The study of citrus plant evolution based on repetitive genomic elements, chloroplast genome, and 35S rDNA
UDC 582.751.92+575.113+575.89
Keywords:
Citrus, LTR, phylogeny, repeatome, repeats
Abstract
In our study, we analyzed the repeatomes of 12 Citrus plants, including 4 ancestral species and 8 the most widespread cultivated species. We detected an atypically high content of “Athila” and “Sire” LTR retrotransposons for angiosperms. For these plants, phylogenetic trees were constructed based on the nuclear repeatome, plastome, and 35S rDNA cistron, using sequencing data from open databases and, for the first time, sequencing data from our collection. The analysis demonstrated that the plastome carries a strong phylogenetic signal, which is most consistent with the updated classification of the Citrus genus, showing a distinct pattern compared to the other two phylogenetic trees.
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References
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Bhattacharya S., Dutta S. 1956. Classification of citrus fruits of Assam. New Dehli: ICAR. 110 pp.
Burke W. D., Malik H. S. Rich S. M., Eickbush T. H. 2002. Ancient lineages of non-LTR retrotransposons in the primitive eukaryote, Giardia lamblia. MBE 19: 619–630. https://doi.org/10.1093/oxfordjournals.molbev.a004121
Chen G. F., Wang G. C., Zhang C. Y., Zhang B. Y., Wang X. K., Zhou B. C. 2008. Development of rRNA and rDNA-targeted probes for fluorescence in situ hybridization to detect Heterosigma akashiwo (Raphidophyceae). J. Exp. Mar. Biol. Ecol. 355: 66–75.
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
Dodsworth S., Chase M. W., Kelly L. J., Leitch I. J., Macas J., Novak, P., Piednoel M., Weiss-Schneeweiss H., Leitch A. R. 2015. Genomic repeat abundances contain phylogenetic signal. System. Biolog. 64: 112–126. https://doi.org/10.1093/sysbio/syu080
Domingues D. S., Cruz G. M., Metcalfe C. J., Nogueira F. T., Vicentini R., de S Alves C., Van Sluys M.-A. 2012. Analysis of plant LTR-retrotransposons at the fine-scale family level reveals individual molecular patterns. BMC Genom. 13: 1–14.
Drost H. G. 2018. Philentropy: information theory and distance quantification with R. JOSS 3: 765. https://doi.org/10.21105/joss.00765
Du D., Du X., Mattia M. R., Wang Y., Yu Q., Huang M., Yu Y., Grosser J. W., Gmitter F. G. 2018. LTR retrotransposons from the Citrus × clementina genome: characterization and application. Tree Genet. Genomes 14: 1–14.
FAO [2025]. FAOSTAT: Agricultural Production Data. URL: https://www.fao.org/.
Garcia S., Panero J. L., Siroky J., Kovarik A. 2010. Repeated reunions and splits feature the highly dynamic evolution of 5S and 35S ribosomal RNA genes (rDNA) in the Asteraceae family. BMC Plant Biol. 10: 1–18.
Garcia S., Wendel J. F., Borowska-Zuchowska N., Aïnouche M., Kuderova, A., Kovarik A. 2020. The utility of graph clustering of 5S ribosomal DNA homoeologs in plant allopolyploids, homoploid hybrids, and cryptic introgressants. Front. Plant Sci. 11: 41. https://doi.org/10.3389/fpls.2020.00041
Guerra M. dos S. 1984. Cytogenetics of rutaceae. II. Nuclear DNA content. Caryologia 37: 219–226.
He J., Lin S., Yu, Z., Song A., Guan Z., Fang W., Chen S., Zhang F., Jiang J., Chen F. 2021. Identification of 5S and 45S rDNA sites in Chrysanthemum species by using oligonucleotide fluorescence in situ hybridization (Oligo-FISH). Mol. Biol. Rep. 48: 21–31.
