Skip to main content
SpringerLink
Log in

Genetic association of ETHYLENE-INSENSITIVE3-like sequence with the sex-determining M locus in cucumber (Cucumis sativus L.)

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Cucumber (Cucumis sativus L.) has served as the model system for sex expression in flowering plants and its sex type is predominantly controlled by two genetic loci, F and M. Ethylene is the major plant hormone that regulates sex expression in cucumber. The current model predicts that ethylene serves as both a promoter of femaleness via the F locus and an inhibitor of the male sex via the M locus. In support of this model, genetic, genomic, and transcript analyses indicate that the F gene encodes a key enzyme in ethylene biosynthesis. In this study, we discovered that the M locus co-segregates with an ETHYLENE-INSENSITIVE3 (EIN3)-like genomic sequence in an F2 population of 96 individuals. This genetic association agrees with the prediction that the M locus is involved in ethylene signaling, thus providing another line of evidence in favor of the model. In addition, we generated an amplified fragment length polymorphism (AFLP®) map of the M locus, which was delimited into a genetic interval of 2.5 cM. The genetic association and the local map will assist the molecular isolation of the M gene using the combination of positional cloning and candidate gene approach.

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89:1133–1144

    Article  PubMed  CAS  Google Scholar 

  • Deng S-l, Pan J-s, He H-l, Wu A-z, R Cai (2006) SRAP molecular marker linked to M Gene in cucumber. J Shanghai Jiaotong Univer (Agric Sci) 24:240–244

    Google Scholar 

  • Galun E (1961) Study of the inheritance of sex expression in the cucumber, the interactions of major genes with modifying genetic and non-genetic factors. Genetica 32:134–163

    Article  Google Scholar 

  • Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7:40–49

    Article  PubMed  CAS  Google Scholar 

  • Iordachescu M, Verlinden S (2005) Transcriptional regulation of three EIN3-like genes of carnation (Dianthus caryophyllus L. cv. Improved White Sim) during flower development and upon wounding, pollination, and ethylene exposure. J Exp Bot 56:2011–2018

    Article  PubMed  CAS  Google Scholar 

  • Kamachi S, Sekimoto H, Kondo N, Sakai S (1997) Cloning of a cDNA for a 1-aminocyclopropane-1-carbo-xylate synthase that is expressed during development of female flowers at the apices of Cucumis sativus L. Plant Cell Physiol 38:1197–1206

    PubMed  CAS  Google Scholar 

  • Kende H (1993) Ethylene biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 44:283–307

    Article  CAS  Google Scholar 

  • Knopf RR, Trebitsh T (2006) The female-specific Cs-ACS1G gene of cucumber. A case of gene duplication and recombination between the non-sex-specific 1-aminocyclopropane-1-carboxylate synthase gene and a branched-chain amino acid transaminase gene. Plant Cell Physiol 47:1217–1228

    Article  PubMed  CAS  Google Scholar 

  • Kosambi DD (1944) The estimation of map distance from recombination values. Ann Eugen 12:172–175

    Google Scholar 

  • Kubicki B (1969a) Investigation of sex determination in cucumber (Cucumis sativus L.). Genet Pol 10:101–121

    Google Scholar 

  • Kubicki B (1969b) Investigation of sex determination in cucumber (Cucumis sativus L.). Genet Pol 10:5–22

    Google Scholar 

  • Kubicki B (1969c) Investigation of sex determination in cucumber (Cucumis sativus L.). Genet Pol 10:123–143

    Google Scholar 

  • Kubicki B (1969d) Investigations of sex determination in cucumber (Cucumis sativus L.). Genet Pol 10:69–86

    Google Scholar 

  • Malepszy S, Niemirowicz-Szczytt K (1991) Sex determination in cucumber (Cucumis sativus) as a model system for molecular biology. Plant Sci 80:39–47

    Article  Google Scholar 

  • Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer ML, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu P, Begley RF, Rothberg JM (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380

    PubMed  CAS  Google Scholar 

  • Mibus H, Tatlioglu T (2004) Molecular characterization and isolation of the F/f gene for femaleness in cucumber (Cucumis sativus L.). Theor Appl Genet 109:1669–1676

    Article  PubMed  CAS  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  PubMed  CAS  Google Scholar 

  • Myburg AA, Remington DL, O’ Malley DM, Sederoff RR, Whetten RW (2001) High-throughput AFLP analysis using infrared dye-labeled primers and an automated DNA sequencer. BioTechniques 30:348–357

    PubMed  CAS  Google Scholar 

  • Perl-Treves P (1999) Male to female conversion along the cucumber shoot: approaches to studying sex genes and floral development in Cucumis sativus. In: Ainsworth CC (ed) Sex determination in plants. BIOS Scientific Publisher, Oxford

  • Peterson CE, Staub JE, Williams PH, Palmer MJ (1986) Wisconsin 1983 cucumber. HortScience 21:1082–1083

    Google Scholar 

  • Pierce LK, Wehner TC (1990) Review of genes and linkage groups in cucumber. HortScience 25:605–615

