Abstract
Acer L. (Sapindaceae) consists of approximately 200 species, with great ornamental and commercial values. However, due to a substantial divergence in inflorescence, leaf shape, and fruit shape during the process of long-term natural evolution, it is remarkably difficult to distinguish them by morphological features. Eight species with compound-leaved maples from Sect. Trifoliata, Pentaphylla, and Negundo play an important role in revealing the morphological variation of Acer. Hence, the complete chloroplast (cp) genomes of all eight compound-leaved maples native to Asia were characterized, and comparative genomic analysis was conducted to infer their phylogenetic relationships. A few differences were found in cp genome size and gene content among eight Acer species. The gene rps2 was only identified in A. griseum. The differences in the cp genome sequences among eight Acer species have been clearly demonstrated, where matK-rps16, trnE-trnT, ndhC-trnV, ccsA-ndhD, and ycf1-trnN were the most divergent regions. The phylogenetic analysis revealed that Acer was clustered into monophyly by 100% bootstrap values, with A. glabrum (Sect. Glabra) and A. pseudoplatanus (Sect. Palmata) as the most basic species. Except for A. henryi and A. negundo, seven compound-leaved maples and some simple-leaved maples were highly supported to cluster into one clade with A. sutchuenense as the primitive species of Sect. Trifoliata and A. pentaphyllum as a series (Ser. Pentaphylla) of Sect. Pentaphylla. Besides, it is speculated by plastid phylogeny reconstruction that A. cissifolium (Sect. Negundo) may have ancestral connections with A. triflorum (Sect. Trifoliata). Finally, we conjectured that compound-leaved maples may have evolved from simple-leaved maples.
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Data availability
Sequence data of eight Acer species generated in this study were submitted to GenBank of NCBI (https://www.ncbi.nlm.nih.gov/) with the accession numbers MN602455, MT216760-MT216765, and MT355072.
Change history
22 July 2022
Handling editor name correction.
11 February 2022
A Correction to this paper has been published: https://doi.org/10.1007/s11295-022-01545-y
References
Abdullah MF, Shahzadi I, Waseem S, Mirza B, Ahmed I, Waheed MT (2019) Chloroplast genome of Hibiscus rosa-sinensis (Malvaceae): comparative analyses and identification of mutational hotspots. Genomics 112(1):581–591. https://doi.org/10.1016/j.ygeno.2019.04.010
Andrews S (2015) FastQC: a quality control tool for high throughput sequence data. available online: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (accessed on 6 October 2019).
Anton B, Sergey N, Dmitry A, Alexey AG, Mikhail D, Alexander SK, Valery ML, Sergey IN, Son P, Andrey DP, Alexey VP, Alexander VS, Nikolay V, Glenn T, Max AA, Pavel AP (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
APG IV (2016) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants. Botanical Journal of the Linnean Society 181. https://doi.org/10.1111/boj.12385
Areces-Berazain F, Wang Y, Hinsinger DD, Strijk JS (2020) Plastome comparative genomics in maples resolves the infrageneric backbone relationships. PeerJ 8:e9483. https://doi.org/10.7717/peerj.9483
Arroyo-García R, Lefort F, Andrés MTD, Ibáñez J, Borrego J, Jouve N, Cabello F, Martínez-Zapater JM (2002) Chloroplast microsatellite polymorphisms in Vitis species. Genome 45:1142–1149. https://doi.org/10.1139/g02-087
Barstow M, Wang K, Crowley D (2019) Acer pentaphyllum. The IUCN red list of threatened species 2019: e.T193850A2285958. https://doi.org/10.2305/IUCN.UK.2019-1.RLTS.T193850A2285958.en. Accessed on 20 January 2022.