Herklotz V., Kovařík A., Wissemann V., Lunerová J., Vozárová R., Buschmann S., Olbricht K., Groth M., Ritz C. M. 2021. Power and weakness of repetition-evaluating the phylogenetic signal from repeatomes in the family Rosaceae with two case studies from genera prone to polyploidy and hybridization (Rosa and Fragaria). Front. Plant Sci. 12: 738119. https://doi.org/10.3389/fpls.2021.738119
Hodgson R. W. 1961. Taxonomy and nomenclature in citrus. In: IOCV Conference Proceedings (Gainesville, 1961). Vol 2(2). Riverside: University of California. Pp. 1–7.
Isobe S., Fujii, H., Shirasawa K., Kawahara Y., Endo T., Shimada T. 2023. Haploid-resolved and chromosome-scale genome assembly in Citrus unshiu and its parental species, C. nobilis and C. kinokuni. bioRxiv 2023.06.02.543356. https://doi.org/10.1101/2023.06.02.543356
Kashkush K., Feldman M., Levy A. A. 2003. Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat. Genet. 33: 102–106.
Katoh K., Standley D. M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. MBE 30: 772–780.
Kress W. J., Soltis D. E., Kersey P. J., Wegrzyn J. L., Leebens-Mack J. H., Gostel M. R., Liu X., Soltis P. S. 2022. Green plant genomes: What we know in an era of rapidly expanding opportunities. Proc. Natl. Acad. Sci. U.S.A. 119, 4: e2115640118. https://doi.org/10.1073/pnas.2115640118
Lee Y.-I., Yap J. W., Izan S., Leitch I. J., Fay M. F., Lee Y.-C., Hidalgo O., Dodsworth S., Smulders M. J. M., Gravendeel B., Leitch A. R. 2018. Satellite DNA in Paphiopedilum subgenus Parvisepalum as revealed by high-throughput sequencing and fluorescent in situ hybridization. BMC Genom. 19: 578. https://doi.org/10.1186/s12864-018-4956-7
Letunic I., Bork P. 2024. Interactive Tree of Life (iTOL) v6: recent updates to the phylogenetic tree display and annotation tool. Nucleic Acids Res. 52, 1: W78–W82. https://doi.org/10.1093/nar/gkae268
Lozano R., Gazave E., Dos Santos J. P. R., Stetter M. G., Valluru R., Bandillo N., et al. 2021. Comparative evolutionary genetics of deleterious load in sorghum and maize. Nat. Plants 7: 17–24. https://doi.org/10.1038/s41477-020-00834-5
Lu X., Zhao C., Shi H., Liao Y., Xu F., Du H., Xiao H., Zheng J. 2023. Nutrients and bioactives in citrus fruits: Different citrus varieties, fruit parts, and growth stages. Crit. Rev. Food Sci. Nutr. 63: 2018–2041. https://doi.org/10.1080/10408398.2021.1969891
Ma J., Clemants S. 2006. A history and overview of the Flora Reipublicae Popularis Sinicae (FRPS, Flora of China, Chinese edition, 1959–2004). Taxon 55: 451–460. https://doi.org/10.2307/25065592
Mabberley D. J. 1997. The plant-book: a portable dictionary of the vascular plants. Cambridge: Cambridge university press. 161 pp.
Mabberley D. J. 1998. Australian Citreae with notes on other Aurantioideae (Rutaceae). Telopea 7: 333–344.
Marie D., Brown S. C. 1993. A cytometric exercise in plant DNA histograms, with 2C values for 70 species. Biol. Cell 78: 41–51.
Moreno-Aguilar M. F., Arnelas I., Sánchez-Rodríguez A., Viruel J., Catalán P. 2020. Museomics unveil the phylogeny and biogeography of the neglected Juan Fernandez Archipelago Megalachne and Podophorus endemic grasses and their connection with relict Pampean-Ventanian fescues. Front. Plant Sci. 11: 819. https://doi.org/10.3389/fpls.2020.00819
Moreno-Aguilar M. F., Inda L. A., Sánchez-Rodríguez A., Arnelas I., Catalán P. 2022. Evolutionary dynamics of the repeatome explains contrasting differences in genome sizes and hybrid and polyploid origins of grass loliinae lineages. Front. Plant Sci. 13: 901733. https://doi.org/10.3389/fpls.2022.901733
Neumann P., Novák P., Hoštáková N., Macas J. 2019. Systematic survey of plant LTR-retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification. Mob. DNA 10: 1–17.
