Insights into chloroplast genome evolution in Rutaceae through population genomics
Chloroplast genomes, pivotal for understanding plant evolution, remain unexplored in Rutaceae, a family with key perennial crops like citrus. Leveraging next-generation sequencing data from 509 Rutaceae accessions across 15 species, we conducted a de novo assembly of 343 chloroplast genomes, unveiling a chloroplast variation map highlighting the heterogeneous evolution rates across genome regions. Notably, differences in chloroplast genome size primarily originate from large single-copy and small single-copy regions. Structural variants predominantly occurred in the single-copy region, with two insertions located at the single-copy and inverted repeat region boundary. Phylogenetic analysis, principal component analysis, and population genetic statistics confirmed the cohesive clustering of different Citrus species, reflecting evolutionary dynamics in Citrus diversification. Furthermore, a close chloroplast genetic affinity was revealed among Atalantia (previously regarded as primitive citrus), Clausena, and Murraya. Zanthoxylum formed a distinct group with heightened genetic diversity. Through expanding our analysis to include 34 published chloroplast genomes, we explored chloroplast gene selection, revealing divergent evolutionary trends in photosynthetic pathways. While Photosystem I and Photosystem II exhibited robust negative selection, indicating stability, the Nicotinamide adenine dinucleotide (NADH) dehydrogenase pathway demonstrated rapid evolution, which was indicative of environmental adaptation. Finally, we discussed the effects of gene length and GC content on chloroplast gene evolution. In conclusion, our study reveals the genetic characterization of chloroplast genomes during Rutaceae diversification, providing insights into the evolutionary history of this family.
Chloroplast genome / Rutaceae / Negative selection / Diversification
[1] | Aphalo P. R package ggpmisc is an extension to ggplot2 and the Grammar of Graphics. Im: Ggpmisc. GitHub. 2021. https://github.com/aphalo/ggpmisc. Accessed 10 Oct 2023. |
[2] | Bayer RJ, Mabberley DJ, Morton C, Miller CH, Sharma IK, Pfeil BE, et al. A molecular phylogeny of the orange subfamily (Rutaceae: Aurantioideae) using nine cpDNA sequences. Am J Bot. 2009;96:668–75. https://doi.org/10.3732/ajb.0800341. |
[3] | Birky CW. Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci. 1995;92:11331–8. https://doi.org/10.1073/pnas.92.25.11331. |
[4] | Carbonell-Caballero J, Alonso R, Ibanez V, Terol J, Talon M, Dopazo J. A phylogenetic analysis of 34 chloroplast genomes elucidates the relationships between wild and domestic species within the genus Citrus. Mol Biol Evol. 2015;32:2015–35. https://doi.org/10.1093/molbev/msv082. |
[5] | Chaudhari NM, Gupta VK, Dutta C. BPGA- an ultra-fast pan-genome analysis pipeline. Sci Rep. 2016;6:24373. https://doi.org/10.1038/srep24373. |
[6] | Chung SM, Staub JE. The development and evaluation of consensus chloroplast primer pairs that possess highly variable sequence regions in a diverse array of plant taxa. Theor Appl Genet. 2003;107:757–67. https://doi.org/10.1007/s00122-003-1311-3. |
[7] | Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. 2012;6:80–92. https://doi.org/10.4161/fly.19695 |
[8] | Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, et al. The variant call format and VCFtools. Bioinformatics. 2011;27:2156–8. https://doi.org/10.1093/bioinformatics/btr330. |
[9] | Daniell H, Lin CS, Yu M, Chang WJ. Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biol. 2016;17:134. https://doi.org/10.1186/s13059-016-1004-2. |
