Abstract
Main conclusion
This study reported 13 new plastomes from Aeonium and Monanthes , and observed new markers for phylogeny and DNA barcoding, such as novel tRNA structures and codon usage bias and aversion.
Abstract
The Macaronesian clade of Crassulaceae consists of three genera: Aichryson, with about 15 species; Monanthes, with about 10 species; Aeonium, with about 40 species. Within this clade, Aeonium, known as “the botanical equivalent of Darwin’s finches”, is regarded as an excellent model plant for researching adaptive evolution. Differing from the well-resolved relationships among three genera of the Macaronesian clade, the internal branching patterns within the genus Aeonium are largely unclear. In this study, we first reported 13 new plastomes from genus Aeonium and the closely related genus Monanthes. We further performed comprehensive analyses of the plastomes, with focuses on the secondary structures of pttRNAs and the patterns of codon usage and aversion. With a typical circular and quadripartite structure, the 13 plastomes ranged from 149,900 to 151,030 bp in size, and the unique pattern in IR junctions might become a family-specific marker for Crassulaceae species. Surprisingly, the π values of plastomes from Monanthes were almost twice those from Aeonium. Most importantly, we strongly recommend that highly polymorphic regions, novel putative pttRNA structures, patterns of codon usage bias and aversion derived from plastomes might have phylogenetic implications, and could act as new markers for DNA barcoding of plants. The results of phylogenetic analyses strongly supported a clear internal branching pattern in Macaronesian clade (represented by Aeonium and Monanthes), with higher nodal support values. The findings reported here will provide new insights into the variation of pttRNAs, and the patterns of codon usage and aversion of the family Crassulaceae.
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Data available statement
The 13 plastome sequence data generated in this study are available in GenBank of the National Center for Biotechnology Information (NCBI) (https://www.ncbi.nlm.nih.gov/nuccore) under the access numbers: OM993518-OM993530.
References
Abdullah MF, Shahzadi I, Waseem S, Mirza B, Ahmed I, Waheed MT (2020) 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
Amiryousefi A, Hyvönen J, Poczai P (2018) IRscope: an online program to visualize the junction sites of chloroplast genomes. Bioinformatics 34(17):3030–3031. https://doi.org/10.1093/bioinformatics/bty220
Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc. Accessed 15 Sept 2019
Baldwin BG, Crawford DJ, Francisco-Ortega J, Kim S-C, Sang T, Stuessy TF (1998) Molecular phylogenetic insights on the origin and evolution of oceanic island plants. In: Soltis DE (ed) Molecular systematics of plants II, 1st edn. Springer, Boston, pp 410–441
Berger A (1930) Crassulaceae. In: Engler A, Prantl K (eds) Die naturlichen Pflanzenfamilien, 2nd edn. W. Engelmann, Leipzig, pp 352–483
Bernhart SH, Hofacker IL, Will S, Gruber AR, Stadler PF (2008) RNAalifold: improved consensus structure prediction for RNA alignments. BMC Bioinform 9:474. https://doi.org/10.1186/1471-2105-9-474
Berry JO, Yerramsetty P, Zielinski AM, Mure CM (2013) Photosynthetic gene expression in higher plants. Photosynth Res 117:91–120. https://doi.org/10.1007/s11120-013-9880-8
