Sect. Coelocentrum), which was a subclade in the Asian Clade D of Asian Begonia. Overall, the current study will be beneficial for designing new species-specific DNA markers for new species identification, evolutionary history, and conservation within Begonia.

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Data availability

The data that support the findings of this study are openly available in the NCBI database.

References

  • Amiryousefi A, Hyvönen J, Poczai P (2018) IRscope: an online program to visualize the junction sites of chloroplast genomes. Bioinformatics 34(17):3030–3031

    Article  CAS  PubMed  Google Scholar 

  • Ardi WH, Campos-Domínguez L, Chung KF, Dong WK, Drinkwater E, Fuller D, Gagul J, Garnett GJL, Girmansyah D et al (2022) Resolving phylogenetic and taxonomic conflict in Begonia. Edin J Bot 79(1928):1–28

    Google Scholar 

  • Beier S, Thiel T, Münch T, Scholz U, Mascher M (2017) MISA-web: A web server for microsatellite prediction. Bioinformatics 33:2583–2585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chakraborty S, Yengkhom S, Uddin A (2020) Analysis of codon usage bias of chloroplast genes in Oryza species. Planta 252:67

    Article  CAS  PubMed  Google Scholar 

  • Chumley TW, Palmer JD, Mower JP, Fourcade HM, Calie PJ, Boore JL, Jansen RK (2006) The complete chloroplast genome sequence of Pelargonium×hortorum: Organization and evolution of the largest and most highly rearranged chloroplast genome of land plants. Mol Biol Evol 23:2175–2190

    Article  CAS  PubMed  Google Scholar 

  • Clement WL, Tebbitt MC, Forrest LL et al (2004) Phylogenetic position and biogeography of Hillebrandia sandwicensis (Begoniaceae): a rare Hawaiian relict. Am J Bot 91(6):905–917

    Article  CAS  PubMed  Google Scholar 

  • Dierckxsens N, Mardulyn P, Smits G (2017) NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res 45(4):e18

    PubMed  Google Scholar 

  • Dong WP, Xu C, Li CH, Sun JH, Zuo YJ, Shi S, Cheng T, Guo JJ, Zhou SL (2015) ycf1 the most promising plastid DNA barcode of land plants. Sci Rep 5:8348

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid procedure for DNA purification from small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Forrest LL, Hughes M, Hollingsworth PM (2005) A phylogeny of Begonia using nuclear ribosomal sequence data and morphological characters. Syst Bot 30(3):671–682

    Article  Google Scholar 

  • Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I (2004) VISTA: computational tools for comparative genomics. Nucleic Acids Res 32:273–279

    Article  Google Scholar 

  • Gao L, Yi X, Yang YX, Su YJ, 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Guan KY, Yamaguchi H, Li JX, Li HZ, Ma H (2007) Traditional uses of begonias (Begoniaceae) in China. Acta Bot Yunnanica 29:58–66

    Google Scholar 

  • Guisinger MM, Kuehl JV, Boore JL, Jansen RK (2011) Extreme reconfiguration of plastid genomes in the angiosperm family Geraniaceae: Rearrangements, repeats, and codon usage. Mol Biol Evol 28:583–600

    Article  CAS  PubMed  Google Scholar 

  • Ivanova Z, Sablok G, Daskalova E, Zahmanova G, Apostolova E, Yahubyan G, Baev V (2017) Chloroplast genome analysis of resurrection tertiary relict Haberlea rhodopensis highlights genes important for desiccation stress response. Front Plant Sci 8:204

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiao Y, Jia HM, Li XW, Chai ML, Jia HJ, Chen Z, Wang GY, Chai CY et al (2012) Development of simple sequence repeat (SSR) markers from a genome survey of Chinese bayberry (Myrica rubra). BMC Genomics 13:201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780

    Article  CAS  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Wang ZH, Xing H, Chi XF, Chen SL, Gao QB (2019) The complete chloroplast genome of Saxifraga sinomontana (Saxifragaceae) and comparative analysis with other Saxifragaceae species. Braz J Bot 42:601–611

    Article  Google Scholar 

  • Li LF, Chen XL, Fang DM, Dong S, Guo X, Li N, Campos-Dominguez L, Wang W, Liu Y et al (2022) Genomes shed light on the evolution of Begonia, a mega-diverse genus. New Phytol 234:295–310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li QQ, Chen X, Yang DF, Xia PG (2023) Genetic relationship of Pleione based on the chloroplast genome. Gene 858:147203

    Article  CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Chang EM, Liu JF, Jiang ZP (2021) Comparative analysis of the complete chloroplast genomes of six white oaks with high ecological amplitude in China. J for Res 5:2203–2218

