Abstract
Annonaceae is the largest family in Magnoliales, exhibiting the greatest diversity among and within genera. In this study, we conducted an analysis of repetitive sequences and codon usage bias in the previously acquired plastome of Miliusa glochidioides. Using a concatenated dataset of shared genes, we constructed the phylogenetic relationships among 27 Annonaceae species. The results showed that the size of the plastomes in the Annonaceae ranged from 159 to 202 kb, with the size of the inverted repeat region ranging from 40 to 65 kb. Within the plastome of M. glochidioides, we identified 42 SSRs, 36 tandem repeats, and 9 dispersed repeats. These SSRs consist of three nucleotide types and eight motif types, with a preference for A/T bases, primarily located in the large single-copy regions and intergenic spacers. Tandem and dispersed repeat sequences were predominantly detected in the IR region. Through codon usage bias analysis, we identified 30 high-frequency codons and 11 optimal codons. The plastome of M. glochidioides demonstrated relatively weak codon usage bias, favoring codons with A/T endings, primarily influenced by natural selection. Phylogenetic analysis revealed that all four subfamilies formed monophyletic groups, with Cananga odorata (Ambavioideae) and Anaxagorea javanica (Anaxagoreoideae) successively nested outside Annonoideae + Malmeoideae. These findings improve our understanding of the plastome of M. glochidioides and provide additional insights for studying plastome evolution in Annonaceae.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10528-024-10874-7/MediaObjects/10528_2024_10874_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10528-024-10874-7/MediaObjects/10528_2024_10874_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10528-024-10874-7/MediaObjects/10528_2024_10874_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10528-024-10874-7/MediaObjects/10528_2024_10874_Fig4_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10528-024-10874-7/MediaObjects/10528_2024_10874_Fig5_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10528-024-10874-7/MediaObjects/10528_2024_10874_Fig6_HTML.png)
Data Availability
The data source is the NCBI database: https://www.ncbi.nlm.nih.gov/nuccore/MN241494,MN241495,KU563738,MT742547,MN241491,MK087989,MT742546,MN241496,MN253545,MN241488,MN241489,MH992130,MN241490,MW136266,MW829282,MZ936420,OK216144,MN253543,MN253544,OL979152,OM047203,OM914484,OM937139,MW018366,MK035708,MN016933,MK087990,NC_037005,NC_030504, (accessed on 1 June 2023). Data is provided within the manuscript or supplementary information files.
References
Amenu SG, Wei N, Wu L, Oyebanji O, Hu GW, Zhou YD, Wang QF (2022) Phylogenomic and comparative analyses of Coffeeae alliance (Rubiaceae): deep insights into phylogenetic relationships and plastome evolution. BMC Plant Biol 22:88
Athey J, Alexaki A, Osipova E, Rostovtsev A, Santana-Quintero LV, Katneni U, Simonyan V, Kimchi-Sarfaty C (2017) A new and updated resource for codon usage tables. BMC Bioinform 18:391
Beier S, Thiel T, Münch T, Scholz U, Mascher M (2017) MISA–web: a web server for microsatellite prediction. Bioinformatics 33(16):2583–2585
Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580
Cai C, Wang LK, Jiang T, Zhou LJ, He PM, Jiao BH (2017) Complete chloroplast genome of green tide algae Ulva flexuosa (Ulvophyceae, Chlorophyta) with comparative analysis. PLoS ONE 12:e0184196
Cauz-Santos LA, da Costa ZP, Callot C, Cauet S, Zucchi MI, Bergès H, van den Berg C, Vieira MLC (2020) A repertory of rearrangements and the loss of an inverted repeat region in Passiflora chloroplast genomes. Genome Biol Evol 12:1841–1857
Chakraborty S, Yengkhom S, Uddin A (2020) Analysis of codon usage bias of chloroplast genes in Oryza species. Planta 252:67
Chaowasku T, Johnson DM, van der Ham RWJM, Chatrou LW (2015) Huberantha, a substitution name for Hubera (Annonaceae—Malmeoideae—Miliuseae). Kew Bull 70:23