Bi Y, Zhang MF, Xue J, Dong R, Du YP, Zhang XH (2018) Chloroplast genomic resources for phylogeny and DNA barcoding: a case study on Fritillaria. Sci Rep 8:1184. https://doi.org/10.1038/s41598-018-19591-9
Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10(4):e1003537. https://doi.org/10.1371/journal.pcbi.1003537
Brennan T, Sundaralingam M (1976) Structure, of transfer RNA molecules containing the long variable loop. Nucleic Acids Res 3(11):3235–3252. https://doi.org/10.1093/nar/3.11.3235
Chan PP, Lin BY, Mak AJ, Lowe TM (2021) tRNAscan-SE 2.0: improved detection and functional classification of transfer RNA genes. Nucleic Acids Res 49(16):9077–9096. https://doi.org/10.1093/nar/gkab688
Chase MW, Christenhusz M, Fay M, Byng J, Judd WS, Soltis D, Mabberley D, Sennikov A, Soltis PS, Stevens PF (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181(1):1–20. https://doi.org/10.1111/boj.12385
Cui Y, Nie L, Sun W, Xu Z, Wang Y, Yu J, Song J, Yao H (2019) Comparative and phylogenetic analyses of ginger (Zingiber officinale) in the family Zingiberaceae based on the complete chloroplast genome. Plants 8(8):283. https://doi.org/10.3390/plants8080283
Cutter AD, Charlesworth B (2006) Selection intensity on preferred codons correlates with overall codon usage bias in Caenorhabditis remanei. Curr Biol 16(20):2053–2057. https://doi.org/10.1016/j.cub.2006.08.067
Daniell H, Lin C-S, Yu M, Chang W-J (2016) Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biol 17:134. https://doi.org/10.1186/s13059-016-1004-2
Darriba D, Posada D, Kozlov AM, Stamatakis A, Morel B, Flouri T (2020) ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Mol Biol Evol 37(1):291–294. https://doi.org/10.1093/molbev/msz189
Darzentas N (2010) Circoletto: visualizing sequence similarity with Circos. Bioinformatics 26(20):2620–2621. https://doi.org/10.1093/bioinformatics/btq484
Dierckxsens N, Mardulyn P, Smits G (2016) NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res 45(4):e18–e18. https://doi.org/10.1093/nar/gkw955
Ding H, Zhu R, Dong J, Bi JL, Zeng J, Huang Q, Liu H, Xu W, Wu L, Kan X (2019) Next-generation genome sequencing of Sedum plumbizincicola sheds light on the structural evolution of plastid rRNA operon and phylogenetic implications within saxifragales. Plants 8(10):386. https://doi.org/10.3390/plants8100386
Dock-Bregeon AC, Westhof E, Giege R, Moras D (1989) Solution structure of a tRNA with a large variable region: yeast tRNASer. J Mol Biol 206(4):707–722. https://doi.org/10.1016/0022-2836(89)90578-0
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(4):e35071. https://doi.org/10.1371/journal.pone.0035071
Dong W, Xu C, Cheng T, Lin K, Zhou S (2013) Sequencing angiosperm plastid genomes made easy: a complete set of universal primers and a case study on the phylogeny of Saxifragales. Genome Biol Evol 5(5):989–997. https://doi.org/10.1093/gbe/evt063
Dong W, Xu C, Wu P, Cheng T, Yu J, Zhou S, Hong D (2018) Resolving the systematic positions of enigmatic taxa: manipulating the chloroplast genome data of Saxifragales. Mol Phylogenet Evol 126:321–330. https://doi.org/10.1016/j.ympev.2018.04.033
Duan H, Zhang Q, Wang C, Li F, Tian F, Lu Y, Hu Y, Yang H, Cui G (2021) Analysis of codon usage patterns of the chloroplast genome in Delphinium grandiflorum L. reveals a preference for AT-ending codons as a result of major selection constraints. PeerJ 9:e10787. https://doi.org/10.7717/peerj.10787
Duret L, Mouchiroud D (1999) Expression pattern and surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc Natl Acad Sci 96(8):4482–4487. https://doi.org/10.1073/pnas.96.8.4482