Nie Y., Liu X., Zhao L., Huang Y. 2024. Repetitive element expansions contribute to genome size gigantism in Pamphagidae: A comparative study (Orthoptera, Acridoidea). Genomics 116: 110896. https://doi.org/10.1016/j.ygeno.2024.110896
Novák P., Neumann P., Macas J. 2010. Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinform. 11: 378. https://doi.org/10.1186/1471-2105-11-378
Novák P., Neumann P., Macas J. 2020. Global analysis of repetitive DNA from unassembled sequence reads using RepeatExplorer2. Nat. Protoc. 15: 3745–3776. https://doi.org/10.1038/s41596-020-0400-y
Novák P., Neumann P., Pech J., Steinhaisl J., Macas J. 2013. RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics 29: 792–793. https://doi.org/10.1093/bioinformatics/btt054
Ollitrault P., Curk F., Krueger R. 2020. Chapter 4 – Citrus taxonomy. In: J. M. Talon, M. Caruso, F. G. Gmitter (eds.). The Genus Citrus. Woodhead Publishing. Pp. 57–81. https://doi.org/10.1016/B978-0-12-812163-4.00004-8
Paradis E., Claude J., Strimmer K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290. https://doi.org/10.1093/bioinformatics/btg412
Peng Z., Bredeson J. V., Wu G. A., Shu S., Rawat N., Du D., Parajuli S., Yu Q., You Q., Rokhsar D. S., Gmitter F. G., Deng Z. 2020. A chromosome‐scale reference genome of trifoliate orange (Poncirus trifoliata) provides insights into disease resistance, cold tolerance and genome evolution in Citrus. Plant J. 104: 1215–1232. https://doi.org/10.1111/tpj.14993
POWO [2025]. Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. URL: https://powo.science.kew.org/ (Accessed 10 March 2025).
Puterova J., Razumova O., Martinek T., Alexandrov O., Divashuk M., Kubat Z., Hobza R., Karlov G., Kejnovsky E. 2017. Satellite DNA and transposable elements in seabuckthorn (Hippophae rhamnoides), a dioecious plant with small Y and large X chromosomes. Genom. Biol. Evol. 9: 197–212.
Rogers S. O., Bendich A. J. 1985. Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol. Biol. 5: 69–76. https://doi.org/10.1007/BF00020088
Rosselló J. A., Maravilla A. J., Rosato M. 2022. The nuclear 35S rDNA world in plant systematics and evolution: A primer of cautions and common misconceptions in cytogenetic studies. Front. Plant Sci. 13: 788911. https://doi.org/10.3389/fpls.2022.788911
Schliep K. P. 2011. phangorn: phylogenetic analysis in R. Bioinformatics 27, 4: 592–593. https://doi.org/10.1093/bioinformatics/btq706
Singh R., Nath N. 1969. Practical approach to the classification of Citrus. In: Proceedings of International Citrus Symposium (Riverside, March 16–26, 1968 ). Vol 1. Riverside: University of California. Pp. 435–440.
Sun C., Lin H. 2021. The complete chloroplast genome and phylogenetic analysis of Citrus clementina (Rutaceae). Mitochondrial DNA, Part B. Resour. 6: 2926–2927. https://doi.org/10.1080/23802359.2021.1972860
Swingle W. T. 1915. A new genus, Fortunella, comprising four species of kumquat oranges. J. Wash. Acad. Sci. 5: 165–176.
Swingle W. T. 1943. The botany of Citrus and its wild relatives in the orange subfamily. The Citrus Industry 1: 128–474.
Swingle W. T. 1967. The botany of Citrus and its wild relatives. The Citrus Industry 1: 190–430.
Tanaka T. 1954. Species problem in citrus: A critical study of wild and cultivated units of citrus based upon field studies in their native homes (Revisio Aurantiacearum IX). JSPS 3: 141.