[10] | Engler A. Rutaceae. In: Engler A, Prantl K, editors. Dia natürlichen pflanzenfamilien. 2nd ed. Leipzig, Germany; 1931:187–359. |
[11] | Feng S, Liu Z, Cheng J, Li Z, Tian L, Liu M, et al. Zanthoxylum-specific whole genome duplication and recent activity of transposable elements in the highly repetitive paleotetraploid Z. bungeanum genome. Hortic Res. 2021;8:205. https://doi.org/10.1038/s41438-021-00665-1 |
[12] | Gao LZ, Liu YL, Zhang D, Li W, Gao J, Liu Y, et al. Evolution of Oryza chloroplast genomes promoted adaptation to diverse ecological habitats. Commun Biol. 2019;2:278. https://doi.org/10.1038/s42003-019-0531-2. |
[13] | Green BR. Chloroplast genomes of photosynthetic eukaryotes. Plant J. 2011;66:34–44. https://doi.org/10.1111/j.1365-313X.2011.04541.x. |
[14] | Greiner S, Lehwark P, Bock R. Organellar Genome DRAW (OGDRAW) version 1.3. 1: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Res. 2019;47:W59–W64. https://doi.org/10.1093/nar/gkz238 |
[15] | Grivet D, Heinze B, Vendramin G, Petit R. Genome walking with consensus primers: application to the large single copy region of chloroplast DNA. Mol Ecol Notes. 2001;1:345–9. https://doi.org/10.1046/j.1471-8278.2001.00107.x. |
[16] | Groppo M, Pirani JR, Salatino ML, Blanco SR, Kallunki JA. Phylogeny of Rutaceae based on two noncoding regions from cpDNA. Am J Bot. 2008;95:985–1005. https://doi.org/10.3732/ajb.2007313. |
[17] | Hagemann R. The sexual inheritance of plant organelles. Molecular biology and biotechnology of plant organelles: Springer; 2004:93–113. https://doi.org/10.1007/978-1-4020-3166-3_4 |
[18] | Hall T, Biosciences I, Carlsbad C. BioEdit: an important software for molecular biology. GERF Bull Biosci. 2011;2:60–1. https://doi.org/10.55838/1980-3540.ge.2018.287 |
[19] | Heinze B. A database of PCR primers for the chloroplast genomes of higher plants. Plant Methods. 2007;3:4. https://doi.org/10.1186/1746-4811-3-4. |
[20] | Hipkins VD, Krutovskii KV, Straws SH. Organelle genome in conifers: structure, evolution. For Genet. 1994;1:179–89. |
[21] | Jin JJ, Yu WB, Yang JB, Song Y, Depamphilis CW, Yi TS, et al. GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biol. 2020;21:241. https://doi.org/10.1101/256479. |
[22] | Kassambara A. n.d. Ggpubr: 'ggplot2' Based Publication Ready Plots. ggpubr. https://rpkgs.datanovia.com/ggpubr/. Accessed 15 Oct 2023 |
[23] | Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80. https://doi.org/10.1093/molbev/mst010. |
[24] | Kelchner SA. The evolution of non-coding chloroplast DNA and its application in plant systematics. Ann Mo Bot Gard. 2000;87:482. https://doi.org/10.2307/2666142. |
[25] | Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, et al. Circos: an information aesthetic for comparative genomics. Genome Res. 2009;19:1639–45. https://doi.org/10.1101/gr.092759.109. |
[26] | Kubitzki K. Flowering Plants. Eudicots: Sapindales, Cucurbitales, Myrtaceae. 1st ed. Berlin: Springer; 2011 |
[27] | Leigh JW, Bryant D. POPART: full-feature software for haplotype network construction. Methods Ecol Evol. 2015;6:1110–6. https://doi.org/10.1111/2041-210x.12410. |
[28] | Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25:1754–60. https://doi.org/10.1093/bioinformatics/btp324. |
[29] | Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078–9. https://doi.org/10.1093/bioinformatics/btp352. |
[30] | Li HT, Luo Y, Gan L, Ma PF, Gao LM, Yang JB, et al. Plastid phylogenomic insights into relationships of all flowering plant families. BMC Biol. 2021;19:232. https://doi.org/10.1186/s12915-021-01166-2. |
