Although plants and animals are evolutionarily distant, the structure and function of their chromosomes are largely conserved. This allowed the establishment of a human-Arabidopsis hybrid cell line in which a neo-chromosome was formed by insertion of segments of Arabidopsis chromosomes into human chromosome 15. We used this unique system to investigate how the introgressed part of a plant genome was maintained in human genetic background. The analysis of the neo-chromosome in 60- and 300-day-old cell cultures by next-generation sequencing and molecular cytogenetics suggested its origin by fusion of DNA fragments of different sizes from Arabidopsis chromosomes 2, 3, 4, and 5, which were randomly intermingled rather than joined end-to-end. The neo-chromosome harbored Arabidopsis centromeric repeats and terminal human telomeres. Arabidopsis centromere wasn't found to be functional. Most of the introgressed Arabidopsis DNA was eliminated during the culture, and the Arabidopsis genome in 300-day-old culture showed significant variation in copy number as compared with the copy number variation in the 60-day-old culture. Amplified Arabidopsis centromere DNA and satellite repeats were localized at particular loci and some fragments were inserted into various positions of human chromosome. Neo-chromosome reorganization and behavior in somatic cell hybrids between the plant and animal kingdoms are discussed.

Centre for Research in Biotechnology for Agriculture Universiti Malaya 50603 Lembah Pantai Kuala Lumpur Malaysia

Graduate School of Human Development and Environment Kobe University Kobe Hyogo 657 8501 Japan

Graduate School of Pharmaceutical Sciences Osaka University Suita Osaka 565 0871 Japan

Graduate School of Technology Industrial and Social Sciences Tokushima University Tokushima Tokushima 770 8503 Japan

Institute of Experimental Botany of the Czech Academy of Sciences Centre of the Region Haná for Biotechnological and Agricultural Research Šlechtitelů 31 779 00 Olomouc Czech Republic

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Sci Rep. 2023 May 25;13(1):8487. doi: 10.1038/s41598-023-35329-8. PubMed

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Elsevier SM, et al. Assignment of the gene for galactokinase to human chromosome 17 and its regional localisation to band q21–22. Nature. 1974;251:633–636. doi: 10.1038/251633a0. PubMed DOI

Boyd Y. Characterization and use of somatic cell hybrids with interspecific translocations involving the human X chromosome. Ann. Hum. Genet. 1987;51:13–26. doi: 10.1111/j.1469-1809.1987.tb00863.x. PubMed DOI

Samoilovich SR, Dugan CB, Macario AJ. Hybridoma technology: new developments of practical interest. J. Immunol. Methods. 1987;101:153–170. doi: 10.1016/0022-1759(87)90147-5. PubMed DOI PMC

Weiss MC, Green H. Human-mouse hybrid cell lines containing partial complements of human chromosomes and functioning human genes. Proc. Natl. Acad. Sci. U. S. A. 1967;58:1104–1111. doi: 10.1073/pnas.58.3.1104. PubMed DOI PMC

Tomizuka K, et al. Functional expression and germline transmission of a human chromosome fragment in chimaeric mice. Nat. Genet. 1997;16:133–143. doi: 10.1038/ng0697-133. PubMed DOI

Shinohara T, et al. Stability of transferred human chromosome fragments in cultured cells and in mice. Chromosome Res. 2000;8:713–725. doi: 10.1023/a:1026741321193. PubMed DOI

Wang DY, Kumar S, Hedges SB. Divergence time estimates for the early history of animal phyla and the origin of plants, animals and fungi. Proc. Biol. Sci. 1999;266:163–171. doi: 10.1098/rspb.1999.0617. PubMed DOI PMC

Allshire RC, et al. A fission yeast chromosome can replicate autonomously in mouse cells. Cell. 1987;50:391–403. doi: 10.1016/0092-8674(87)90493-4. PubMed DOI

McManus J, et al. Unusual chromosome structure of fission yeast DNA in mouse cells. J. Cell Sci. 1994;107(Pt 3):469–486. doi: 10.1242/jcs.107.3.469. PubMed DOI

Maximilian HFJ, et al. Large domains of heterochromatin direct the formation of short mitotic chromosome loops. eLife. 2020;9:e57212. doi: 10.7554/eLife.57212. PubMed DOI PMC

Kishida M, Muguruma T, Sakanaka K, Katsuragi T, Sakai T. Chromosomal deletion or rearrangement in chimeric hybrids of Saccharomycopsis fibuligera and Saccharomyces diastaticus obtained by cell fusion. J. Ferment. Bioeng. 1996;81:281–285. doi: 10.1016/0922-338X(96)80577-0. DOI