Tanaka T. 1977. Fundamental discussion of Citrus classification. Stud. Citrol. 14: 1.
Vitales D., Garcia S., Dodsworth S. 2020. Reconstructing phylogenetic relationships based on repeat sequence similarities. Mol. Phylogenetics Evol. 147: 106766. https://doi.org/10.1016/j.ympev.2020.106766
Vitte C., Fustier M.-A., Alix K., Tenaillon M. I. 2014. The bright side of transposons in crop evolution. Brief. Funct. Genom. 13: 276–295.
Wang T., Chen L.-L., Shu H.-J., You F., Liang X.-L., Li J., Ren J., Wanga V. O., Mutie F. M., Cai X. Z. 2022. Fortunella venosa (Champ. ex Benth.) C. C. Huang and F. hindsii (Champ. ex Benth.) swingle as independent species: evidence from morphology and molecular systematics and taxonomic revision of Fortunella (Rutaceae). Front. Plant Sci. 13: 867659.
Wang X., Xu Y., Zhang S., Cao L., Huang Y., Cheng J., et al. 2017. Genomic analyses of primitive, wild and cultivated Citrus provide insights into asexual reproduction. Nat. Genet. 49: 765–772. https://doi.org/10.1038/ng.3839
Wu G. A., Terol J., Ibanez V., López-García A., Pérez-Román E., Borredá C., et al. 2018. Genomics of the origin and evolution of Citrus. Nature 554: 311–316. https://doi.org/10.1038/nature25447
Wu Y., Wang F., Lyu K., Liu R. 2024. Comparative analysis of transposable elements in the genomes of Citrus and Citrus-related genera. Plants 13: 2462. https://doi.org/10.3390/plants13172462
Zhang Y., Barthe G., Grosser J. W., Wang N. 2016. Transcriptome analysis of root response to Citrus blight based on the newly assembled Swingle citrumelo draft genome. BMC Genom. 17: 485. https://doi.org/10.1186/s12864-016-2779-y
Zhu C., Zheng X., Huang Yu., Ye J., Chen P., Zhang C., et al. 2019. Genome sequencing and CRISPR /Cas9 gene editing of an early flowering Mini‐Citrus (Fortunella hindsii). Plant Biotechnol. J. 17(11): 2199–2210. https://doi.org/10.1111/pbi.13132
Bhattacharya S., Dutta S. 1956. Classification of citrus fruits of Assam. New Dehli: ICAR. 110 pp.
Burke W. D., Malik H. S. Rich S. M., Eickbush T. H. 2002. Ancient lineages of non-LTR retrotransposons in the primitive eukaryote, Giardia lamblia. MBE 19: 619–630. https://doi.org/10.1093/oxfordjournals.molbev.a004121
Chen G. F., Wang G. C., Zhang C. Y., Zhang B. Y., Wang X. K., Zhou B. C. 2008. Development of rRNA and rDNA-targeted probes for fluorescence in situ hybridization to detect Heterosigma akashiwo (Raphidophyceae). J. Exp. Mar. Biol. Ecol. 355: 66–75.
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
Dodsworth S., Chase M. W., Kelly L. J., Leitch I. J., Macas J., Novak, P., Piednoel M., Weiss-Schneeweiss H., Leitch A. R. 2015. Genomic repeat abundances contain phylogenetic signal. System. Biolog. 64: 112–126. https://doi.org/10.1093/sysbio/syu080
Domingues D. S., Cruz G. M., Metcalfe C. J., Nogueira F. T., Vicentini R., de S Alves C., Van Sluys M.-A. 2012. Analysis of plant LTR-retrotransposons at the fine-scale family level reveals individual molecular patterns. BMC Genom. 13: 1–14.
Drost H. G. 2018. Philentropy: information theory and distance quantification with R. JOSS 3: 765. https://doi.org/10.21105/joss.00765
Du D., Du X., Mattia M. R., Wang Y., Yu Q., Huang M., Yu Y., Grosser J. W., Gmitter F. G. 2018. LTR retrotransposons from the Citrus × clementina genome: characterization and application. Tree Genet. Genomes 14: 1–14.