Bayly MJ, Rigault P, Spokevicius A, Ladiges PY, Ades PK, Anderson C, Bossinger G, Merchant A, Udovicic F, Woodrow IE (2013) Chloroplast genome analysis of Australian eucalypts-Eucalyptus, Corymbia, Angophora, Allosyncarpia and Stockwellia (Myrtaceae). Mol Phylogenet Evol 69:704–716. https://doi.org/10.1016/j.ympev.2013.07.006
Besnard G, Rubio de Casas R, Vargas P (2007) Plastid and nuclear DNA polymorphism reveals historical processes of isolation and reticulation in the olive tree complex (Olea europaea). J Biogeogr 34:736–752. https://doi.org/10.1136/adc.2006.104885
Bi W, Gao Y, Shen J, He CN, Liu HB, Peng Y, Zhang CH, Xiao PG (2016) Traditional uses, phytochemistry, andpharmacology of the genus Acer (maple): a review. J Ethnopharmacol 189:31–60. https://doi.org/10.1016/j.jep.2016.04.021
Birky CW (1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci 92:11331–11338. https://doi.org/10.1073/pnas.92.25.11331
Bock R (2007) Structure, function, and inheritance of plastid genomes. Top Curr Genet 19:29–63. https://doi.org/10.1007/4735_2007_0223
Clegg MT, Gaut BS, Learn GH, Morton BR (1994) Rates and patterns of chloroplast DNA evolution. Proc Natl Acad Sci 91:6795–6801. https://doi.org/10.2307/2365166
Crowley D (2020) Acer sutchuenense. The IUCN red list of threatened species 2020: e.T193876A2288054. https://doi.org/10.2305/IUCN.UK.2020-1.RLTS.T193876A2288054.en. Accessed on 20 January 2022.
Drouin G, Daoud H, Xia JN (2008) Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Mol Phylogenet Evol 49:827–831. https://doi.org/10.1016/j.ympev.2008.09.009
Du Y, Bi Y, Yang F, Zhang M, Chen X, Xue J, Zhang X (2017) Complete chloroplast genome sequences of Lilium: insights into evolutionary dynamics and phylogenetic analyses. Scientific Reports 7. https://doi.org/10.1038/s41598-017-06210-2
Fang PW (1981) Flora of China, vol 46. Science Press, Beijing (in Chinese)
Fu QD, Yu XD, Xia XH, Zheng YQ, Zhang CH (2020) Complete chloroplast genome sequence of Acer nikoense (Sapindaceae). Mitochondrial DNA Part B 5(3):3118–3119. https://doi.org/10.1080/23802359.2020.1797574
Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I (2004) VISTA: computational tools for comparative genomics. Nucleic Acids Res 32:273–279. https://doi.org/10.1093/nar/gkh458
Gitzendanner MA, Soltis PS, Wong GKS, Ruhfel BR, Soltis DE (2018) Plastid phylogenomic analysis of green plants: a billion years of evolutionary history. Am J Bot 105:291–301. https://doi.org/10.1002/ajb2.1048
Green BR (2011) Chloroplast genomes of photosynthetic eukaryotes. Plant J 66:34–44. https://doi.org/10.1111/j.1365-313x.2011.04541.x
Guo LC, Zhao MM, Sun W, Teng hl, Huang BS, Zhao XP, (2016) Differentiation of the Chinese minority medicinal plant genus Berchemia spp. by evaluating three candidate barcodes. Springerplus 5:1–10. https://doi.org/10.1186/s40064-016-2207-4
Haddad B, Gristina AS, Mercati F, Saadi AE, Aiter N, Martorana A, Sharaf A, Carimi F (2020) Molecular analysis of the official Algerian olive collection highlighted a hotspot of biodiversity in the central Mediterranean basin. Genes 11. https://doi.org/10.3390/genes11030303
Harris JGS (1975) Tree genera—3. Acer—of the maple [J]. Arboricultural Journal: the International Journal of Urban Forestry 2:361–369. https://doi.org/10.1080/03071375.1975.0590443
Hong SY, Cheon KS, Yoo KO, Lee HO, Cho K, Suh JT, Kim SJ, Nam JH, Sohn HB, Kim YH (2017) Complete chloroplast genome sequences and comparative analysis of Chenopodium quinoa and C. album. Frontiers in Plant Science. 8:1696. https://doi.org/10.3389/fpls.2017.01696
Khan G, Nolzen J, Schepker H, Albach DC (2021) Incongruent phylogenies and its implications for the study of diversification, taxonomy and genome size evolution of Rhododendron. Am J Bot 108(10):1957–1981. https://doi.org/10.1002/ajb2.1747
Kitamura A, Kimoto K (2006) History of the inflow of the warm Tsushima current into the Sea of Japan between 3.5 and 0.8 Ma. Palaeogeogr Palaeoclimatol Palaeoecol 236:355–366. https://doi.org/10.1016/j.palaeo.2005.11.015