Ebersbach J, Muellner-Riehl A, Michalak I, Tkach N, Hoffmann M, Röser M, Sun H, Favre A (2017) In and out of the Qinghai-Tibet Plateau: divergence time estimation and historical biogeography of the large arctic-alpine genus Saxifraga L. J Biogeogr 44(4):900–910. https://doi.org/10.1111/jbi.12899
Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I (2004) VISTA: computational tools for comparative genomics. Nucleic Acids Res 32(suppl 2):W273–W279. https://doi.org/10.1093/nar/gkh458
Goodenbour JM, Pan T (2006) Diversity of tRNA genes in eukaryotes. Nucleic Acids Res 34(21):6137–6146. https://doi.org/10.1093/nar/gkl725
Guo X, Liu J, Hao G, Zhang L, Mao K, Wang X, Zhang D, Ma T, Hu Q, Al-Shehbaz IA (2017) Plastome phylogeny and early diversification of Brassicaceae. BMC Genomics 18:176. https://doi.org/10.1186/s12864-017-3555-3
Guo YY, Yang JX, Bai MZ, Zhang GQ, Liu ZJ (2021) The chloroplast genome evolution of Venus slipper (Paphiopedilum): IR expansion, SSC contraction, and highly rearranged SSC regions. BMC Plant Biol 21:248. https://doi.org/10.1186/s12870-021-03053-y
Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Henriquez CL, Abdullah AI, Carlsen MM, Zuluaga A, Croat TB, McKain MR (2020a) Evolutionary dynamics of chloroplast genomes in subfamily Aroideae (Araceae). Genomics 112(3):2349–2360. https://doi.org/10.1016/j.ygeno.2020.01.006
Henriquez CL, Abdullah AI, Carlsen MM, Zuluaga A, Croat TB, McKain MR (2020b) Molecular evolution of chloroplast genomes in Monsteroideae (Araceae). Planta 251:72. https://doi.org/10.1007/s00425-020-03365-7
Hernández-Castillo GR, Cevallos-Ferriz SR (1999) Reproductive and vegetative organs with affinities to Haloragaceae from the Upper Cretaceous Huepac Chert Locality of Sonora. Mexico. Am J Bot 86(12):1717–1734. https://doi.org/10.2307/2656670
Iriarte A, Lamolle G, Musto H (2021) Codon usage bias: an endless tale. J Mol Evol 89:589–593. https://doi.org/10.1007/s00239-021-10027-z
Jian S, Soltis PS, Gitzendanner MA, Moore MJ, Li R, Hendry TA, Qiu YL, Dhingra A, Bell CD, Soltis DE (2008) Resolving an ancient, rapid radiation in Saxifragales. Syst Biol 57(1):38–57. https://doi.org/10.1080/10635150801888871
Jin JJ, Yu WB, Yang JB, Song Y, dePamphilis CW, Yi TS, Li DZ (2020) GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biol 21:241. https://doi.org/10.1186/s13059-020-02154-5
Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36(suppl_2):W5–W9. https://doi.org/10.1093/nar/gkn201
Jorgensen TH, Frydenberg J (1999) Diversification in insular plants: inferring the phylogenetic relationship in Aeonium (Crassulaceae) using ITS sequences of nuclear ribosomal DNA. Nord J Bot 19(5):613–621. https://doi.org/10.1111/j.1756-1051.1999.tb01150.x
Jorgensen TH, Olesen JM (2001) Adaptive radiation of island plants: evidence from Aeonium (Crassulaceae) of the Canary Islands. Perspect Plant Ecol Evol Syst 4(1):29–42. https://doi.org/10.1078/1433-8319-00013
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780. https://doi.org/10.1093/molbev/mst010
Kim SC, McGowen MR, Lubinsky P, Barber JC, Mort ME, Santos-Guerra A (2008) Timing and tempo of early and successive adaptive radiations in Macaronesia. PLoS ONE 3(5):e2139. https://doi.org/10.1371/journal.pone.0002139
Kirchner S, Ignatova Z (2015) Emerging roles of tRNA in adaptive translation, signalling dynamics and disease. Nat Rev Genet 16:98–112. https://doi.org/10.1038/nrg3861
