Skip to main content
SpringerLink
Log in

Retrotransposon- and microsatellite sequence-associated genomic changes in early generations of a newly synthesized allotetraploid Cucumis × hytivus Chen & Kirkbride

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Allopolyploidization is considered an essential evolutionary process in plants that could trigger genomic shock in allopolyploid genome through activation of transcription of retrotransposons, which may be important in plant evolution. Two retrotransposon-based markers, inter-retrotransposon amplified polymorphism and retrotransposon-microsatellite amplified polymorphism and a microsatellite-based marker, inter simple sequence repeat were employed to investigate genomic changes in early generations of a newly synthesized allotetraploid Cucumis × hytivus Chen & Kirkbride (2n = 4x = 38) which was derived from crossing between cultivated cucumber C. sativus L. (2n = 2x = 14) and its wild relative C. hystrix Chakr. (2n = 2x = 24). Extensive genomic changes were observed, most of which involved the loss of parental DNA fragments and gain of novel fragments in the allotetraploid. Among the 28 fragments examined, 24 were lost while four were novel, suggesting that DNA sequence elimination is a relatively frequent event during polyploidization in Cucumis. Interestingly, of the 24 lost fragments, 18 were of C. hystrix origin, four were C. sativus-specific, and the remaining two were shared by both species, implying that fragment loss may be correlated with haploid DNA content (genome size) of diploid parents. Most changes were observed in the first generation after polyploidization (S1) and stably inherited in the subsequent three generations (S2–S4), indicating that genomic changes might be a rapid driving force for the stabilization of allotetraploids. Sequence analysis of 11 of the 28 altered DNA fragments showed that genomic changes in the allotetraploid occurred in both coding and non-coding regions, which might suggest that retrotransposons inserted into genome randomly and had a genome-wide effect on the allotetraploid evolution. Fluorescence in situ hybridization (FISH) analysis revealed a unique distribution of retrotransposon and/or microsatellite flanking sequences in mitotic and meiotic chromosomes, where the preferential FISH signals occurred in the centromeric and telomeric regions, implying that these regions were the possible hotspots for genomic changes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Adams KL, Cronn R, Percifeld R et al (2003) Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc Natl Acad Sci USA 100:4649–4654

    Article  PubMed  CAS  Google Scholar 

  • Baumel A, Ainouche M, Kalendar R et al (2002) Retrotransposons and genomic stability in populations of the young allopolyploid species Spartina anglica C.E. Hubbard (Poaceae). Mol Biol Evol 19(8):1218–1227

    Google Scholar 

  • Beaulieu J, Jean M, Belzile F (2009) The allotetraploid Arabidopsis thaliana-Arabidopsis lyrata subsp petraea as an alternative model system for the study of polyploidy in plants. Mol Genet Genomics 281:421–435

    Article  PubMed  CAS  Google Scholar 

  • Bento M, Pereira HS, Rocheta M et al (2008) Polyploidization as a retraction force in plant genome evolution: sequence rearrangements in Triticale. PLoS ONE 1(e1402):1–8

    Google Scholar 

  • Bento M, Gustafson JP, Viegas W et al (2011) Size matters in Triticeae polyploids: larger genomes have higher remodeling. Genome 54:175–183

    Article  PubMed  Google Scholar 

  • Chen LZ, Chen JF (2008) Changes of cytosine methylation induced by wide hybridization and allopolyploidy in Cucumis. Genome 51:789–799

    Article  PubMed  CAS  Google Scholar 

  • Chen JF, Kirkbride JJ (2000) A new synthetic species of Cucumis (Cucurbitaceae) from interspecific hybridization and chromosome doubling. Brittonia 52:315–319

    Article  Google Scholar 

  • Chen JF, Staub JE, Tashiro Y et al (1997) Successful interspecific hybridization between Cucumis sativus L. and Cucumis hystrix Chakr. Euphytica 96:413–419

    Article  Google Scholar 

  • Chen LZ, Lou QF, Zhuang Y et al (2007) Cytological diploidization and rapid genome changes of the newly synthesized allotetraploids Cucumis × hytivus. Planta 225:603–614