Dudits D, Rasko I, Hadlaczky G, Lima-de-Faria A. Fusion of human cells with carrot protoplasts induced by polyethylene glycol. Hereditas. 1976;82:121–123. doi: 10.1111/j.1601-5223.1976.tb01545.x. PubMed DOI

Ahkong QF, et al. Fusion of hen erythrocytes with yeast protoplasts induced by polyethylene glycol. Nature. 1975;255:66–67. doi: 10.1038/255066a0. PubMed DOI

Zepp HD, Conover JH, Hirschhorn K, Hodes HL. Human-mosquito somatic cell hybrids induced by ultraviolet-inactivated Sendai virus. Nat. New Biol. 1971;229:119–121. doi: 10.1038/newbio229119a0. PubMed DOI

Wada N, et al. Maintenance and function of a plant chromosome in human cells. ACS Synth. Biol. 2017;6:301–310. doi: 10.1021/acssynbio.6b00180. PubMed DOI

Weckselblatt B, Rudd MK. Human structural variation: mechanisms of chromosome rearrangements. Trends Genet. 2015;31:587–599. doi: 10.1016/j.tig.2015.05.010. PubMed DOI PMC

Rausch T, et al. DELLY: structural variant discovery by integrated paired-end and split-read analysis. Bioinformatics. 2012;28:i333–i339. doi: 10.1093/bioinformatics/bts378. PubMed DOI PMC

Smit, A. F. A., R., H. & P., G. RepeatMasker Open-4.0., http://www.repeatmasker.org/ (2013–2015).

Xie C, Tammi MT. CNV-seq, a new method to detect copy number variation using high-throughput sequencing. BMC Bioinform. 2009;10:80. doi: 10.1186/1471-2105-10-80. PubMed DOI PMC

Richards EJ, Ausubel FM. Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell. 1988;53:127–136. doi: 10.1016/0092-8674(88)90494-1. PubMed DOI

Croce CM. Loss of mouse chromosomes in somatic cell hybrids between HT-1080 human fibrosarcoma cells and mouse peritioneal macrophages. Proc. Natl. Acad. Sci. U. S. A. 1976;73:3248–3252. doi: 10.1073/pnas.73.9.3248. PubMed DOI PMC

Kucherlapati RS, Ruddle FH. Mammalian somatic hybrids and human gene mapping. Ann. Intern. Med. 1975;83:553–560. doi: 10.7326/0003-4819-83-4-553. PubMed DOI

Johnston SD, Zee YP, López-Fernández C, Gosálvez J. The effect of chilled storage and cryopreservation on the sperm DNA fragmentation dynamics of a captive population of koalas. J. Androl. 2012;33:1007–1015. doi: 10.2164/jandrol.111.015248. PubMed DOI

Kopeika J, Thornhill A, Khalaf Y. The effect of cryopreservation on the genome of gametes and embryos: principles of cryobiology and critical appraisal of the evidence. Hum. Reprod. Update. 2015;21:209–227. doi: 10.1093/humupd/dmu063. PubMed DOI

Meyne J, et al. Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes. Chromosoma. 1990;99:3–10. doi: 10.1007/bf01737283. PubMed DOI

Reimann N, et al. Evidence that metacentric and submetacentric chromosomes in canine tumors can result from telomeric fusions. Cytogenet. Cell Genet. 1994;67:81–85. doi: 10.1159/000133804. PubMed DOI

Lee C, Sasi R, Lin CC. Interstitial localization of telomeric DNA sequences in the Indian muntjac chromosomes: further evidence for tandem chromosome fusions in the karyotypic evolution of the Asian muntjacs. Cytogenet. Cell Genet. 1993;63:156–159. doi: 10.1159/000133525. PubMed DOI

Schubert I, Schriever-Schwemmer G, Werner T, Adler ID. Telomeric signals in robertsonian fusion and fission chromosomes: implications for the origin of pseudoaneuploidy. Cytogenet. Cell Genet. 1992;59:6–9. doi: 10.1159/000133186. PubMed DOI

Schlötterer C, Tautz D. Slippage synthesis of simple sequence DNA. Nucleic Acids Res. 1992;20:211–215. doi: 10.1093/nar/20.2.211. PubMed DOI PMC

Messier W, Li SH, Stewart CB. The birth of microsatellites. Nature. 1996;381:483. doi: 10.1038/381483a0. PubMed DOI

Gascoigne KE, Cheeseman IM. Induced dicentric chromosome formation promotes genomic rearrangements and tumorigenesis. Chromosome Res. 2013;21:407–418. doi: 10.1007/s10577-013-9368-6. PubMed DOI PMC

Maciejowski J, Li Y, Bosco N, Campbell PJ, de Lange T. Chromothripsis and kataegis induced by telomere crisis. Cell. 2015;163:1641–1654. doi: 10.1016/j.cell.2015.11.054. PubMed DOI PMC