Leffler EM, Bullaughey K, Matute DR, Meyer WK, Segurel L, Venkat A, Andolfatto P, Przeworski M (2012) Revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biol 10(9):e1001388. https://doi.org/10.1371/journal.pbio.1001388
Lems K (1960) Botanical notes on the Canary Islands II. The evolution of plant forms in the islands: Aeonium. Ecology 41(1):1–17. https://doi.org/10.2307/1931934
Liu H-Y (1986) Systematics of Aeonium (Crassulaceae). Dissertation, National Museum of Natural Science
Liu H, Lu Y, Lan B, Xu J (2020) Codon usage by chloroplast gene is bias in Hemiptelea davidii. J Genet 99:8. https://doi.org/10.1007/s12041-019-1167-1
Lu Y (2018) Assembly and transfer of iron–sulfur clusters in the plastid. Front Plant Sci 9:336. https://doi.org/10.3389/fpls.2018.00336
Magallon S, Crane PR, Herendeen PS (1999) Phylogenetic pattern, diversity, and diversification of eudicots. Ann Mo Bot Gard 86:297–372. https://doi.org/10.2307/2666180
Maréchal-Drouard L, Guillemaut P, Pfitzingzer H, Weil J (1991) Chloroplast tRNAs and tRNA genes: structure and function. In: Mache R, Stutz E, Subramanian AR (eds) The Translational apparatus of photosynthetic organelles, 1st edn. Springer, Berlin, pp 45–57
Mehmood F, Abdullah SI, Ahmed I, Waheed MT, Mirza B (2020) Characterization of Withania somnifera chloroplast genome and its comparison with other selected species of Solanaceae. Genomics 112(2):1522–1530. https://doi.org/10.1016/j.ygeno.2019.08.024
Mes T, Hart H (1996) The evolution of growth-forms in the Macaronesian genus Aeonium (Crassulaceae) inferred from chloroplast DNA RFLPs and morphology. Mol Ecol 5(3):351–363. https://doi.org/10.1046/j.1365-294X.1996.00090.x
Mes TH, Wijers GJ, Hart HT (1997) Phylogenetic relationships in Monanthes (Crassulaceae) based on morphological, chloroplast and nuclear DNA variation. J Evol Biol 10(2):193–216. https://doi.org/10.1046/j.1420-9101.1997.10020193.x
Messerschmid TF, Klein JT, Kadereit G, Kadereit JW (2020) Linnaeus’s folly–phylogeny, evolution and classification of Sedum (Crassulaceae) and Crassulaceae subfamily Sempervivoideae. Taxon 69(5):892–926. https://doi.org/10.1002/tax.12316
Miller JB, Hippen AA, Belyeu JR, Whiting MF, Ridge PG (2017) Missing something? Codon aversion as a new character system in phylogenetics. Cladistics 33(5):545–556. https://doi.org/10.1111/cla.12183
Miller JB, McKinnon LM, Whiting MF, Ridge PG (2019) CAM: an alignment-free method to recover phylogenies using codon aversion motifs. PeerJ 7:e6984. https://doi.org/10.7717/peerj.6984
Miller JB, McKinnon LM, Whiting MF, Ridge PG (2020) Codon use and aversion is largely phylogenetically conserved across the tree of life. Mol Phylogenet Evol 144:106697. https://doi.org/10.1016/j.ympev.2019.106697
Mohanta TK, Syed AS, Ameen F, Bae H (2017) Novel genomic and evolutionary perspective of cyanobacterial tRNAs. Front Genet 8:200. https://doi.org/10.3389/fgene.2017.00200
Moore MJ, Soltis PS, Bell CD, Burleigh JG, Soltis DE (2010) Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots. Proc Natl Acad Sci 107(10):4623–4628. https://doi.org/10.1073/pnas.090780110
Mort ME, Soltis DE, Soltis PS, Francisco-Ortega J, Santos-Guerra A (2001) Phylogenetic relationships and evolution of Crassulaceae inferred from matK sequence data. Am J Bot 88(1):76–91. https://doi.org/10.2307/2657129