Chaowasku T, Damthongdee A, Jongsook H, Nuraliev MS, Ngo D, Le HT, Lithanatudom P, Osathanunkul M, Deroin T, Xue B et al (2018) Genus Huberantha (Annonaceae) revisited: erection of Polyalthiopsis, a new genus for H. floribunda, with a new combination H. luensis. Ann Bot Fenn 55:121–136
Chatrou LW, Pirie MD, Erkens RHJ, Couvreur TLP, Neubig KM, Abbott JR, Mols JB, Maas JW, Saunders MK, Chase MW (2012) A new subfamilial and tribal classification of the pantropical plant family Annonaceae informed by molecular phylogenetics. Bot J Linn Soc 169:5–40
Chatrou LW, Turner IM, Klitgaard BB, Maas PJ, Utteridge T (2018) A linear sequence to facilitate curation of herbarium specimens of Annonaceae. Kew Bull 73:1–10
Chaw SM, Wu CS, Sudianto E (2018) Evolution of gymnosperm plastid genomes. Adv Bot Res 85:195–222
Chmielewski M, Meyza K, Chybicki IJ, Dzialuk A, Litkowiec M, Burczyk J (2015) Chloroplast microsatellites as a tool for phylogeographic studies: the case of white oaks in poland. Iforest 8:765
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
Couvreur TL, Pirie MD, Chatrou LW, Saunders RM, Su YC, Richardson JE, Erkens RH (2011) Early evolutionary history of the flowering plant family Annonaceae: Steady diversification and boreotropical geodispersal. J Biogeogr 38:664–680
Dugas DV, Hernandez D, Koenen EJ, Schwarz E, Straub S, Hughes CE, Jansen RK, Nageswara-Rao M, Staats M, Trujillo JT et al (2015) Mimosoid legume plastome evolution: IR expansion, tandem repeat expansions and accelerated rate of evolution in clpP. Sci Rep 5:1–13
Fages-Lartaud M, Hundvin K, Hohmann-Marriott MF (2022) Mechanisms governing codon usage bias and the implications for protein expression in the chloroplast of Chlamydomonas reinhardtii. Plant J 112:919–945
Fasanella M, Souto CP, Premoli AC (2020) Preliminary cross–genera transferability of SSRs among threatened South American Cupressaceae. N Z J Bot 58:153–166
Gan YY, Xu FX (2018) The coexistence of bicellular and tricellular pollen. Grana 58:129–132
Gan YY, Liu Y, Xu FX (2015) Pollen morphology of selected species from Annonaceae. Grana 54:271–281
Gan Y, Zhang Q, ** J (2022) The complete chloroplast genome of Miliusa glochidioides (Annonaceae) and phylogenetic analysis. Mitochondrial DNA B 7:1604–1605
Gao R, Wang WZ, Huang QY, Fan RF, Wang X, Feng P, Zhao GM, Bian S, Ren HL, Chang Y (2018) Complete chloroplast genome sequence of Dryopteris fragrans (L.) Schott and the repeat structures against the thermal environment. Sci Rep 8:1–11
Goulding SE, Wolfe KH, Olmstead RG, Morden CW (1996) Ebb and flow of the chloroplast inverted repeat. Mol Genet Genomics 252:195–206
Gui L, Jiang S, **e D, Yu L, Huang Y, Zhang Z, Liu Y (2020) Analysis of complete chloroplast genomes of Curcuma and the contribution to phylogeny and adaptive evolution. Gene 732:144355
Guo X, Tang CC, Thomas DC, Couvreur TL, Saunders RM (2017) A mega–phylogeny of the Annonaceae: taxonomic placement of five enigmatic genera and support for a new tribe, Phoenicantheae. Sci Rep 7:1–11
Huang CY, Yin QY, Khadka D, Meng KK, Fan Q, Chen SF, Liao WB (2019) Identification and development of microsatellite (SSRs) makers of Exbucklandia (Hamamelidaceae) by high–throughput sequencing. Mol Biol Rep 46:3381–3386
Ingvarsson PK (2008) Molecular evolution of synonymous codon usage in Populus. BMC Evol Biol 8:307
** DM, Wicke S, Gan L, Yang JB, ** JJ, Yi TS (2020) The loss of the inverted repeat in the putranjivoid clade of Malpighiales. Front Plant Sci. https://doi.org/10.3389/fpls.2020.00942
Karnkowska A, Bennett MS, Triemer RE (2018) Dynamic evolution of inverted repeats in Euglenophyta plastid genomes. Sci Rep 8:1–10
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649
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
Kurtz S, Schleiermacher C (1999) REPuter: fast computation of maximal repeats in complete genomes. Bioinformatics 15:426–427
Lei JM, Liang ZR, Zhang H, Lim YQ, Xue BE (2022) Advances in exploitation and utilization of wild fruit resources of Annonaceae in China. J Fruit Sci 39:121–130 (in Chinese)