FAO [2025]. FAOSTAT: Agricultural Production Data. URL: https://www.fao.org/.
Garcia S., Panero J. L., Siroky J., Kovarik A. 2010. Repeated reunions and splits feature the highly dynamic evolution of 5S and 35S ribosomal RNA genes (rDNA) in the Asteraceae family. BMC Plant Biol. 10: 1–18.
Garcia S., Wendel J. F., Borowska-Zuchowska N., Aïnouche M., Kuderova, A., Kovarik A. 2020. The utility of graph clustering of 5S ribosomal DNA homoeologs in plant allopolyploids, homoploid hybrids, and cryptic introgressants. Front. Plant Sci. 11: 41. https://doi.org/10.3389/fpls.2020.00041
Guerra M. dos S. 1984. Cytogenetics of rutaceae. II. Nuclear DNA content. Caryologia 37: 219–226.
He J., Lin S., Yu, Z., Song A., Guan Z., Fang W., Chen S., Zhang F., Jiang J., Chen F. 2021. Identification of 5S and 45S rDNA sites in Chrysanthemum species by using oligonucleotide fluorescence in situ hybridization (Oligo-FISH). Mol. Biol. Rep. 48: 21–31.
Herklotz V., Kovařík A., Wissemann V., Lunerová J., Vozárová R., Buschmann S., Olbricht K., Groth M., Ritz C. M. 2021. Power and weakness of repetition-evaluating the phylogenetic signal from repeatomes in the family Rosaceae with two case studies from genera prone to polyploidy and hybridization (Rosa and Fragaria). Front. Plant Sci. 12: 738119. https://doi.org/10.3389/fpls.2021.738119
Hodgson R. W. 1961. Taxonomy and nomenclature in citrus. In: IOCV Conference Proceedings (Gainesville, 1961). Vol 2(2). Riverside: University of California. Pp. 1–7.
Isobe S., Fujii, H., Shirasawa K., Kawahara Y., Endo T., Shimada T. 2023. Haploid-resolved and chromosome-scale genome assembly in Citrus unshiu and its parental species, C. nobilis and C. kinokuni. bioRxiv 2023.06.02.543356. https://doi.org/10.1101/2023.06.02.543356
Kashkush K., Feldman M., Levy A. A. 2003. Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat. Genet. 33: 102–106.
Katoh K., Standley D. M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. MBE 30: 772–780.
Kress W. J., Soltis D. E., Kersey P. J., Wegrzyn J. L., Leebens-Mack J. H., Gostel M. R., Liu X., Soltis P. S. 2022. Green plant genomes: What we know in an era of rapidly expanding opportunities. Proc. Natl. Acad. Sci. U.S.A. 119, 4: e2115640118. https://doi.org/10.1073/pnas.2115640118
Lee Y.-I., Yap J. W., Izan S., Leitch I. J., Fay M. F., Lee Y.-C., Hidalgo O., Dodsworth S., Smulders M. J. M., Gravendeel B., Leitch A. R. 2018. Satellite DNA in Paphiopedilum subgenus Parvisepalum as revealed by high-throughput sequencing and fluorescent in situ hybridization. BMC Genom. 19: 578. https://doi.org/10.1186/s12864-018-4956-7
Letunic I., Bork P. 2024. Interactive Tree of Life (iTOL) v6: recent updates to the phylogenetic tree display and annotation tool. Nucleic Acids Res. 52, 1: W78–W82. https://doi.org/10.1093/nar/gkae268
Lozano R., Gazave E., Dos Santos J. P. R., Stetter M. G., Valluru R., Bandillo N., et al. 2021. Comparative evolutionary genetics of deleterious load in sorghum and maize. Nat. Plants 7: 17–24. https://doi.org/10.1038/s41477-020-00834-5
Lu X., Zhao C., Shi H., Liao Y., Xu F., Du H., Xiao H., Zheng J. 2023. Nutrients and bioactives in citrus fruits: Different citrus varieties, fruit parts, and growth stages. Crit. Rev. Food Sci. Nutr. 63: 2018–2041. https://doi.org/10.1080/10408398.2021.1969891
Ma J., Clemants S. 2006. A history and overview of the Flora Reipublicae Popularis Sinicae (FRPS, Flora of China, Chinese edition, 1959–2004). Taxon 55: 451–460. https://doi.org/10.2307/25065592
Mabberley D. J. 1997. The plant-book: a portable dictionary of the vascular plants. Cambridge: Cambridge university press. 161 pp.