    Article  PubMed  CAS  Google Scholar 

  • Comai L (2000) Genetic and epigenetic interactions in allopolyploidy plants. Plant Mol Biol 43:387–399

    Article  PubMed  CAS  Google Scholar 

  • Contento A, Heslop-Harrison JS, Schwarzacher T (2005) Diversity of a major repetitive DNA sequence in diploid and polyploid Triticaeae. Cytogenet Genome Res 109:34–42

    Article  PubMed  CAS  Google Scholar 

  • Dernburg AF, Sedat JW, Hawley RS (1996) Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell 86:135–146

    Article  PubMed  CAS  Google Scholar 

  • Dolezel J, Greihuber J, Lucretti S et al (1998) Plant genome size estimation by flow cytometry: inter-laboratory comparison. Ann Bot 82(suppl 1):17–26

    Google Scholar 

  • Feldman M, Levy AA (2005) Allopolyploidy-a shaping force in the evolution of wheat genomes. Cytogenet Genome Res 109:250–258

    Article  PubMed  CAS  Google Scholar 

  • Feldman M, Liu B, Sehgal G et al (1997) Rapid elimination of low copy DNA sequence in polyploid wheat: a possible mechanism for differentiation of homoeologous chromosomes. Genetics 147:1381–1387

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jiang JM, Gill BS, Wang GL et al (1995) Metaphase and interphase fluorescence in situ hybridization mapping of the rice genome with bacterial artificial chromosomes. Proc Natl Acad Sci USA 92:4487–4491

    Article  PubMed  CAS  Google Scholar 

  • Jiang B, Lou QF, Wang D et al (2011) Allopolyploidization induced the activation of Ty1-copia retrotransposons in Cucumis hytivus, a newly formed Cucumis allotetraploid. Bot Stud 52:145–152

    CAS  Google Scholar 

  • Josefsson C, Dilkes B, Comai L (2006) Parent-dependent loss of gene silencing during interspecies hybridization. Curr Biol 16:1322–1328

    Article  PubMed  CAS  Google Scholar 

  • Kalendar R, Grob T, Regina M et al (1999) IRAP and REMAP: two new retrotransposon-based DNA fingerprinting techniques. Theor Appl Genet 98:704–711

    Article  CAS  Google Scholar 

  • Karpen GH, Le MH, Le H (1996) Centric heterochromatin and the efficiency of achiasmate disjunction in Drosophila female meiosis. Science 273:118–122

    Article  PubMed  CAS  Google Scholar 

  • Kashkush K, Feldman M, Levy AA (2002) Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160:1651–1659

    PubMed  CAS  Google Scholar 

  • Kashkush K, Feldman M, Levy AA (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet 33:102–106

    Article  PubMed  CAS  Google Scholar 

  • Kraitshtein Z, Yaakow B, Khasdan V et al (2010) Genetic and epigenetic dynamics of a retrotransposon after allopolyploidization of wheat. Genetics 186:801–812

    Article  PubMed  CAS  Google Scholar 

  • Leitch IJ, Bennett MD (1997) Polyploidy in angiosperms. Trends Plant Sci 2:470–476

    Article  Google Scholar 

  • Leitch IJ, Bennett MD (2004) Genome downsizing in polyploid plants. Biol J Linn Soc 82:651–663

    Article  Google Scholar 

  • Liu B, Wendel JF (2000) Retrotransposon activation followed by rapid repression in introgressed rice plants. Genome 43:874–880

    Article  PubMed  CAS  Google Scholar 

  • Liu ZL, Wang YM, Shen Y et al (2004) Extensive alterations in DNA methylation and transcription in rice caused by introgression from Zizania latifolia. Plant Mol Biol 54:571–582

    Article  PubMed  CAS  Google Scholar 

  • Ma XF, Gustafson JP (2006) Timing and rate of genome variation in triticale following allopolyploidization. Genome 49:950–958

    Article  PubMed  CAS  Google Scholar 

  • Madlung A, Masuelli RW, Watson B et al (2002) Remodeling of DNA methylation and phenotypic and transcriptional changes in synthetic Arabidopsis allopolyploids. Plant Physiol 129:733–746