[31] | Li Y, Li X, Sylvester S, Duan Y. Plastid genomes reveal evolutionary shifts in elevational range and flowering time of Osmanthus (Oleaceae). Ecol Evol. 2022;12: e8777. https://doi.org/10.1002/ece3.8777. |
[32] | Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–2. https://doi.org/10.1093/bioinformatics/btp187. |
[33] | Liu H, Ye H, Zhang N, Ma J, Wang J, Hu G, et al. Comparative analyses of chloroplast genomes provide comprehensive insights into the adaptive evolution of Paphiopedilum (Orchidaceae). Horticulturae. 2022;8:391. https://doi.org/10.3390/horticulturae8050391. |
[34] | Magdy M, Ou L, Yu H, Chen R, Zhou Y, Heba Hassan, et al. Pan-plastome approach empowers the assessment of genetic variation in cultivated Capsicum species. Hort Res. 2019;6:108. https://doi.org/10.1038/s41438-019-0191-x. |
[35] | Minh B, Schmidt H, Chernomor O, Schrempf D, Woodhams M, von Haeseler A, et al. IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37:1530–4. https://doi.org/10.1093/molbev/msaa015. |
[36] | Mower JP, Guo W, Partha R, Fan W, Levsen N, Wolff K, et al. 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. 2021;162: 107217. https://doi.org/10.1016/j.ympev.2021.107217. |
[37] | Nagano Y, Mimura T, Kotoda N, Matsumoto R, Nagano AJ, Honjo MN, et al. Phylogenetic relationships of Aurantioideae (Rutaceae) based on RAD-Seq. Tree Genet Genomes. 2018;14:6. https://doi.org/10.1007/s11295-017-1223-z. |
[38] | Narasimhan V, Danecek P, Scally A, Xue Y, Tyler-Smith C, Durbin R. BCFtools/RoH: a hidden Markov model approach for detecting autozygosity from next-generation sequencing data. Bioinformatics. 2016;32:1749–51. https://doi.org/10.1093/bioinformatics/btw044. |
[39] | Ogoma C, Liu J, Stull G, Wambulwa M, Oyebanji O, Milne R, et al. Deep insights into the plastome evolution and phylogenetic relationships of the Tribe Urticeae (Family Urticaceae). Front Plant Sci. 2022;13: 870949. https://doi.org/10.3389/fpls.2022.870949. |
[40] | Ortiz E. vcf2phylip v2. 0: convert a VCF matrix into several matrix formats for phylogenetic analysis. 2019. https://doi.org/105281/zenodo2540861. Accessed 13 Nov 2023 |
[41] | Palmer JD. Chloroplast DNA evolution and biosystematic uses of chloroplast DNA variation. Am Nat. 1987;130:6–29. https://doi.org/10.1086/284689. |
[42] | Patil, I. Visualizations with statistical details: The 'ggstatsplot' approach. J Open Source Softw. 2021;6:3167. https://doi.org/10.21105/joss.03167 |
[43] | Poplin R, Chang PC, Alexander D, Schwartz S, Colthurst T, Ku A, et al. A universal SNP and small-indel variant caller using deep neural networks. Nat Biotechnol. 2018;36:983–7. https://doi.org/10.1038/nbt.4235. |
[44] | Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007;81:559–75. https://doi.org/10.1086/519795. |
[45] | Qu XJ, Moore MJ, Li DZ, Yi TS. PGA: a software package for rapid, accurate, and flexible batch annotation of plastomes. Plant Methods. 2019;15:50. https://doi.org/10.1186/s13007-019-0435-7. |
[46] | Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841–2. https://doi.org/10.1093/bioinformatics/btq033. |
[47] | Rao MJ, Zuo H, Xu Q. Genomic insights into citrus domestication and its important agronomic traits. Plant Commun. 2021;2: 100138. https://doi.org/10.1016/j.xplc.2020.100138. |
[48] | Raubeson LA, Jansen RK. Chloroplast genomes of plants. In: Henry RJ, editor. Plant diversity and evolution: genotypic and phenotypic variation in higher plants.Cambridge: CAB International; 2005:45–68. |
[49] | Rausch T, Zichner T, Schlattl A, Stütz AM, Benes V, Korbel JO. DELLY: structural variant discovery by integrated paired-end and split-read analysis. Bioinformatics. 2012;28:i333–9. https://doi.org/10.1093/bioinformatics/bts378. |