Mort ME, Soltis DE, Soltis PS, Francisco-Ortega J, Santos-Guerra A (2002) Phylogenetics and evolution of the Macaronesian clade of Crassulaceae inferred from nuclear and chloroplast sequence data. Syst Bot 27(2):271–288. https://doi.org/10.1043/0363-6445-27.2.271
Mort ME, Solits DE, Soltis PS, Santos-Guerra A, Francisco-Ortega J (2007) Physiological evolution and association between physiology and growth form in Aeonium (Crassulaceae). Taxon 56(2):453–464. https://doi.org/10.1002/tax.562016
Morton BR (1998) Selection on the codon bias of chloroplast and cyanelle genes in different plant and algal lineages. J Mol Evol 46:449–459. https://doi.org/10.1007/PL00006325
Morton BR (2021) Context-dependent mutation dynamics, not selection, explains the codon usage bias of most angiosperm chloroplast genes. J Mol Evol 90:17–29. https://doi.org/10.1007/s00239-021-10038-w
Mower JP, Guo W, Partha R, Fan W, Levsen N, Wolff K, Nugent JM, Pabon-Mora N, Gonzalez F (2021) Plastomes from tribe Plantagineae (Plantaginaceae) reveal infrageneric structural synapormorphies and localized hypermutation for Plantago and functional loss of ndh genes from Littorella. Mol Phylogenet Evol 162:107217. https://doi.org/10.1016/j.ympev.2021.107217
Murray M, Thompson W (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8(19):4321–4326. https://doi.org/10.1093/nar/8.19.4321
Parks M, Cronn R, Liston A (2009) Increasing phylogenetic resolution at low taxonomic levels using massively parallel sequencing of chloroplast genomes. BMC Biol 7:84. https://doi.org/10.1186/1741-7007-7-84
Peden JF (2000) Analysis of codon usage. PhD thesis, University of Nottingham
Pigg KB, Ickert-Bond SM, Wen J (2004) Anatomically preserved Liquidambar (Altingiaceae) from the middle Miocene of Yakima Canyon, Washington state, USA, and its biogeographic implications. Am J Bot 91(3):499–509. https://doi.org/10.3732/ajb.91.3.499
Praeger LR (2011) An account of the Sempervivum group. Royal Horticultural Society, London
Rambaut A (2014) FigTree v1.4.2, a graphical viewer of phylogenetic trees. http://tree.bio.ed.ac.uk/software/figtree/. Accessed Jan 2019
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67(5):901–904. https://doi.org/10.1093/sysbio/syy032
Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542. https://doi.org/10.1093/sysbio/sys029
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34(12):3299–3302. https://doi.org/10.1093/molbev/msx248
Sabater B (2018) Evolution and function of the chloroplast. Current investigations and perspectives. Int J Mol Sci 19(10):3095. https://doi.org/10.3390/ijms19103095
Shahzadi I, Abdullah MF, Ali Z, Ahmed I, Mirza B (2020) Chloroplast genome sequences of Artemisia maritima and Artemisia absinthium: comparative analyses, mutational hotspots in genus Artemisia and phylogeny in family Asteraceae. Genomics 112(2):1454–1463. https://doi.org/10.1016/j.ygeno.2019.08.016
Sharp PM, Li W-H (1986) An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol 24:28–38. https://doi.org/10.1007/BF02099948
Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Am J Bot 94(3):275–288. https://doi.org/10.3732/ajb.94.3.275
Shen X, Wu M, Liao B, Liu Z, Bai R, Xiao S, Li X, Zhang B, Xu J, Chen S (2017) Complete chloroplast genome sequence and phylogenetic analysis of the medicinal plant Artemisia annua. Molecules 22(8):1330. https://doi.org/10.3390/molecules22081330
Sheng J, She X, Liu X, Wang J, Hu Z (2021) Comparative analysis of codon usage patterns in chloroplast genomes of five Miscanthus species and related species. PeerJ 9:e12173. https://doi.org/10.7717/peerj.12173