Kramina TE, Degtjareva GV, Samigullin TH, Valiejo-Roman CM, Kirkbride JJH, Volis S, Deng T, Sokoloff DD (2016) Phylogeny of Lotus (Leguminosae: Loteae): partial incongruence between nrITS, nrETS and plastid markers and biogeographic implications. Taxon 65(5):997–1018. https://doi.org/10.12705/655.4
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. https://doi.org/10.1093/nar/29.22.4633
Li JH, Stukel M, Bussies P, Skinner K, Lemmon AR, Lemmon EM, Brown K, Bekmetjev A, Swenson NG (2019) Maple phylogeny and biogeography inferred from phylogenomic data. J Syst Evol 57(6):594–606. https://doi.org/10.1111/jse.12535
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Lin L, Lin LJ, Zhu ZY, Ding YL, Kuai BK (2017) Studies on the taxonomy and molecular phylogeny of Acer in China. Acta Horticulturae Sinica 44:1535–1547. https://doi.org/10.16420/j.issn.0513-353x.2016-0912 (in Chinese)
Liu HY, Yu Y, Deng YQ, Li J, Huang ZX, Zhou SD (2018) The chloroplast genome of Lilium henrici: genome structure and comparative analysis. Molecules 23. https://doi.org/10.3390/molecules23061276
Lohse M, Drechsel O, Kahlau S, Bock R (2013) Organellar genome DRAW-a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Res 41:W575. https://doi.org/10.3390/10.1093/nar/gkt289
Ma HL, Zhu ZB, Zhang XM, Miao YY, Guo QS (2014) Species identification of the medicinal plant Tulipa edulis (Liliaceae) by DNA barcode marker. Biochem Syst Ecol 55:362–368. https://doi.org/10.1016/j.bse.2014.03.038
Ma QY, Wang YN, Zhu L, Bi CW, Li SX, Li SS, Wen J, Yan KY, Li QZ (2019) Characterization of the complete chloroplast genome of Acer truncatum Bunge (Sapindales: Aceraceae): a new woody oil tree species producing nervonic acid. Biomed Res Int 11:1–3. https://doi.org/10.1155/2019/7417239
Mai DH (1984) Die endokarpien bei der gattung Acer L. (Aceraceae)-Eine biosystematische studie. Gleditschia 11:17–46
Maruyama S, Isozaki Y, Kimura G, Terabayashi M (1997) Paleogeographic maps of the Japanese islands: plate tectonic synthesis from 750 Ma to the present. Island A Rc 6:121–142. https://doi.org/10.1111/j.1440-1738.1997.tb00043.x
Mohamed A, Ragab MF, Kareem AM, Mohamed H, Fawzy AEF (2017) Identification of effective DNA barcodes for Triticum plants through chloroplast genome-wide analysis. Comput Biol Chem 71:20–31. https://doi.org/10.1016/j.compbiolchem.2017.09.003
Nakamura T, Yamada KD, Tomii K, Katoh K (2018) Parallelization of MAFFT for large-scale multiple sequence alignments. Bioinformatics 34:2490–2492. https://doi.org/10.1093/bioinformatics/bty121
Pang XB, Liu HS, Wu SR, Yuan YC, Li HJ, Dong JS, Liu ZH, An CZ, Su ZH, Li B (2019) Species identification of oaks (Quercus L., Fagaceae) from gene to genome. International Journal of Molecular Sciences 20(23):5940. https://doi.org/10.3390/ijms20235940
Reboud X, Zeyl C (1994) Organelle inheritance in plants. Heredity 72:13–140. https://doi.org/10.1038/hdy.1994.19
Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577. https://doi.org/10.1080/10635150701472164
Thiel T, Michalek W, Varshney RK, 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. https://doi.org/10.1007/s00122-002-1031-0
Tian X, Guo ZH, Li DZ (2002) Phylogeny of Aceraceae based on ITS and trnL-F data sets. Acta Botanica Sinica 6:714–724. https://doi.org/10.3321/j.issn:1672-9072.2002.06.015
Trifinopoulos J, Nguyen LT, von Haeseler A, Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 44(W1):W232–W235. https://doi.org/10.1093/nar/gkw256
Van Gelderen D M, de Jong P C, Oterdoom H J (1994) Maples of the world. Timber press, Portland, p 63–238
Wang W, Chen S, Zhang X (2020) Complete plastomes of 17 species of maples (Sapindaceae: Acer): comparative analyses and phylogenomic implications. Plant Syst Evol 306(3):61. https://doi.org/10.1007/s00606-020-01690-8
Wei BY (2019) The phylogeny study of Acer L. sect. Trifoliata Pax. Northeast Normal University, Changchun, p 24–25. (in Chinese)