[50] | Saarela JM, Burke SV, Wysocki WP, Barrett MD, Clark LG, Craine JM, et al. A 250 plastome phylogeny of the grass family (Poaceae): topological support under different data partitions. PeerJ. 2018;6: e4299. https://doi.org/10.7717/peerj.4299. |
[51] | Shen W, Le S, Li Y, Hu F. SeqKit: a cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PLoS ONE. 2016;11: e0163962. https://doi.org/10.1371/journal.pone.0163962. |
[52] | Wang X, Xu Y, Zhang S, Cao L, Huang Y, Cheng J, et al. Genomic analyses of primitive, wild and cultivated citrus provide insights into asexual reproduction. Nat Genet. 2017;49:765–72. https://doi.org/10.1038/ng.3839. |
[53] | Wang L, He F, Yue H, He J, Yang S, Zeng J, et al. Genome of Wild Mandarin and Domestication History of Mandarin. Mol Plant. 2018;11:1024–37. https://doi.org/10.1016/j.molp.2018.06.001. |
[54] | Wang N, Li C, Kuang L, Wu X, Xie K, Zhu A, et al. Pan-mitogenomics reveals the genetic basis of cytonuclear conflicts in citrus hybridization, domestication, and diversification. Proc Natl Acad Sci. 2022b;119: e2206076119. https://doi.org/10.1073/pnas.2206076119. |
[55] | Wang J, Liao X, Gu C, Xiang K, Wang J, et al. The Asian lotus (Nelumbo nucifera) pan-plastome: diversity and divergence in a living fossil grown for seed, rhizome, and aesthetics. Ornamental Plant Research. 2022. https://doi.org/10.48130/OPR-2022-0002 |
[56] | Wei L, Xiang XG, Wang YZ, Li ZY. Phylogenetic relationships and evolution of the Androecia in Ruteae (Rutaceae). PLoS ONE. 2015;10: e0137190. https://doi.org/10.1371/journal.pone.0137190. |
[57] | Wickham H. ggplot2. Wiley Interdiscip Rev Comput Stat. 2011;3:180–5. https://doi.org/10.1002/wics.147. |
[58] | Wu GA, Terol J, Ibanez V, Lopez-Garcia A, Perez-Roman E, Borreda C, et al. Genomics of the origin and evolution of Citrus. Nature. 2018;554:311–6. https://doi.org/10.1186/s12864-015-1926-1. |
[59] | Yan LJ, Zhu ZG, Wang P, Fu CN, Guan XJ, Kear P, et al. Comparative analysis of 343 plastid genomes of Solanum section Petota: Insights into potato diversity, phylogeny, and species discrimination. J Syst Evol. 2022;61:599–612. https://doi.org/10.1111/jse.12898. |
[60] | Yang Z. PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007;24:1586–91. https://doi.org/10.1093/molbev/msm088. |
[61] | Yi X, Gao L, Wang B, Su YJ, Wang T. The complete chloroplast genome sequence of Cephalotaxus oliveri (Cephalotaxaceae): Evolutionary comparison of Cephalotaxus chloroplast DNAs and insights into the loss of inverted repeat copies in gymnosperms. Genome Biol Evol. 2013;5:688–98. https://doi.org/10.1093/gbe/evt042. |
[62] | Yun T, Li H, Chang PC, Lin MF, Carroll A, McLean CY. Accurate, scalable cohort variant calls using DeepVariant and GLnexus. Bioinformatics. 2020;36:5582–9. https://doi.org/10.1093/bioinformatics/btaa1081. |
[63] | Zhang SD, Jin JJ, Chen SY, Chase MW, Soltis DE, Li HT, et al. Diversification of Rosaceae since the late cretaceous based on plastid phylogenomics. New Phytol. 2017;214:1355–67. https://doi.org/10.1111/nph.14461. |
[64] | Zhou J, He W, Wang J, Liao X, Xiang K, et al. The pan-plastome of tartary buckwheat (fagopyrum tataricum): Key insights into genetic diversity and the history of lineage divergence. BMC Plant Biol. 2023;23:212. https://doi.org/10.1186/s12870-023-04218-7. |
[65] | Zhu A, Guo W, Gupta S, Fan W, Mower J. Evolutionary dynamics of the plastid inverted repeat: The effects of expansion, contraction, and loss on substitution rates. New Phytol. 2015;209:1747–56. https://doi.org/10.1111/nph.13743. |
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