Skip to main content
Log in

Fine genetic mapping of the white immature fruit color gene w to a 33.0-kb region in cucumber (Cucumis sativus L.)

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

Abstract

Key message

The white immature fruit color gene w was rapidly mapped to a 33.0-kb region to identify a valuable candidate gene that encodes peroxidase.

Abstract

The skin color of immature fruit is a crucial external trait of cucumbers, and white skin is shared by limited numbers of commercial cultivars. Herein, one BC1 population and two F2 segregating populations were constructed using four inbred parental lines (WD3 × B-2-2 and Q30 × Q24) to investigate the inheritance patterns and chromosomal locations of immature fruit color genes in cucumbers. Consequently, a single recessive gene, w, was identified that controls white immature fruit color. A total of 526 markers, which were derived from published genetic maps, two reference cucumber genomes (“9930” and GY14), and two parents (Q30 and Q24) for which whole-genome sequence information is available, were used to map the target gene w to a 33.0-kb region flanked by two SNP-based markers, ASPCR39262 and ASPCR39229, which are physically located at 39262450 and 39229482 of chromosome 3 (“9930” draft genome assembly), respectively. Gene prediction indicated that four potential genes were located in the target region. One gene that encodes peroxidase is likely to be a valuable candidate gene because quantitative real-time PCR revealed an eightfold difference in its transcriptional level, and several amino acid variations were found when the deduced amino acid sequence was aligned. A co-segregating marker was used synergistically to test its ability to predict the skin colors of 83 dark green/white germplasms, and the validity of its utility in marker-assisted selection was confirmed. Fine mapping of this locus will assist in cloning the gene and in marker-assisted breeding to develop dark green/white cucumber cultivars.

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

Access this article

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

Similar content being viewed by others

References

  • Abeles FB, Dunn LJ (1989) Role of peroxidase during ethylene-induced chlorophyll breakdown in Cucumis sativus cotyledons. J Plant Growth Regul 8:319–325

    Article  CAS  Google Scholar 

  • Beale SI (2005) Green genes gleaned. Trends Plant Sci 10:309–312

    Article  CAS  PubMed  Google Scholar 

  • Bisognin DA (2002) Origin and evolution of cultivated cucurbits. Ciência Rural 32:715–723

    Article  Google Scholar 

  • Bollivar DW, Suzuki JY, Beatty JT, Dobrowolski JM, Bauer CE (1994) Directed mutational analysis of bacteriochlorophyll a biosynthesis in Rhodobacter capsulatus. J Mol Biol 237:622–640

    Article  CAS  PubMed  Google Scholar 

  • Cavagnaro PF, Senalik DA, Yang LM et al (2010) Genome-wide characterization of simple sequence repeats in cucumber (Cucumis sativus L.). BMC Genom 11:569. doi:10.1186/1471-2164-11-569

    Article  Google Scholar 

  • Chang CC-C, Ball L, Fryer MJ, Baker NR, Karpinski S, Mullineaux PM (2004) Induction of ASCORBATE PEROXIDASE 2 expression in wounded Arabidopsis leaves does not involve known wound-signalling pathways but is associated with changes in photosynthesis. Plant J 38:499–511. doi:10.1111/j.1365-313X.2004.02066.x

    Article  CAS  PubMed  Google Scholar 

  • Clark MS (ed) (1997) Plant molecular biology—a laboratory manual. Springer, Berlin. doi:10.1007/978-3-642-87873-2

  • Dong S, Miao H, Zhang S, Liu M, Wang Y, Gu X (2012) Genetic analysis and gene mapping of white fruit skin in cucumber (Cucumis sativus L.). Acta Bot Boreal Occident Sin 32:2177–2181

    CAS  Google Scholar 

  • Drenkard E, Richter BG, Rozen S et al (2000) A simple procedure for the analysis of single nucleotide polymorphisms facilitates map-based cloning in Arabidopsis. Plant Physiol 124:1483–1492

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Faris J, Laddomada B, Gill B (1998) Molecular mapping of segregation distortion loci in Aegilops tauschii. Genetics 149:319–327

    PubMed Central  CAS  PubMed  Google Scholar 

  • Feller A, Machemer K, Braun EL, Grotewold E (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 66:94–116

    Article  CAS  PubMed  Google Scholar 

  • Funamoto Y, Yamauchi N, Shigyo M (2003) Involvement of peroxidase in chlorophyll degradation in stored broccoli (Brassica oleracea L.) and inhibition of the activity by heat treatment. Postharvest Biol Technol 28:39–46

    Article  CAS  Google Scholar 

  • Howden R, Park SK, Moore JM, Orme J, Grossniklaus U, Twell D (1998) Selection of T-DNA-tagged male and female gametophytic mutants by segregation distortion in Arabidopsis. Genetics 149:621–631

    PubMed Central  CAS  PubMed  Google Scholar 

  • Huang S, Li R, Zhang Z et al (2009) The genome of the cucumber, Cucumis sativus L. Nat Genet 41:1275–1281. doi:10.1038/ng.475

