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QTL-seq identifies an early flowering QTL located near Flowering Locus T in cucumber

Abstract

Key message

Next-generation sequencing enabled a fast discovery of a major QTL controlling early flowering in cucumber, corresponding to the FT gene conditioning flowering time in Arabidopsis.

Abstract

Next-generation sequencing technologies are making it faster and more efficient to establish the association of agronomic traits with molecular markers or candidate genes, which is the requirement for marker-assisted selection in molecular breeding. Early flowering is an important agronomic trait in cucumber (Cucumis sativus L.), but the underlying genetic mechanism is unknown. In this study, we identified a candidate gene for early flowering QTL, Ef1.1 through QTL-seq. Segregation analysis in F2 and BC1 populations derived from a cross between two inbred lines “Muromskij” (early flowering) and “9930” (late flowering) suggested quantitative nature of flowering time in cucumber. Genome-wide comparison of SNP profiles between the early and late-flowering bulks constructed from F2 plants identified a major QTL, designated Ef1.1 on cucumber chromosome 1 for early flowering in Muromskij, which was confirmed by microsatellite marker-based classical QTL mapping in the F2 population. Joint QTL-seq and traditional QTL analysis delimited Ef1.1 to an 890 kb genomic region. A cucumber gene, Csa1G651710, was identified in this region, which is a homolog of the FLOWERING LOCUS T (FT), the main flowering switch gene in Arabidopsis. Quantitative RT-PCR study of the expression level of Csa1G651710 revealed significantly higher expression in early flowering genotypes. Data presented here provide support for Csa1G651710 as a possible candidate gene for early flowering in the cucumber line Muromskij.

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References

  • Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H, Kanzaki H, Matsumura H, Yoshida K, Mitsuoka C, Tamiru M (2012) Genome sequencing reveals agronomically important loci in rice using MutMap. Nature Biotech 30:174–178

    CAS  Article  Google Scholar 

  • Chambers C, Shuai B (2009) Profiling microRNA expression in Arabidopsis pollen using microRNA array and real-time PCR. BMC Plant Biol 9(1):87

    PubMed Central  PubMed  Article  Google Scholar 

  • Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033

    CAS  PubMed  Article  Google Scholar 

  • Dijkhuizen A, Staub JE (2002) QTL conditioning yield and fruit quality traits in cucumber (Cucumis sativus L.) effects of environment and genetic background. J New Seeds 4:1–30

    Article  Google Scholar 

  • Ehrenreich IM, Torabi N, Jia Y, Kent J, Martis S et al (2010) Dissection of genetically complex traits with extremely large pools of yeast segregants. Nature 464:1039–1042

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Fazio F, Staub JE, Stevens MR (2003) Genetic mapping and QTL analysis of horticultural traits in cucumber (Cucumis sativus L.) using recombinant inbred lines. Theor Appl Genet 107:864–874

    CAS  PubMed  Article  Google Scholar 

  • Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, Lucas WJ, Wang X, Xie B, Ni P (2009) The genome of the cucumber, Cucumis sativus L. Nature Genet 41:1275–1281

    CAS  PubMed  Article  Google Scholar 

  • Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286(5446):1962–1965

    CAS  PubMed  Article  Google Scholar 

  • Kong F, Liu B, Xia Z, Sato S, Kim B, Watanabe S, Yamada T, Tabata S, Kanazawa A, Harada K, Abe J (2010) Two coordinately regulated homologs of FLOWERING LOCUS T are involved in the control of photoperiodic flowering in soybean. Plant Physiol 154:1220–1231

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Koornneef M, Alonso-Blanco C, Peeters AJ, Soppe W (1998) Genetic control of flowering time in Arabidopsis. Annu Rev Plant Biol 49:345–370

    CAS  Article  Google Scholar 

  • Lee R, Baldwin S, Kenel F, McCallum J, Macknight R (2013) FLOWERING LOCUS T genes control onion bulb formation and flowering. Nat Commun 4:2884

    PubMed  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Li Z, Zhang ZH, Yan PC, Huang SW, Fei ZJ, Lin K (2011) RNA-seq improves annotation of protein-coding genes in the cucumber genome. BMC Genom 12:540

    CAS  Article  Google Scholar 

  • Li Q, Zhang C, Li J, Wang L, Ren Z (2012) Genome-wide identification and characterization of R2R3MYB family in Cucumis sativus. PLoS One 7(10):e47576

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Lifschitz E, Eviatar T, Rozman A, Shalit A, Goldshmidt A, Amsellem Z, Alvarez JP, Eshed Y (2006) The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc Natl Acad Sci USA 103:6398–6403

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Lindhout P, Van Heusden S, Pet G, Van Ooijen JW, Sandbrink H, Verkerk R, Vrielink R, Zabel P (1994) Perspectives of molecular marker assisted breeding for earliness in tomato. Euphytica 79:279–286

    CAS  Article  Google Scholar 

  • Livaja M, Wang Y, Wieckhorst S, Haseneyer G, Seidel M, Hahn V, Knapp SJ, Taudien S, Schön C-C, Bauer E (2013) BSTA: a targeted approach combines bulked segregant analysis with next-generation sequencing and de novo transcriptome assembly for SNP discovery in sunflower. BMC Genom 14:628