    Article  PubMed  CAS  Google Scholar 

  • Madlung A, Tyagi AP, Watson B et al (2005) Genomic changes in synthetic Arabidopsis polyploids. Plant J 41:221–230

    Article  PubMed  CAS  Google Scholar 

  • McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801

    Article  PubMed  CAS  Google Scholar 

  • Messing J, Bharti AK, Karlowski WM et al (2004) Sequence composition and genome organization of maize. Proc Natl Acad Sci USA 101:14349–14354

    Article  PubMed  CAS  Google Scholar 

  • Murray HG, Thompson WF (1980) Rapid isolation of higher weight DNA. Nucl Acids Res 8:4321–4326

    Article  PubMed  CAS  Google Scholar 

  • Ozkan H, Levy A, Feldman M (2001) Allopolyploid-induced rapid genomic evolution in the wheat (Aegilops-Triticum) group. Plant Cell 13:1735–1747

    Article  PubMed  CAS  Google Scholar 

  • Petit M, Guidat C, Daniel J et al (2010) Mobilization of retrotransposons in synthetic allotetraploid tobacco. New Phytol 186:135–147

    Article  PubMed  CAS  Google Scholar 

  • Shan XH, Liu ZL, Dong ZY et al (2005) Mobilization of the active MITE transposons mPing and Pong in rice by introgression from wild rice (Zizania latifolia Griseb.). Mol Biol Evol 22:976–990

    Article  PubMed  CAS  Google Scholar 

  • Song K, Lu P, Tang K et al (1995) Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proc Natl Acad Sci USA 92:7719–7723

    Article  PubMed  CAS  Google Scholar 

  • Volkov RA, Borisjuk NV, Panchuk II et al (1999) Elimination and rearrangement of parental rDNA in the allotetraploid Nicotiana tabacum. Mol Biol Evol 16:311–320

    PubMed  CAS  Google Scholar 

  • Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249

    Article  PubMed  CAS  Google Scholar 

  • Zhuang Y, Chen JF (2009) Changes of gene expression in early generations of the synthetic allotetraploid Cucumis × hytivus Chen et Kirkbride. Genet Resour Crop Evol 56:1071–1076

    Article  Google Scholar 

Download references

Acknowledgments

This research was partially supported by the Key Program (30830079) and the General Program (31071801, 30972007) from the National Natural Science Foundation of China; National Basic Research Program of China (973 Program) (2009CB119000); the ‘863’ Programs (2008AA10Z150); the National Supporting Programs (2008BADB105) from the Ministry of Science and Technology of China; Ph. D. Funding (20070307034, 20090097110024) from the Ministry of Education of China; the Priority Academic Program Development of Jiangsu Higher Education Institution.

Author information

Authors and Affiliations

  1. State Key Laboratory of Crop Genetics and Germplasm Enhancement, Key Laboratory of Southern Vegetable Crop Genetic Improvement, College of Horticulture, Nanjing Agricultural University, Nanjing, 210095, China

    Biao Jiang, Qunfeng Lou, Zhiming Wu, Dong Wang, Kere George Mbira & Jinfeng Chen

  2. Vegetable Research Institute, Guangdong Academy of Agriculture Science, Guangzhou, 510640, China

    Biao Jiang

  3. Institute of Economic Crop Research, Hebei Academy of Agricultural and Forestry Sciences, Shijiazhuang, 050051, China

    Zhiming Wu

  4. College of Agriculture, Guizhou University, Guiyang, 550025, China

    Wanping Zhang

  5. USDA-ARS, Vegetable Crops Research Unit, Horticulture Department, University of Wisconsin, Madison, WI, 53705, USA

    Yiqun Weng

Authors
  1. Biao Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qunfeng Lou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhiming Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wanping Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kere George Mbira
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yiqun Weng
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jinfeng Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yiqun Weng or Jinfeng Chen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 189 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jiang, B., Lou, Q., Wu, Z. et al. Retrotransposon- and microsatellite sequence-associated genomic changes in early generations of a newly synthesized allotetraploid Cucumis × hytivus Chen & Kirkbride. Plant Mol Biol 77, 225–233 (2011). https://doi.org/10.1007/s11103-011-9804-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-011-9804-y

Keywords

Search

Navigation