    Article  Google Scholar 

  • Luo RB, Liu BH, Xie YL, Li ZY, Huang WH, Yuan JY, He GZ, Chen YX, Pan Q, Liu YJ et al (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1:18

    Article  PubMed  PubMed Central  Google Scholar 

  • Moonlight PW, Ardi WH, Padilla LA, Chung KF, Fuller D, Girmansyah D, Hollands R, Jara-Muñoz A et al (2018) Dividing and conquering the fastest-growing genus: towards a natural sectional classification of the mega-diverse genus Begonia (Begoniaceae). Taxon 67(2):267–323

    Article  Google Scholar 

  • Nguyen LT, Schmidt HA, von Haeseler A et al (2014) IQ-TREE: a fast and efective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274

    Article  PubMed  PubMed Central  Google Scholar 

  • Nock CJ, Baten A, King GJ (2014) Complete chloroplast genome of Macadamia integrifolia confirms the position of the Gondwanan early-diverging eudicot family Proteaceae. BMC Genomic 15(Suppl 9):S13

    Article  Google Scholar 

  • Ogoma CA, Liu J, Stull GW, Wambulwa MC, Oyebanji O, Milne RI, Monro AK, Zhao Y, Li D-Z, Wu Z-Y (2022) Deep insights into the plastome evolution and phylogenetic relationships of the tribe Urticeae (Family Urticaceae). Front Plant Sci 13:870949

    Article  PubMed  PubMed Central  Google Scholar 

  • Pauwels M, Vekemans X, Godé C, Frérot H, Castric V, Saumitoul-aprade P (2012) Nuclear and chloroplast DNA phylogeography reveals vicariance among European populations of the model species for the study of metal tolerance, Arabidopsis halleri (Brassicaceae). New Phytol 193:916–928

    Article  CAS  PubMed  Google Scholar 

  • Pombert JF, Lemieux C, Turmel M (2006) The complete chloroplast DNA sequence of the green alga Oltmannsiellopsis viridis reveals a distinctive quadripartite architecture in the chloroplast genome of early diverging ulvophytes. BMC Biol 4(1):3

    Article  PubMed  PubMed Central  Google Scholar 

  • Qu XJ, Moore MJ, Li DZ, Yi TS (2019) PGA: a software package for rapid, accurate, and flexible batch annotation of plastomes. Plant Methods 15:50

    Article  PubMed  PubMed Central  Google Scholar 

  • Rajbhandary S (2015) Traditional Uses of Begonia Species (Begoniacae) in Nepal. J Nat Hist Mus 27:25–34

    Article  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Ren T, Yang YC, Zhou T, Liu ZL (2018) Comparative plastid genomes of Primula species: Sequence divergence and phylogenetic relationships. Int J Mol Sci 19(4):1050

    Article  PubMed  PubMed Central  Google Scholar 

  • Shen J, Zhang X, Jacob BL, Zhang HJ, Deng T, Sun H, Wang HC (2020) Plastome evolution in Dolomiaea (Asteraceae, Cardueae) using phylogenomic and comparative analyses. Front Plant Sci 11:376

    Article  PubMed  PubMed Central  Google Scholar 

  • Shi C, Liu Y, Huang H, Xia EH, Zhang HB, Gao LZ (2013) Contradiction between plastid gene transcription and function due to complex posttranscriptional splicing: an exemplary study of ycf15 function and evolution in Angiosperms. PLoS ONE 8(3):e59620

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Shui YM, Chen WH (2005) New data of sect coelocentrum (Begonia) in Begoniaceae. Acta Bot. Yunnanica 27(4):355–374

    Google Scholar 

  • Shui YM, Chen WH, Peng H, Huang SH, Liu ZW (2019) Taxonomy of Begonias. Yunnan Science and Technology Press, Kunming

    Google Scholar 

  • Somaratne Y, Guan DL, Wang WQ, Zhao L, Xu SQ (2019) Complete chloroplast genome sequence of Xanthium sibiricum provides useful DNA barcodes for future species identification and phylogeny. Plant Syst Evol 305:949–960

    Article  CAS  Google Scholar 

  • Tian DK, Xiao Y, Tong Y, Fu NF, Liu QQ, Li C (2018) Diversity and conservation of Chinese wild Begonias. Plant Diversity 40:75–90