Soltis DE, Mort ME, Latvis M, Mavrodiev EV, O’Meara BC, Soltis PS, Burleigh JG, Rubio de Casas R (2013) Phylogenetic relationships and character evolution analysis of Saxifragales using a supermatrix approach. Am J Bot 100(5):916–929. https://doi.org/10.3732/ajb.1300044
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Suda J, Kyncl T, Jarolímová V (2005) Genome size variation in Macaronesian angiosperms: forty percent of the Canarian endemic flora completed. Plant Syst Evol 252(3):215–238. https://doi.org/10.1007/s00606-004-0280-6
Sueoka N (1999) Two aspects of DNA base composition: G+C content and translation-coupled deviation from intra-strand rule of A=T and G=C. J Mol Evol 49:49–62. https://doi.org/10.1007/PL00006534
Suzuki H, Morton BR (2016) Codon adaptation of plastid genes. PLoS ONE 11(5):e0154306. https://doi.org/10.1371/journal.pone.0154306
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. https://doi.org/10.1007/s00427-020-00670-9
Thiede J, Eggli U (2007) Crassulaceae. In: Kubitzki K (ed) Flowering plants. Eudicots, 1st edn. Springer, Berlin, pp 83–118
Thomson RC, Wang IJ, Johnson JR (2010) Genome-enabled development of DNA markers for ecology, evolution and conservation. Mol Ecol 19(11):2184–2195. https://doi.org/10.1111/j.1365-294X.2010.04650.x
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(W1):W6–W11. https://doi.org/10.1093/nar/gkx391
Ueda M, Fujimoto M, Arimura S-i, Murata J, Tsutsumi N, Kadowaki K-i (2007) Loss of the rpl32 gene from the chloroplast genome and subsequent acquisition of a preexisting transit peptide within the nuclear gene in Populus. Gene 402(1–2):51–56. https://doi.org/10.1016/j.gene.2007.07.019
Van Ham R, Hart H (1998) Phylogenetic relationships in the Crassulaceae inferred from chloroplast DNA restriction-site variation. Am J Bot 85(1):123–134. https://doi.org/10.2307/2446561
Wang N, Dong WL, Zhang XJ, Zhou T, Huang XJ, Li BG, Liu JN, Ma XF, Li ZH (2021) Evolutionary characteristics and phylogeny of cotton chloroplast tRNAs. Planta 254:116. https://doi.org/10.1007/s00425-021-03775-1
Wickham H (2011) ggplot2. Wiley Interdiscipl Rev Comput Stat 3(2):180–185. https://doi.org/10.1002/wics.147
Wright F (1990) The ‘effective number of codons’ used in a gene. Gene 87(1):23–29. https://doi.org/10.1016/0378-1119(90)90491-9
Wu Y, Liu F, Yang D-G, Li W, Zhou X-J, Pei X-Y, Liu Y-G, He K-L, Zhang W-S, Ren Z-Y (2018) Comparative chloroplast genomics of Gossypium species: insights into repeat sequence variations and phylogeny. Front Plant Sci 9:376. https://doi.org/10.3389/fpls.2018.00376
Xu C, Cai X, Chen Q, Zhou H, Cai Y, Ben A (2011) Factors affecting synonymous codon usage bias in chloroplast genome of oncidium gower ramsey. Evol Bioinform 7:271–278. https://doi.org/10.4137/EBO.S8092
Yang Z, Wang G, Ma Q, Ma W, Liang L, Zhao T (2019) The complete chloroplast genomes of three Betulaceae species: implications for molecular phylogeny and historical biogeography. PeerJ 7:e6320. https://doi.org/10.7717/peerj.6320
Yang J, Ding H, Kan X (2021) Codon usage patterns and evolution of HSP60 in birds. Int J Biol Macromol 183:1002–1012. https://doi.org/10.1016/j.ijbiomac.2021.05.017
Yengkhom S, Uddin A, Chakraborty S (2019) Deciphering codon usage patterns and evolutionary forces in chloroplast genes of Camellia sinensis var. assamica and Camellia sinensis var. sinensis in comparison to Camellia pubicosta. J Integr Agric 18(12):2771–2785. https://doi.org/10.1016/s2095-3119(19)62716-4