Mabberley D. J. 1998. Australian Citreae with notes on other Aurantioideae (Rutaceae). Telopea 7: 333–344.
Marie D., Brown S. C. 1993. A cytometric exercise in plant DNA histograms, with 2C values for 70 species. Biol. Cell 78: 41–51.
Moreno-Aguilar M. F., Arnelas I., Sánchez-Rodríguez A., Viruel J., Catalán P. 2020. Museomics unveil the phylogeny and biogeography of the neglected Juan Fernandez Archipelago Megalachne and Podophorus endemic grasses and their connection with relict Pampean-Ventanian fescues. Front. Plant Sci. 11: 819. https://doi.org/10.3389/fpls.2020.00819
Moreno-Aguilar M. F., Inda L. A., Sánchez-Rodríguez A., Arnelas I., Catalán P. 2022. Evolutionary dynamics of the repeatome explains contrasting differences in genome sizes and hybrid and polyploid origins of grass loliinae lineages. Front. Plant Sci. 13: 901733. https://doi.org/10.3389/fpls.2022.901733
Neumann P., Novák P., Hoštáková N., Macas J. 2019. Systematic survey of plant LTR-retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification. Mob. DNA 10: 1–17.
Nie Y., Liu X., Zhao L., Huang Y. 2024. Repetitive element expansions contribute to genome size gigantism in Pamphagidae: A comparative study (Orthoptera, Acridoidea). Genomics 116: 110896. https://doi.org/10.1016/j.ygeno.2024.110896
Novák P., Neumann P., Macas J. 2010. Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinform. 11: 378. https://doi.org/10.1186/1471-2105-11-378
Novák P., Neumann P., Macas J. 2020. Global analysis of repetitive DNA from unassembled sequence reads using RepeatExplorer2. Nat. Protoc. 15: 3745–3776. https://doi.org/10.1038/s41596-020-0400-y
Novák P., Neumann P., Pech J., Steinhaisl J., Macas J. 2013. RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics 29: 792–793. https://doi.org/10.1093/bioinformatics/btt054
Ollitrault P., Curk F., Krueger R. 2020. Chapter 4 – Citrus taxonomy. In: J. M. Talon, M. Caruso, F. G. Gmitter (eds.). The Genus Citrus. Woodhead Publishing. Pp. 57–81. https://doi.org/10.1016/B978-0-12-812163-4.00004-8
Paradis E., Claude J., Strimmer K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290. https://doi.org/10.1093/bioinformatics/btg412
Peng Z., Bredeson J. V., Wu G. A., Shu S., Rawat N., Du D., Parajuli S., Yu Q., You Q., Rokhsar D. S., Gmitter F. G., Deng Z. 2020. A chromosome‐scale reference genome of trifoliate orange (Poncirus trifoliata) provides insights into disease resistance, cold tolerance and genome evolution in Citrus. Plant J. 104: 1215–1232. https://doi.org/10.1111/tpj.14993
POWO [2025]. Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. URL: https://powo.science.kew.org/ (Accessed 10 March 2025).
Puterova J., Razumova O., Martinek T., Alexandrov O., Divashuk M., Kubat Z., Hobza R., Karlov G., Kejnovsky E. 2017. Satellite DNA and transposable elements in seabuckthorn (Hippophae rhamnoides), a dioecious plant with small Y and large X chromosomes. Genom. Biol. Evol. 9: 197–212.