    CAS  Google Scholar 

  • Rieu I, Mariani C, Weterings K (2003) Expression analysis of five tobacco EIN3 family members in relation to tissue-specific ethylene responses. J Exp Bot 54:2239–2244

    Article  PubMed  CAS  Google Scholar 

  • Rudich J, Halevy AH, Kedar N (1972) Ethylene evolution from cucumber plants as related to sex expression. Plant Physiol 49:998–999

    Article  PubMed  CAS  Google Scholar 

  • Shifriss O (1961) Sex control in cucumbers. J Hered 52:5–12

    Google Scholar 

  • Stam P (1993) Construction of integrated genetic linkage maps by means of a new computer package: Join Map. Plant J 3:739–744

    Article  CAS  Google Scholar 

  • Stepanova AN, Alonso JM (2005) Arabidopsis ethylene signaling pathway. Sci STKE 2005:cm4

  • Takahashi H, Saito T, Suge H (1983) Separation of effects of photoperiod and hormones on sex expression in cucumber. Plant Cell Physiol 24:142–154

    Google Scholar 

  • Tanurdzic M, Banks JA (2004) Sex-determining mechanisms in land plants. Plant Cell 16(Suppl):S61–S71

    Article  PubMed  CAS  Google Scholar 

  • Tieman DM, Ciardi JA, Taylor MG, Klee HJ (2001) Members of the tomato LeEIL (EIN3-like) gene family are functionally redundant and regulate ethylene responses throughout plant development. Plant J 26:47–58

    Article  PubMed  CAS  Google Scholar 

  • Trebitsh T, Staub JE, O’Neill SD (1997) Identification of a 1-aminocyclopropane-1-carboxylic acid synthase gene linked to the female (F) locus that enhances female sex expression in cucumber. Plant Physiol 113:987–995

    Article  PubMed  CAS  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M et al (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    Article  PubMed  CAS  Google Scholar 

  • Witkowicz J, Urbanczyk-Wochniak E, Przybecki Z (2003) AFLP marker polymorphism in cucumber (Cucumis sativus L.) near isogenic lines differing in sex expression. Cell Mol Biol Lett 8:375–381

    PubMed  CAS  Google Scholar 

  • Yamasaki S, Fujii N, Matsuura S, Mizusawa H, Takahashi H (2001) The M locus and ethylene-controlled sex determination in andromonoecious cucumber plants. Plant Cell Physiol 42:608–619

    Article  PubMed  CAS  Google Scholar 

  • Yamasaki S, Fujii N, Takahashi H (2003) Photoperiodic regulation of CS-ACS2, CS-ACS4 and CS-ERS gene expression contributes to the femaleness of cucumber flowers through diurnal ethylene production under short-day conditions. Plant Cell Environ 26:537–546

    Article  CAS  Google Scholar 

  • Yin T, Quinn JA (1995) Tests of a mechanistic model of one hormone regulating both sexes in Cucumis sativus (Cucurbitaceae). Am J Bot 82:1537–1546

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The experiment was carried out in the Sino-Dutch Joint Lab of Horticultural Genomics Technology and the Opening Lab of Vegetable Genetics and Physiology of Ministry of Agriculture, both located in the Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences. We thank Dr. J. E. Staub (Agricultural Research Service, U. S. Department of Agriculture, Horticulture Department, University of Wisconsin, Madison) for providing the cucumber materials and Dr. Zhonghua Zhang of our lab for bioinformatics analysis. This work was supported by grants from Ministry of Agriculture (“948” Program: 2008-Z42) and Ministry of Science and Technology (2006DFA32140) to S. H.

Author information

Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, College of Life Sciences, Nanjing Agricultural University, 210095, Nanjing, China

    Shiqiang Liu & Qing Yang

  2. Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, 100081, Beijing, China

    Shiqiang Liu, Zhiqi Jia & Sanwen Huang

  3. Lab of Biochemistry and Fermentation, Hunan Agricultural University, 410128, Changsha, China

    Liang Xu, Xiangyang Lu & Huiming Chen

  4. Hunan Vegetable Research Institute, Hunan Academy of Agricultural Sciences, 410125, Changsha, China

    Liang Xu, Xiangyang Lu & Huiming Chen

  5. Beijing Vegetable Research Centre, 100089, Beijing, China

    Yong Xu

  6. Boyce Thompson Institute and USDA Plant, Soil, and Nutrition Laboratory, Cornell University, 14853, Ithaca, NY, USA

    Zhangjun Fei

Authors
  1. Shiqiang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhiqi Jia
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yong Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qing Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhangjun Fei
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiangyang Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Huiming Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Sanwen Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Huiming Chen or Sanwen Huang.

Additional information

Communicated by I. L. Goldman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, S., Xu, L., Jia, Z. et al. Genetic association of ETHYLENE-INSENSITIVE3-like sequence with the sex-determining M locus in cucumber (Cucumis sativus L.). Theor Appl Genet 117, 927–933 (2008). https://doi.org/10.1007/s00122-008-0832-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-008-0832-1

Keywords

Search

Navigation