Centromeres of Cucumis melo L. comprise Cmcent and two novel repeats, CmSat162 and CmSat189

Autoři: Agus Budi Setiawan aff001;  Chee How Teo aff002;  Shinji Kikuchi aff001;  Hidenori Sassa aff001;  Kenji Kato aff003;  Takato Koba aff001
Působiště autorů: Laboratory of Genetics and Plant Breeding, Graduate School of Horticulture, Chiba University, Matsudo, Chiba, Japan aff001;  Center for Research in Biotechnology for Agriculture, University of Malaya, Kuala Lumpur, Malaysia aff002;  Graduate School of Environmental and Life Science, Okayama University, Kita-ku, Okayama, Japan aff003
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0227578


Centromeres are prerequisite for accurate segregation and are landmarks of primary constrictions of metaphase chromosomes in eukaryotes. In melon, high-copy-number satellite DNAs (SatDNAs) were found at various chromosomal locations such as centromeric, pericentromeric, and subtelomeric regions. In the present study, utilizing the published draft genome sequence of melon, two new SatDNAs (CmSat162 and CmSat189) of melon were identified and their chromosomal distributions were confirmed using fluorescence in situ hybridization. DNA probes prepared from these SatDNAs were successfully hybridized to melon somatic and meiotic chromosomes. CmSat162 was located on 12 pairs of melon chromosomes and co-localized with the centromeric repeat, Cmcent, at the centromeric regions. In contrast, CmSat189 was found to be located not only on centromeric regions but also on specific regions of the chromosomes, allowing the characterization of individual chromosomes of melon. It was also shown that these SatDNAs were transcribed in melon. These results suggest that CmSat162 and CmSat189 might have some functions at the centromeric regions.

Klíčová slova:

Centromeres – DNA sequence analysis – Melons – Repeated sequences – Sequence analysis – Tandem repeats – Tandem repeat sequence analysis – Satellite DNA


1. Rodríguez-Moreno L, González VM, Benjak A, et al. Determination of the melon chloroplast and mitochondrial genome sequences reveals that the largest reported mitochondrial genome in plants contains a significant amount of DNA having a nuclear origin. BMC Genomics. 2011; 12: 424. doi: 10.1186/1471-2164-12-424 21854637

2. Biscotti MA, Canapa A, Forconi M, et al. Transcription of tandemly repetitive DNA: functional roles. Chromosome Res. 2015; 23: 463–477. doi: 10.1007/s10577-015-9494-4 26403245

3. Mehrotra S, Goyal V. Repetitive sequences in plant nuclear DNA: Types, distribution, evolution and function. Genomics, Proteomics Bioinforma. 2014; 12: 164–171. doi: 10.1016/j.gpb.2014.07.003 25132181

4. Kubis S, Schmidt T, Heslop-Harrison JS. Repetitive DNA elements as a major component of plant genomes. Ann Bot. 1998; 82: 45–55.

5. Schmidt T. LINEs, SINEs and repetitive DNA: Non-LTR retrotransposons in plant genomes. Plant Mol Biol. 1999; 40:903–910. doi: 10.1023/a:1006212929794 10527415

6. Feschotte C, Pritham EJ. DNA transposons and the evolution of eukaryotic genomes. Ann Rev Genet. 2007; 41: 331–368. doi: 10.1146/annurev.genet.40.110405.090448 18076328

7. Garrido-Ramos MA. Satellite DNA in plants: More than just rubbish. Cytogenet Genome Res. 2015; 146: 153–170. doi: 10.1159/000437008 26202574

8. Pitrat M. Melon. In Handbook of crop breeding. Vol. I: Vegetables. ( Prohens J and Nuez F, eds) Springer, New York. 2008; pp: 283–315.

9. Hemleben V, Lewekel B, Roth A, Stadler J. Organization of highly repetitive satellite DNA of two Cucurbitaceae species (Cucumis melo and Cucumis sativus). Nucleic Acids Res. 1982; 10: 631–644. doi: 10.1093/nar/10.2.631 6278425

10. Brennicke A, Hemleben V. Sequence analysis of the cloned Cucumis melo highly repetitive satellite DNA. Z Naturforsch. 1983; 38: 1062–1065.

11. Han Y, Zhang Z, Liu C, et al. Centromere repositioning in cucurbit species: Implication of the genomic impact from centromere activation and inactivation. Proc Natl Acad Sci. 2009; 106: 14937–14941. doi: 10.1073/pnas.0904833106 19706458

12. Koo D-H, Nam Y-W, Choi D, et al. Molecular cytogenetic mapping of Cucumis sativus and C. melo using highly repetitive DNA sequences. Chromosom Res. 2010; 18: 325–336. doi: 10.1007/s10577-010-9116-0 20198418

13. Setiawan AB, Teo CH, Kikuchi S, et al. An improved method for inducing prometaphase chromosomes in plants. Mol Cytogenet. 2018; 11: 32. doi: 10.1186/s13039-018-0380-6 29760782

14. Han YH, Zhang ZH, Liu JH, et al. Distribution of the tandem repeat sequences and karyotyping in cucumber (Cucumis sativus L.) by fluorescence in situ hybridization. Cytogenet Genome Res. 2008; 122: 80–88. doi: 10.1159/000151320 18931490

15. Jiang J, Birchler JA, Parrott WA, Dawe RK. A molecular view of plant centromeres. Trends Plant Sci. 2003; 8: 570–575. doi: 10.1016/j.tplants.2003.10.011 14659705

16. Nagaki K, Talbert PB, Zhong CX, et al. Chromatin immunoprecipitation reveals that the 180-bp satellite repeat is the key functional DNA element of Arabidopsis thaliana centromeres. Genetics. 2003; 163: 1221–1225. 12663558

17. Nagaki K, Tanaka K, Yamaji N, et al. Sunflower centromeres consist of a centromere-specific LINE and a chromosome-specific tandem repeat. Front Plant Sci. 2015; 6: 1–12.