    Article  CAS  PubMed  Google Scholar 

  • Hwang J, Oh J, Kim Z, Staub JE, Chung S-M, Park Y (2014) Fine genetic mapping of a locus controlling short internode length in melon (Cucumis melo L.). Mol Breeding 34:949–961. doi:10.1007/s11032-014-0088-1

    Article  CAS  Google Scholar 

  • Jacob-Wilk D, Holland D, Goldschmidt EE, Riov J, Eyal Y (1999) Chlorophyll breakdown by chlorophyllase: isolation and functional expression of the Chlase1 gene from ethylene-treated Citrus fruit and its regulation during development. Plant J 20:653–661. doi:10.1046/j.1365-313X.1999.00637.x

    Article  CAS  PubMed  Google Scholar 

  • Kooistra E (1971) Inheritance of fruit flesh and skin colours in powdery mildew resistant cucumbers (Cucumis sativus L.). Euphytica 20:521–523. doi:10.1007/bf00034206

    Google Scholar 

  • Ky C-L, Barre P, Lorieux M et al (2000) Interspecific genetic linkage map, segregation distortion and genetic conversion in coffee (Coffea sp.). Theor Appl Genet 101:669–676

    Article  CAS  Google Scholar 

  • Li Y (2008) SRAP markers linked to the green skin trait of cucumber. Dissertation. Northwest A&F University, Yangling

    Google Scholar 

  • Li Y, Wen C, Weng Y (2013) Fine mapping of the pleiotropic locus B for black spine and orange mature fruit color in cucumber identifies a 50 kb region containing a R2R3-MYB transcription factor. Theor Appl Genet 126:2187–2196. doi:10.1007/s00122-013-2128-3

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lorieux M, Goffinet B, Perrier X, de León DG, Lanaud C (1995a) Maximum-likelihood models for mapping genetic markers showing segregation distortion. 1. Backcross populations. Theor Appl Genet 90:73–80. doi:10.1007/bf00220998

    Article  CAS  PubMed  Google Scholar 

  • Lorieux M, Perrier X, Goffinet B, Lanaud C, de León DG (1995b) Maximum-likelihood models for mapping genetic markers showing segregation distortion. 2. F2 populations. Theor Appl Genet 90:81–89. doi:10.1007/bf00220999

    Article  CAS  PubMed  Google Scholar 

  • Lu H, Romero-Severson J, Bernardo R (2002) Chromosomal regions associated with segregation distortion in maize. Theor Appl Genet 105:622–628. doi:10.1007/s00122-002-0970-9

    Article  CAS  PubMed  Google Scholar 

  • McCouch S, Kochert G, Yu Z, Wang Z, Khush G, Coffman W, Tanksley S (1988) Molecular mapping of rice chromosomes. Theor Appl Genet 76:815–829. doi:10.1007/BF00273666

    Article  CAS  PubMed  Google Scholar 

  • Meglic V, Staub JE (1996) Inheritance and linkage relationships of isozyme and morphological loci in cucumber (Cucumis sativus L.). Theor Appl Genet 92:865–872. doi:10.1007/bf00221899

    Article  CAS  PubMed  Google Scholar 

  • Miao H, Zhang S, Wang X et al (2011) A linkage map of cultivated cucumber (Cucumis sativus L.) with 248 microsatellite marker loci and seven genes for horticulturally important traits. Euphytica 182:167–176. doi:10.1007/s10681-011-0410-5

    Article  Google Scholar 

  • Michaels SD, Amasino RM (1998) A robust method for detecting single-nucleotide changes as polymorphic markers by PCR. Plant J 14:381–385. doi:10.1046/j.1365-313X.1998.00123.x

    Article  CAS  PubMed  Google Scholar 

  • Motamayor JC, Mockaitis K, Schmutz J et al (2013) The genome sequence of the most widely cultivated cacao type and its use to identify candidate genes regulating pod color. Genome Biol 14:r53. doi:10.1186/gb-2013-14-6-r53

    Article  PubMed Central  PubMed  Google Scholar 

  • Neff MM, Neff JD, Chory J, Pepper AE (1998) dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics. Plant J 14:387–392

    Article  CAS  PubMed  Google Scholar 

  • Nie J, He H, Peng J et al (2015) Identification and fine mapping of pm5. 1: a recessive gene for powdery mildew resistance in cucumber (Cucumis sativus L.). Mol Breeding 35:1–13

    Article  CAS  Google Scholar 

  • Paterson AH, Lander ES, Hewitt JD, Peterson S, Lincoln SE, Tanksley SD (1988) Resolution of quantitative traits into mendelian factors by using a complete linkage map of restriction fragment length polymorphisms. Nature 335:721–726

    Article  CAS  PubMed  Google Scholar 

  • Phadnis N, Orr HA (2009) A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323:376–379

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Ren Y, Zhang ZH, Liu JH et al (2009) Integrated genetic and cytogenetic map of the cucumber genome. PLoS One 4:e5795. doi:10.1371/journal.pone.0005795