Zhang Y, Nie X, Jia X, Zhao C, Biradar SS, Wang L, Du X, Weining S (2012) Analysis of codon usage patterns of the chloroplast genomes in the Poaceae family. Aust J Bot 60(5):461–470. https://doi.org/10.1071/BT12073
Zhang H, Li C, Miao H, Xiong S (2013) Insights from the complete chloroplast genome into the evolution of Sesamum indicum L. PLoS ONE 8(11):e80508. https://doi.org/10.1371/journal.pone.0080508
Zhang R, Zhang L, Wang W, Zhang Z, Du H, Qu Z, Li X-Q, Xiang H (2018) Differences in codon usage bias between photosynthesis-related genes and genetic system-related genes of chloroplast genomes in cultivated and wild solanum species. Int J Mol Sci 19(10):3142. https://doi.org/10.3390/ijms19103142
Zhang TT, Hou YK, Yang T, Zhang SY, Yue M, Liu J, Li Z (2020) Evolutionary analysis of chloroplast tRNA of Gymnosperm revealed the novel structural variation and evolutionary aspect. PeerJ 8:e10312. https://doi.org/10.7717/peerj.10312
Zhang TT, Yang Y, Song XY, Gao XY, Zhang XL, Zhao JJ, Zhou KH, Zhao CB, Li W, Yang DG, Ma XF, Li ZH (2021) Novel structural variation and evolutionary characteristics of chloroplast tRNA in Gossypium plants. Genes 12(6):822. https://doi.org/10.3390/genes12060822
Zhao Y-H, Zhou T, Wang J-X, Li Y, Fang M-F, Liu J-N, Li Z-H (2021) Evolution and structural variations in chloroplast tRNAs in gymnosperms. BMC Genomics 22:750. https://doi.org/10.1186/s12864-021-08058-3
Zheng S, Poczai P, Hyvönen J, Tang J, Amiryousefi A (2020) Chloroplot: an online program for the versatile plotting of organelle genomes. Front Genet 11:576124. https://doi.org/10.3389/fgene.2020.576124
Zhong QY, Fu XG, Zhang TT, Zhou T, Yue M, Liu JN, Li ZH (2021) Phylogeny and evolution of chloroplast tRNAs in Adoxaceae. Ecol Evol 11(3):1294–1309. https://doi.org/10.1002/ece3.7133
Zhou J-h, Ding Y-z, He Y, Chu Y-f, Zhao P, Ma L-y, Wang X-j, Li X-r, Liu Y-s (2014) The effect of multiple evolutionary selections on synonymous codon usage of genes in the Mycoplasma bovis genome. PLoS ONE 9(10):e108949. https://doi.org/10.1371/journal.pone.0108949
Zhou Z, Crepet WL, Nixon KC (2001) The earliest fossil evidence of the Hamamelidaceae: Late Cretaceous (Turonian) inflorescences and fruits of Altingioideae. Am J Bot 88(5):753–766. https://doi.org/10.2307/2657028
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The authors would like to thank the anonymous reviewers for their critical reviews and helpful suggestions.
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This study was supported by the Opening Foundation of National Engineering Laboratory of Soil Pollution Control and Remediation Technologies, and Key Laboratory of Heavy Metal Pollution Prevention & Control, Ministry of Agriculture and Rural Affairs (Grant no. NEL&MARA-003), the Basic Research Program (Natural Science Foundation) of Jiangsu Province (Grant no. BK20211078), and the Scientific Research Project Foundation of Postgraduate of the Anhui Higher Education Institutions of China (Grant no. YJS20210136).
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Han, S., Bi, D., Yi, R. et al. Plastome evolution of Aeonium and Monanthes (Crassulaceae): insights into the variation of plastomic tRNAs, and the patterns of codon usage and aversion. Planta 256, 35 (2022). https://doi.org/10.1007/s00425-022-03950-y
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DOI: https://doi.org/10.1007/s00425-022-03950-y