Li Q, Wei R (2022) Comparison of boraginales plastomes: insights into codon usage bias, adaptive evolution, and phylogenetic relationships. Diversity 14:1104
Li X, Yang Y, Henry RJ, Rossetto M, Wang Y, Chen S (2015) Plant DNA barcoding: from gene to genome. Biol Rev 90:157–166
Li L, Hu YF, He M, Zhang B, Wu W, Cai PM, Huo D, Hong YC (2021a) Comparative chloroplast genomes: Insights into the evolution of the chloroplast genome of Camellia sinensis and the phylogeny of Camellia. BMC Genomics 22:138
Li XP, Zhao YM, Tu XD, Li CR, Zhu YT, Zhong ZJ, Wu SS, Zhai JW (2021b) Comparative analysis of plastomes in Oxalidaceae: phylogenetic relationships and potential molecular markers. Plant Divers 43:281–291
Li G, Zhang L, Xue P (2021c) Codon usage pattern and genetic diversity in chloroplast genomes of Panicum species. Gene 802:145866
Li ZZ, Lehtonen S, Chen JM (2023) The dynamic history of plastome structure across aquatic subclass Alismatidae. BMC Plant Biol 23:125
Liu Q (2012) Mutational bias and translational selection sha** the codon usage pattern of tissue–specific genes in rice. PLoS ONE 7:e48295
Liu Y (2020) A code within the genetic code: codon usage regulates co–translational protein folding. Cell Commun Signal 18:145
Liu SS, Wang Z, Su YJ, Wang T (2021) Comparative genomic analysis of Polypodiaceae chloroplasts reveals fine structural features and dynamic insertion sequences. BMC Plant Biol 21:1–15
Maas PJM, Westra LYT, Guerrero SA, Lobão AQ, Scharf U, Zamora NA, Erkens RHJ (2015) Confronting a morphological nightmare: revision of the neotropical genus Guatteria (Annonaceae). Blumea-Bio Evol Biogeogra Plants 60:1–219
Mazumdar P, Othman RB, Mebus K, Ramakrishnan N, Harikrishna JA (2017) Codon usage and codon pair patterns in non–grass monocot genomes. Ann Bot-London 120:893909
Mols JB, Gravendeel B, Chatrou LW, Pirie MD, Bygrave PC, Chase MW, Keßler PJ (2004) Identifying clades in Asian Annonaceae: monophyletic genera in the polyphyletic Miliuseae. Am J Bot 91:590–600
Mower JP, Vickrey TL (2018) Structural diversity among plastid genomes of land plants. Adv Bot Res 85:263–292
Ortiz-Rodriguez AE, Ornelas JF, Ruiz-Sanchez E (2018) A jungle tale: molecular phylogeny and divergence time estimates of the Desmopsis-Stenanona clade (Annonaceae) in Mesoamerica. Mol Phylogenet Evol 122:80–94
Parvathy ST, Udayasuriyan V, Bhadana V (2022) Codon usage bias. Mol Biol Rep 49:539–565
** JY, Feng PP, Li JY, Zhang RJ, Su YJ, Wang T (2021a) Molecular evolution and SSRs analysis based on the chloroplast genome of Callitropsis funebris. Ecol Evol 11:4786–4802
** JY, Feng PP, Hao J, Li JY, Su YJ, Wang T (2021b) The molecular evolution pattern of rps12 gene in gymnosperms. Chin Sci Bull 66:3182–3193 (in Chinese)
** JY, Zhong XN, Wang T, Su YJ (2023) Structural characterization of Trivalvaria costata chloroplast genome and molecular evolution of rps12 gene in Magnoliids. Forests 14:1101
Punyasena SW, Eshel G, McElwain JC (2008) The influence of climate on the spatial patterning of Neotropical plant families. J Biogeogr 35:117–130
Quax TE, Claassens NJ, Söll D, van der Oost J (2015) Codon bias as a means to fine–tune gene expression. Mol Cell 59:149–161
Raubeson LA, Jansen RK (1992) Chloroplast DNA evidence on the ancient evolutionary split in vascular land plants. Science 255:1697–1699
Raubeson LA, Jansen RK (2005) Chloroplast genomes of plants. In: Henry RJ (ed) Plant diversity and evolution: genotypic and phenotypic variation in higher plants. CAB International, London, pp 45–68
Ruhlman TA, Jansen RK (2014) The plastid genomes of flowering plants. In: Maliga P (ed) Chloroplast biotechnology: methods and protocols. Springer, New York, pp 3–38
Ruhlman TA, Zhang J, Blazier JC, Sabir JS, Jansen RK (2017) Recombination–dependent replication and gene conversion homogenize repeat sequences and diversify plastid genome structure. Am J Bot 104:559–572