    Article  PubMed  PubMed Central  Google Scholar 

  • Tian SB, Lu PL, Zhang ZH, Wu JQ, Zhang H, Shen HB (2021) Chloroplast genome sequence of Chongming lima bean (Phaseolus lunatus L.) and comparative analyses with other legume chloroplast genomes. BMC Genomics 22:194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tillich M, Lehwark P, Pellizzer T, Ulbricht-Jones ES, Fischer A, Bock R, Greiner S (2017) GeSeq – versatile and accurate annotation of organelle genomes. Nucleic Acids Res 45:W6–W11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tseng YH, Hsieh CL, Campos-Domínguez L, Hu AQ, Chang CC, Hsu YT, Kidner CA, Hughes M, Moonlight PW, Hung CH, Wang YC, Wang YT, Liu SH, Girmansyah D, Chung KF (2022) Insights into the evolution of the chloroplast genome and the phylogeny of Begonia. Edin J Bot 79(408):1–32

    Google Scholar 

  • Wang LY, Wang J, He CY, Zhang JG, Zeng YF (2021) Characterization and comparison of chloroplast genomes from two sympatric Hippophae species (Elaeagnaceae). J Forestry Res 32(1):307–318

    Article  CAS  Google Scholar 

  • Wang NJ, Chen SF, Xie L, Wang L, Feng YY, Lv T, Fang YM, Ding H (2022a) The complete chloroplast genomes of three Hamamelidaceae species: comparative and phylogenetic analyses. Eco and Evol 12:e8637

    Article  Google Scholar 

  • Wang ZJ, Cai QW, Wang Y, Li MH, Wang CC, Wang ZX, Jiao CY, Xu CC, Wang HY, Zhang ZL (2022b) Comparative analysis of codon bias in the chloroplast genomes of Theaceae species. Front Genet 13:824610

    Article  PubMed  PubMed Central  Google Scholar 

  • Weng ML, Blazier JC, Govindu M, Jansen RK (2014) Reconstruction of the ancestral plastid genome in Geraniaceae reveals a correlation between genome rearrangements, repeats, and nucleotide substitution rates. Mol Biol Evol 31(3):645–659

    Article  CAS  PubMed  Google Scholar 

  • Xie YP, Yang GG, Zhang C, Zhang XW, Jiang XF (2023) Comparative analysis of chloroplast genomes of endangered heterostylous species Primula wilsonii and its closely related species. Ecol Evol 13:e9730

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiong AS, Peng RH, Zhuang J, Gao F, Zhu B, Fu XY, Xue Y, Jin XF, Tian YS, Zhao W, Yao QH (2009) Gene duplication, transfer, and evolution in the chloroplast genome. Biotechnol Adv 27(4):340–347

    Article  CAS  PubMed  Google Scholar 

  • Xu WB, Xia BS, Li XW (2020) The complete chloroplast genome sequences of five pinnate-leaved Primula species and phylogenetic analyses. Sci Rep 10(1):20782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang J, Vázquez L, Chen XD, Li HM, Zhang H, Liu ZL, Zhao GF (2017) Development of chloroplast and nuclear DNA markers for Chinese oaks (Quercus subgenus Quercus) and assessment of their utility as DNA barcodes. Front Plant Sci 8:816

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang XM, Zhou TT, Su XY, Wang GB, Zhang XH, Guo QR, Cao FL (2021) Structural characterization and comparative analysis of the chloroplast genome of Ginkgo biloba and other gymnosperms. J for Res 32:765–778

    Article  CAS  Google Scholar 

  • Yao XH, Tang P, Li ZZ, Li DW, Liu YF, Huang HW (2015) The first complete chloroplast genome sequences in Actinidiaceae: genome structure and comparative analysis. PLoS ONE 10:e0129347

    Article  PubMed  PubMed Central  Google Scholar 

  • Zheng S, Poczai P, Hyvönen J, Tang J, Amiryousefi A (2020) Chloroplot: an online program for the versatile plotting of organelle genomes. Front Genet 25(11):576124

    Article  Google Scholar 

  • Zhu M, Feng PP, Ping JY, Li JY, Su YJ, Wang T (2021) Phylogenetic significance of the characteristics of simple sequence repeats at the genus level based on the complete chloroplast genome sequences of Cyatheaceae. Ecol Evol 00:1–14

    Google Scholar 

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Acknowledgements

This work was supported by the Guangxi Natural Science Foundation Program, China [2020GXNSFBA159052], the Guangxi Science and Technology Base and Special Talents Program, China [guike AD20325009] and the National Natural Science Foundation of China [31960083].

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Q.F.L. collected the sample and analyzed the data. W.H.L. provided research idea and supervised the experiments and research documentation. Q.F.L. and W.H.L. wrote the article. All authors read and approved the manuscript.

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Correspondence to Wenhua Luo.

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Lu, Q., Luo, W. Chloroplast genome sequence of Begonia asteropyrifolia and comparative analysis with other related species. Braz. J. Bot 47, 105–117 (2024). https://doi.org/10.1007/s40415-023-00969-7

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