18. Tek AL, Kashihara K, Murata M, Nagaki K. Functional centromeres in Astragalus sinicus include a compact centromere-specific histone H3 and a 20-bp tandem repeat. Chromosom Res. 2011; 19: 969–978. doi: 10.1007/s10577-011-9247-y 22065151

19. Comai L, Maheshwari S, Marimuthu MPA. Plant centromeres. Curr Opin Plant Biol. 2017; 36: 158–167. doi: 10.1016/j.pbi.2017.03.003 28411416

20. Zhang W, Zuo S, Li Z, et al. Isolation and characterization of centromeric repetitive DNA sequences in Saccharum spontaneum. Sci Rep. 2017; 7: 1–12.

21. Garcia-Mas J, Benjak A, Sanseverino W, et al. The genome of melon (Cucumis melo L.). Proc Natl Acad Sci. 2012; 109: 11872–11877. doi: 10.1073/pnas.1205415109 22753475

22. Kalendar R, Khassenov B, Ramankulov Y, et al. FastPCR: An in silico tool for fast primer and probe design and advanced sequence analysis. Genomics. 2017; 109: 312–319. doi: 10.1016/j.ygeno.2017.05.005 28502701

23. Doyle JJ, Doyle JL. Isolation of plant DNA from fresh tissue. Focus. 1990; 12: 13–15.

24. Minamikawa MF, Fujii D, Kakui H, et al. Identifcation of an S-RNase binding protein1 (SBP1) homolog of apple (Malus×domestica). Plant Biotechnol. 2013; 30: 119–123. doi: 10.5511/plantbiotechnology.13.0109a

25. Kato S, Ohmido N, Hara M, Kataoka R, Fukui K. Image analysis of small plant chromosomes by using an improved system CHIAS IV. Chrom Sci. 2009; 12: 43–50.

26. Biscotti MA, Olmo E, Heslop-Harrison JS. Repetitive DNA in eukaryotic genomes. Chromosom Res. 2015; 23: 415–420. doi: 10.1007/s10577-015-9499-z 26514350

27. Shapiro JA, Von Sternberg R. Why repetitive DNA is essential to genome function. Biol Rev Camb Philos Soc. 2005; 80: 227–250. doi: 10.1017/s1464793104006657 15921050

28. Waminal NE, Choi H Il, Kim NH, et al. A refined Panax ginseng karyotype based on an ultra-high copy 167-bp tandem repeat and ribosomal DNAs. J Ginseng Res. 2016; 41: 469–476. doi: 10.1016/j.jgr.2016.08.002 29021693

29. Maluszynska J, Heslop-Harrison JS. Localization of tandemly repeated DNA sequences in Arabidopsis thaliana. Plant J. 1991; 1:159–166.

30. Gindullis F, Desel C, Galasso I, Schmidt T. The large-scale organization of the centromeric region in Beta species. Genome Res. 2001; 11: 253–265. doi: 10.1101/gr.162301 11157788

31. Cheng Z, Dong F, Langdon T, et al. Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell. 2002; 14:1691–1704. doi: 10.1105/tpc.003079 12172016

32. Henikoff S, Ahmad K, Malik HS. The centromere paradox: Stable inheritance with rapidly evolving DNA. Science. 2001; 293: 1098–1102. doi: 10.1126/science.1062939 11498581

33. Topp CN, Zhong CX, Dawe RK. Centromere-encoded RNAs are integral components of the maize kinetochore. Proc Natl Acad Sci. 2004; 101:15986–15991. doi: 10.1073/pnas.0407154101 15514020

34. May BP, Lippman ZB, Fang Y, et al. Differential regulation of strand-specific transcripts from Arabidopsis centromeric satellite repeats. PLoS Genet. 2005; 1: 0705–0714. doi: 10.1371/journal.pgen.0010079 16389298

35. Zhang W, Yi C, Bao W, et al. The transcribed 165-bp CentO satellite is the major functional centromeric element in the wild rice species Oryza punctata. Plant Physiol. 2005; 139:306–315. doi: 10.1104/pp.105.064147 16113220

36. Lee HR, Neumann P, Macas J, Jiang J. Transcription and evolutionary dynamics of the centromeric satellite repeat CentO in rice. Mol Biol Evol. 2006; 23: 2505–2520. doi: 10.1093/molbev/msl127 16987952

37. Teo CH. LTR retrotransposons and tandem repeats in Musa genomes and their contribution to Musa diversity and genome evolution. 2007; Doctoral Thesis, University of Leicester, UK.

38. Bouzinba-Segard H, Guais A, Francastel C. Accumulation of small murine minor satellite transcripts leads to impaired centromeric architecture and function. Proc Natl Acad Sci. 2006; 103: 8709–8714. doi: 10.1073/pnas.0508006103 16731634

39. Rošić S, Köhler F, Erhardt S. Repetitive centromeric satellite RNA is essential for kinetochore formation and cell division. J Cell Biol. 2014; 207:335–349. doi: 10.1083/jcb.201404097 25365994

40. Gent JI, Wang N, Dawe RK. Stable centromere positioning in diverse sequence contexts of complex and satellite centromeres of maize and wild relatives. Genome Biol. 2017; 18: 121 doi: 10.1186/s13059-017-1249-4 28637491

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