    CAS  Article  Google Scholar 

  • Lv J, Qi J, Shi Q, Shen D, Zhang S, Shao G, Li H, Sun Z, Weng Y, Shang Y (2012) Genetic diversity and population structure of cucumber (Cucumis sativus L.). PLoS One 7:e46919

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Maheswaran M, Huang N, Sreerangasamy S, McCouch S (2000) Mapping quantitative trait loci associated with days to flowering and photoperiod sensitivity in rice (Oryza sativa L.). Mol Breed 6:145–155

    CAS  Article  Google Scholar 

  • Miao H, Gu XF, Zhang SP, Zhang ZH, Huang SW, Wang Y, Fang ZY (2012) Mapping QTLs for seedling-associated traits in cucumber. Acta Hort Sinica 39:879–887

    CAS  Google Scholar 

  • Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Murray M, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326

    CAS  PubMed Central  PubMed  Article  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

    CAS  PubMed  Article  Google Scholar 

  • Qi J, Liu X, Shen D, Miao H, Xie B, Li X, Zeng P, Wang S, Shang Y, Gu X (2013) A genomic variation map provides insights into the genetic basis of cucumber domestication and diversity. Nat Genet 45:1510–1515

    CAS  PubMed  Article  Google Scholar 

  • Ren Y, Zhang Z, Liu J, Staub JE, Han Y, Cheng Z, Li X, Lu J, Miao H, Kang H (2009) An integrated genetic and cytogenetic map of the cucumber genome. PLoS One 4:e5795

    PubMed Central  PubMed  Article  Google Scholar 

  • Robbins MD, Staub JE (2009) Comparative analysis of marker-assisted and phenotypic selection for yield components in cucumber. Theor Appl Genet 119:621–634

    PubMed  Article  Google Scholar 

  • Salvi S, Tuberosa R (2005) To clone or not to clone plant QTLs: present and future challenges. Trends Plant Sci 10:297–304

    CAS  PubMed  Article  Google Scholar 

  • Sato H, Heang D, Sassa H, Koba T (2009) Identification and characterization of FT/TFL1 gene family in cucumber. Breed Sci 59:3–11

    CAS  Article  Google Scholar 

  • Schneeberger K, Ossowski S, Lanz C, Juul T, Petersen AH, Nielsen KL, Jørgensen J-E, Weigel D, Andersen SU (2009) SHOREmap: simultaneous mapping and mutation identification by deep sequencing. Nat Methods 6:550–551

    CAS  PubMed  Article  Google Scholar 

  • Swinnen S, Schaerlaekens K, Pais T, Claesen J, Hubmann G et al (2012) Identification of novel causative genes determining the complex trait of high ethanol tolerance in yeast using pooled-segregant whole-genome sequence analysis. Genome Res 22:975–984

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Takagi H, Abe A, Yoshida K, Kosugi S, Natsume S, Mitsuoka C, Uemura A, Utsushi H, Tamiru M, Takuno S (2013) QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J 74:174–183

    CAS  PubMed  Article  Google Scholar 

  • Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science 316:1033–1036

    CAS  PubMed  Article  Google Scholar 

  • Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2005) Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol 138(4):2337–2343

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Taoka K, Ohki I, Tsuji H, Kojima C, Shimamoto K (2013) Structure and function of florigen and the receptor complex. Trends Plant Sci 18:287–294

    CAS  PubMed  Article  Google Scholar 

  • Tatlioglu T (1993) Cucumber Cucumis sativus L. Genetic improvement of vegetable crops. Pergamon Press, Tarrytown, pp 197–234

    Book  Google Scholar 

  • Van Ooijen JW (2011) Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genet Res 93(5):343–349

    Article  Google Scholar 

  • Van Ooijen JW, Boer MP, Jansen RC, Maliepaard C (2002) MapQTL4.0, software for the calculation of QTL positions on genetic maps. Plant Research International, Wagenigen

    Google Scholar 

  • Weng Y, Johnson S, Staub JE, Huang SW (2010) An extended microsatellite genetic map of cucumber, Cucumis sativus L. HortScience 45:880–886

    Google Scholar 

  • Yang Z, Huang D, Tang W, Zheng Y, Liang K, Cutler AJ, Wu WR (2013) Mapping of quantitative trait loci underlying cold tolerance in rice seedlings via high-throughput sequencing of pooled extremes. PLoS One 8(7):e68433

    CAS  PubMed Central  PubMed  Article  Google Scholar 

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Acknowledgments

This work was supported by funding from the National Natural Science Foundation of China (NSFC: 31225025), the National Program on Key Basic Research Projects in China (The 973 Program: 2012CB113900), the National High Tech Research Development Program in China (The 863 Program: 2010AA10A108, 2012AA100101), and the Chinese Ministry of Finance (1251610601001).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standard

The experiments in this study comply with the current laws of China.

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Correspondence to Sanwen Huang.

Additional information

H. Lu and T. Lin contributed equally.

Communicated by M. J. Havey.

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Lu, H., Lin, T., Klein, J. et al. QTL-seq identifies an early flowering QTL located near Flowering Locus T in cucumber. Theor Appl Genet 127, 1491–1499 (2014). https://doi.org/10.1007/s00122-014-2313-z

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  • DOI: https://doi.org/10.1007/s00122-014-2313-z

Keywords

  • Quantitative Trait Locus
  • Flowering Time
  • Quantitative Trait Locus Analysis
  • Quantitative Trait Locus Mapping
  • Early Flowering