Gisselsson D, et al. Chromosomal breakage-fusion-bridge events cause genetic intratumor heterogeneity. Proc. Natl. Acad. Sci. U. S. A. 2000;97:5357–5362. doi: 10.1073/pnas.090013497. PubMed DOI PMC

MacKinnon RN, Duivenvoorden HM, Campbell LJ. Unbalanced translocations of 20q in AML and MDS often involve interstitial rather than terminal deletions of 20q. Cancer Genet. 2011;204:153–161. doi: 10.1016/j.cancergen.2010.12.001. PubMed DOI

Aravin AA, Hannon GJ, Brennecke J. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science. 2007;318:761–764. doi: 10.1126/science.1146484. PubMed DOI

Kapitonov VV, Jurka J. Molecular paleontology of transposable elements from Arabidopsis thaliana. Genetica. 1999;107:27–37. doi: 10.1023/A:1004030922447. PubMed DOI

Friend KK, Dorman BP, Kucherlapati RS, Ruddle FH. Detection of interspecific translocations in mouse-human hybrids by alkaline Giemsa staining. Exp. Cell Res. 1976;99:31–36. doi: 10.1016/0014-4827(76)90676-5. PubMed DOI

Stephens PJ, et al. Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell. 2011;144:27–40. doi: 10.1016/j.cell.2010.11.055. PubMed DOI PMC

Zhang CZ, et al. Chromothripsis from DNA damage in micronuclei. Nature. 2015;522:179–184. doi: 10.1038/nature14493. PubMed DOI PMC

Korbel JO, Campbell PJ. Criteria for inference of chromothripsis in cancer genomes. Cell. 2013;152:1226–1236. doi: 10.1016/j.cell.2013.02.023. PubMed DOI

Gu S, et al. Mechanisms for complex chromosomal insertions. PLoS Genet. 2016;12:e1006446. doi: 10.1371/journal.pgen.1006446. PubMed DOI PMC

Ly P, Cleveland DW. Rebuilding chromosomes after catastrophe: emerging mechanisms of chromothripsis. Trends Cell Biol. 2017;27:917–930. doi: 10.1016/j.tcb.2017.08.005. PubMed DOI PMC

Jovtchev G, Stergios M, Schubert I. A comparison of N-methyl-N-nitrosourea-induced chromatid aberrations and micronuclei in barley meristems using FISH techniques. Mutat. Res. 2002;517:47–51. doi: 10.1016/S1383-5718(02)00038-4. PubMed DOI

Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 1988;16:1215. doi: 10.1093/nar/16.3.1215. PubMed DOI PMC

Sánchez-Martín J, et al. Rapid gene isolation in barley and wheat by mutant chromosome sequencing. Genome Biol. 2016;17:221. doi: 10.1186/s13059-016-1082-1. PubMed DOI PMC

Tarasov A, Vilella AJ, Cuppen E, Nijman IJ, Prins P. Sambamba: fast processing of NGS alignment formats. Bioinformatics. 2015;31:2032–2034. doi: 10.1093/bioinformatics/btv098. PubMed DOI PMC

Simon, A., Pierre, L., Brian, H., & Phil, E. Babraham Bioinformatics—FastQC A Quality Control tool for High Throughput Sequence Data. https://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (2011).

Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC

Li H, et al. The sequence alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078–2079. doi: 10.1093/bioinformatics/btp352. PubMed DOI PMC

Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841–842. doi: 10.1093/bioinformatics/btq033. PubMed DOI PMC

Chikhi R, Rizk G. Space-efficient and exact de Bruijn graph representation based on a Bloom filter. Algorithms Mol. Biol. 2013;8:22. doi: 10.1186/1748-7188-8-22. PubMed DOI PMC

Chikhi R, Medvedev P. Informed and automated k-mer size selection for genome assembly. Bioinformatics. 2014;30:31–37. doi: 10.1093/bioinformatics/btt310. PubMed DOI

Sramkoski RM, et al. A new human prostate carcinoma cell line, 22Rv1. Vitro Cell. Dev. Biol. Anim. 1999;35:403–409. doi: 10.1007/s11626-999-0115-4. PubMed DOI

Ijdo, J. W., Wells, R. A., Baldini, A. & Reeders, S. T. Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. 19, 4780 (1991). PubMed PMC

Ohmido N, Fukui K. Visual verification of close disposition between a rice A genome-specific DNA sequence (TrsA) and the telomere sequence. Plant Mol. Biol. 1997;35:963–968. doi: 10.1023/A:1005822504690. PubMed DOI

Epigenetic Distribution of Recombinant Plant Chromosome Fragments in a Human-Arabidopsis Hybrid Cell Line