Wolfe KH, Li W-H, Sharp PM (2009) Rates of nucleotide substitutionvary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci 84:9054–9058. https://doi.org/10.1073/pnas.84.24.9054
Wyman SK, Jansen RK, Boore JL (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20(17):3252–3255. https://doi.org/10.1093/bioinformatics/bth352
Xia XH, Yu XD, Fu QD, Zheng YQ, Zhang CH (2020) Complete chloroplast genome sequence of the three-flowered maple, Acer triflorum (Sapindaceae). Mitochondrial DNA Part B 5(2):1859–1860. https://doi.org/10.1080/23802359.2020.1751000
Xu TZ (1998) The systematic evolution and distribution of the genus Acer. Acta Botanica Yunnan 20(4):393 (in Chinese)
Xu TZ, Chen YS, de Jong PC, Oterdoom HJ, Chang CS (2008) Flora of China: Oxalidaceae through Aceraceae. Science Press, Beijing/Missouri Botanical Garden Press, St. Louis, pp 516–553
Xu C, Dong WP, Li WQ, Lu YZ, Xie XM, Jin XB, Shi JP, He KH, Suo ZL (2017) Comparative analysis of six Lagerstroemia complete chloroplast genomes. Front Plant Sci 8:15. https://doi.org/10.3389/fpls.2017.00015
Yu T, Gao J, Huang BH, Dayananda B, Ma WB, Zhang YY, Liao PC, Li JQ (2020) Comparative plastome analyses and phylogenetic applications of the Acer section Platanoidea. Forests 11(4):462. https://doi.org/10.3390/f11040462
Yurina NP, Sharapova LS, Odintsova MS (2017) Structure of plastid genomes of photosynthetic eukaryotes. Biochem Mosc 82:678–691. https://doi.org/10.1134/S0006297917060049
Zhao JT, Xu Y, Xi LJ, Yang JW, Chen HW, Zhang J (2018) Characterization of the chloroplast genome sequence of Acer miaotaiense: comparative and phylogenetic analyse. Molecules 23:1740. https://doi.org/10.3390/molecules23071740
Zhou T, Ruhsam M, Wang J, Zhu H, Li WL, Zhang X, Xu YC, Xu FS, Wang XM (2019) The complete chloroplast genome of Euphrasia regelii, pseudogenization of ndh genes and the phylogenetic relationships within Orobanchaceae. Front Genet 10:444. https://doi.org/10.3389/fgene.2019.00444
Zhou T, Zhu H, Wang J, Xu YC (2020) Complete chloroplast genome sequence determination of Rheum species and comparative chloroplast genomics for the members of Rumiceae. Plant Cell Reports 39(6). https://doi.org/10.1007/s00299-020-02532-0
Zhang W, Xia XH, Chen DF, Li JY, He W, Ma WB, Wu BX, Zheng YQ, Zhang CH (2020) Complete chloroplast genome sequence of Acer sutchuenense subsp tienchuanenge. (Sapindaceae). Mitochondrial DNA Part B 5(3):2886–2887. https://doi.org/10.1080/23802359.2020.1791002
Zheng Y, Zhang G, Wu WR (2011) Characterization and comparison of microsatellites in Gramineae. Genomics and Applied Biology 30(5):513–520. https://doi.org/10.3969/gab.030.000513(inChinese)
Zheng G, Wei LL, Ma L, Wu ZQ, Gu CH, Chen K (2020) Comparative analyses of chloroplast genomes from 13 Lagerstroemia (Lythraceae) species: identifcation of highly divergent regions and inference of phylogenetic relationships. Plant Mol Biol. https://doi.org/10.1007/s11103-020-00972-6
Acknowledgements
We are grateful to associate researcher Bin Li of Xi’an Botanical Garden and assistant researcher Wei Zhang of Sichuan Academy of Forestry for their help in the sample collection.
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This work was supported by the Fundamental Research Fund of CAF (CAFYBB2020ZB005-01).
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All authors commented on the previous versions of the manuscript. All authors read and approved the final manuscript.
Conceptualization: ZCH. Methodology: XXH. Formal analysis and investigation: XXH and FQD. Writing—original draft preparation: XXH and YXD. Writing—review and editing: XXH, YXD, ZCH, ZYX, and WYX. Funding acquisition: ZCH. Resources: FQD. Supervision: ZYQ.
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Xia, X., Yu, X., Fu, Q. et al. Comparison of chloroplast genomes of compound-leaved maples and phylogenetic inference with other Acer species. Tree Genetics & Genomes 18, 11 (2022). https://doi.org/10.1007/s11295-022-01541-2
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DOI: https://doi.org/10.1007/s11295-022-01541-2