Saunders RMK, Guo X, Tang CC (2020) Friesodielsia subaequalis (Annonaceae) a new nomenclatural combination following conservation of the generic name against Schefferomitra. Phytotaxa 464:183–184
Sauquet H, Doyle JA, Scharaschkin T, Borsch T, Hilu KW, Chatrou LW, Le Thomas A (2003) Phylogenetic analysis of Magnoliales and Myristicaceae based on multiple data sets: Implications for character evolution. Bot J Linn Soc 142:125–186
Sawicki J, Bączkiewicz A, Buczkowska K, Górski P, Krawczyk K, Mizia P, Myszczyński K, Ślipiko M, Szczecińska M (2020) The increase of simple sequence repeats during diversification of marchantiidae, an early land plant lineage, leads to the first known expansion of inverted repeats in the evolutionarily–stable structure of liverwort plastomes. Genes 11:299
Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallón S, Lupia R (2004) Ferns diversified in the shadow of angiosperms. Nature 428(6982):553–557
Stamatakis A (2014) RaxML version 8: a tool for phylogenetic analysis and post–analysis of large phylogeies. Bioinformatics 30:1312–1313
Tang D, Wei F, Cai Z, Wei Y, Khan A, Miao J, Wei K (2021) Analysis of codon usage bias and evolution in the chloroplast genome of Mesona chinensis Benth. Dev Genes Evol 231:1–9
Thomas DC, Surveswaran S, Xue B, Sankowsky G, Mols JB, Keßler PJ, Saunders RM (2012) Molecular phylogenetics and historical biogeography of the Meiogyne-Fitzalania clade (Annonaceae): generic paraphyly and late Miocene-Pliocene diversification in Australasia and the Pacific. Taxon 61:559–575
Tonti-Filippini J, Nevill PG, Dixon K, Small I (2017) What can we do with 1000 plastid genomes? Plant J 90:808–818
Wang Z, Cai Q, Wang Y, Li M, Wang C, Wang Z, Jiao C, Xu C, Wang H, Zhang Z (2022) Comparative analysis of codon bias in the chloroplast genomes of theaceae species. Fronteir Genet 13:824610
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 31:645–659
Wu S, Chen J, Li Y, Liu A, Li A, Yin M, Shrestha N, Liu J, Ren G (2021) Extensive genomic rearrangements mediated by repetitive sequences in plastomes of Medicago and its relatives. BMC Plant Biol 21:1–16
Xue B, Tan YH (2016) Excluding Miliusa velutina (Annonaceae) from Flora of China. Phytotaxa 282:166–169
Xue B, Ding HB, Yao G, Shao YY, Fan XJ, Tan YH (2020) From Polyalthia to Polyalthiopsis (Annonaceae): transfer of species enlarges a previously monotypic genus. PhytoKeys 148:71
Xue B, Nurmawati S, Xu Y, Li YQ (2021) Excluding the species Monoon fragrans (Annonaceae) from the flora of China. Phytotaxa 487:91–96
Zhou XM, Zhao J, Yang JJ, Le Péchon T, Zhang L, He ZR, Zhang LB (2022) Plastome structure, evolution, and phylogeny of Selaginella. Mol Phylogenet Evol 169:107410
Zhu AD, Guo WH, Gupta S, Fan WS, Mower JP (2016) Evolutionary dynamics of the plastid inverted repeat: the effects of expansion, contraction, and loss on substitution rates. New Phytol 209:1747–1756
Zhu M, Feng PP, ** 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 11:14327–14340
Acknowledgements
The authors thank Dr. **ao Chunfen for her assistance with material collection.
Funding
This work was funded by the National Natural Science Foundation of China (31800184).
Author information
Authors and Affiliations
Contributions
Y.G. designed the study and wrote the manuscript. J.P. analyzed the data and revised the manuscript. X.L. and C.P. analyzed some of the data and revised the manuscript. All authors read and contributed to the final version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Ethical Approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Informed Consent
All authors have read the manuscript and approved the submission.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Gan, Y., **, J., Liu, X. et al. Repetitive Sequences, Codon Usage Bias and Phylogenetic Analysis of the Plastome of Miliusa glochidioides. Biochem Genet (2024). https://doi.org/10.1007/s10528-024-10874-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10528-024-10874-7