Rogers S. O., Bendich A. J. 1985. Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol. Biol. 5: 69–76. https://doi.org/10.1007/BF00020088
Rosselló J. A., Maravilla A. J., Rosato M. 2022. The nuclear 35S rDNA world in plant systematics and evolution: A primer of cautions and common misconceptions in cytogenetic studies. Front. Plant Sci. 13: 788911. https://doi.org/10.3389/fpls.2022.788911
Schliep K. P. 2011. phangorn: phylogenetic analysis in R. Bioinformatics 27, 4: 592–593. https://doi.org/10.1093/bioinformatics/btq706
Singh R., Nath N. 1969. Practical approach to the classification of Citrus. In: Proceedings of International Citrus Symposium (Riverside, March 16–26, 1968 ). Vol 1. Riverside: University of California. Pp. 435–440.
Sun C., Lin H. 2021. The complete chloroplast genome and phylogenetic analysis of Citrus clementina (Rutaceae). Mitochondrial DNA, Part B. Resour. 6: 2926–2927. https://doi.org/10.1080/23802359.2021.1972860
Swingle W. T. 1915. A new genus, Fortunella, comprising four species of kumquat oranges. J. Wash. Acad. Sci. 5: 165–176.
Swingle W. T. 1943. The botany of Citrus and its wild relatives in the orange subfamily. The Citrus Industry 1: 128–474.
Swingle W. T. 1967. The botany of Citrus and its wild relatives. The Citrus Industry 1: 190–430.
Tanaka T. 1954. Species problem in citrus: A critical study of wild and cultivated units of citrus based upon field studies in their native homes (Revisio Aurantiacearum IX). JSPS 3: 141.
Tanaka T. 1977. Fundamental discussion of Citrus classification. Stud. Citrol. 14: 1.
Vitales D., Garcia S., Dodsworth S. 2020. Reconstructing phylogenetic relationships based on repeat sequence similarities. Mol. Phylogenetics Evol. 147: 106766. https://doi.org/10.1016/j.ympev.2020.106766
Vitte C., Fustier M.-A., Alix K., Tenaillon M. I. 2014. The bright side of transposons in crop evolution. Brief. Funct. Genom. 13: 276–295.
Wang T., Chen L.-L., Shu H.-J., You F., Liang X.-L., Li J., Ren J., Wanga V. O., Mutie F. M., Cai X. Z. 2022. Fortunella venosa (Champ. ex Benth.) C. C. Huang and F. hindsii (Champ. ex Benth.) swingle as independent species: evidence from morphology and molecular systematics and taxonomic revision of Fortunella (Rutaceae). Front. Plant Sci. 13: 867659.
Wang X., Xu Y., Zhang S., Cao L., Huang Y., Cheng J., et al. 2017. Genomic analyses of primitive, wild and cultivated Citrus provide insights into asexual reproduction. Nat. Genet. 49: 765–772. https://doi.org/10.1038/ng.3839
Wu G. A., Terol J., Ibanez V., López-García A., Pérez-Román E., Borredá C., et al. 2018. Genomics of the origin and evolution of Citrus. Nature 554: 311–316. https://doi.org/10.1038/nature25447
Wu Y., Wang F., Lyu K., Liu R. 2024. Comparative analysis of transposable elements in the genomes of Citrus and Citrus-related genera. Plants 13: 2462. https://doi.org/10.3390/plants13172462
Zhang Y., Barthe G., Grosser J. W., Wang N. 2016. Transcriptome analysis of root response to Citrus blight based on the newly assembled Swingle citrumelo draft genome. BMC Genom. 17: 485. https://doi.org/10.1186/s12864-016-2779-y
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Published
2025-10-11
How to Cite
Monakhos M. G., Ulyanov D. S., Romanov D. V., Smotrova Y. N., Korobkova V. A. The study of citrus plant evolution based on repetitive genomic elements, chloroplast genome, and 35S rDNA // Turczaninowia, 2025. Vol. 28, № 3. P. 60–69 DOI: 10.14258/turczaninowia.28.3.6. URL: https://turczaninowia.asu.ru/article/view/18000.
Section
Science articles
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