    Article  PubMed Central  PubMed  Google Scholar 

  • Salamov AA, Solovyev VV (2000) Ab initio gene finding in Drosophila genomic DNA. Genome Res 10:516–522

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sebastian P, Schaefer H, Telford IR, Renner SS (2010) Cucumber (Cucumis sativus) and melon (C. melo) have numerous wild relatives in Asia and Australia, and the sister species of melon is from Australia. Proc Natl Acad Sci 107:14269–14273

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Siegel BZ (1993) Plant peroxidases—an organismic perspective. Plant Growth Regul 12:303–312. doi:10.1007/bf00027212

    Article  CAS  Google Scholar 

  • Singh R, Low E-TL, Ooi LC-L et al (2014) The oil palm VIRESCENS gene controls fruit colour and encodes a R2R3-MYB. Nat Commun 5:4106. doi:10.1038/ncomms5106

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tripathi BN, Bhatt I, Dietz K-J (2009) Peroxiredoxins: a less studied component of hydrogen peroxide detoxification in photosynthetic organisms. Protoplasma 235:3–15

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Fang X, Li X, Chen Y, Fang Z, Xu Y (2013) Genetic study on immature fruit color of cucumber. Acta Hortic Sin 40:479–486

    Google Scholar 

  • Weng Y (2014) Molecularly tagged genes and quantitative trait loci in cucumber. Paper presented at the CUCURBITACEAE 2014, Bay Harbor, October 12–16, 2014

  • Weng Y, Li W, Devkota RN, Rudd JC (2005) Microsatellite markers associated with two Aegilops tauschii-derived greenbug resistance loci in wheat. Theor Appl Genet 110:462–469. doi:10.1007/s00122-004-1853-z

    Article  CAS  PubMed  Google Scholar 

  • Weng Y, Johnson S, Staub JE, Huang S (2010) An extended intervarietal microsatellite linkage map of cucumber, Cucumis sativus L. HortScience 45:882–886

    Google Scholar 

  • Xie J, Wehner TC (2001) Gene list 2001 for cucumber. Cucurbit Genet Coop Rep 24:110–136

    Google Scholar 

  • Yamauchi N, Funamoto Y, Shigyo M (2004) Peroxidase-mediated chlorophyll degradation in horticultural crops. Phytochem Rev 3:221–228. doi:10.1023/b:phyt.0000047796.98784.06

    Article  CAS  Google Scholar 

  • Yang L, Koo D-H, Li Y et al (2012) Chromosome rearrangements during domestication of cucumber as revealed by high-density genetic mapping and draft genome assembly. Plant J 71:895–906. doi:10.1111/j.1365-313X.2012.05017.x

    Article  CAS  PubMed  Google Scholar 

  • Yang L, Li D, Li Y, Gu X, Huang S, Garcia-Mas J, Weng Y (2013) A 1,681-locus consensus genetic map of cultivated cucumber including 67 NB-LRR resistance gene homolog and ten gene loci. BMC Plant Biol 13:53

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang X, Li Y, Zhang W, He H, Pan J, Cai R (2014a) Fine mapping of the uniform immature fruit color gene u in cucumber (Cucumis sativus L.). Euphytica 196:341–348

    Article  CAS  Google Scholar 

  • Yang X, Zhang W, Li Y et al (2014b) High-resolution mapping of the dull fruit skin gene D in cucumber (Cucumis sativus L.). Mol Breed 33:15–22

    Article  Google Scholar 

  • Yuan X, Pan J, Cai R et al (2008) Genetic mapping and QTL analysis of fruit and flower related traits in cucumber (Cucumis sativus L.) using recombinant inbred lines. Euphytica 164:473–491

    Article  CAS  Google Scholar 

  • Zhang WW, Pan JS, He HL et al (2012) Construction of a high density integrated genetic map for cucumber (Cucumis sativus L.). Theor Appl Genet 124:249–259. doi:10.1007/s00122-011-1701-x

    Article  CAS  PubMed  Google Scholar 

  • Zivy M, Devaux P, Blaisonneau J, Jean R, Thiellement H (1992) Segregation distortion and linkage studies in microspore-derived double haploid lines of Hordeum vulgare L. Theor Appl Genet 83:919–924. doi:10.1007/bf00226716

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful for the assistance provided by the laboratory of Yiqun Weng (USDA-ARS, Vegetable Crops Research Unit and Horticultural Department, University of Wisconsin, 1575 Linden Drive, Madison, WI 53706). We also thank Zheng Li for ideas and Dr. Sikandar Hayat and Husain Ahmad for critical reading of the manuscript. This research was supported by a grant from the National Natural Science Foundation of China (Project #31372074).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhihui Cheng.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

The authors declare that this study complies with the current laws of the countries in which the experiments were performed.

Additional information

Communicated by S. Huang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 1787 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, H., Meng, H., Pan, Y. et al. Fine genetic mapping of the white immature fruit color gene w to a 33.0-kb region in cucumber (Cucumis sativus L.). Theor Appl Genet 128, 2375–2385 (2015). https://doi.org/10.1007/s00122-015-2592-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-015-2592-z

Keywords

Navigation