Skip to main content
SpringerLink
Log in

Quantitative trait locus analysis of cucumber fruit morphological traits based on image analysis

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

Fruit morphology is one of the most important traits in cucumber because it directly affects its commercial value. The cucumber line CS-PMR1 is a promising breeding material for improving disease resistance, but its fruit morphology is not ideal for the Japanese market, and this hampers breeding. We used recombinant inbred lines derived from a cross between CS-PMR1 and the Japanese cultivar ‘Santou’ for genetic analysis of fruit morphological traits. Fruit shape variation was evaluated in detail by means of image analysis, and quantitative trait locus (QTL) analyses were performed by composite interval mapping or interval mapping with a nonparametric model. We detected 41 QTLs: 5 for length, 6 for diameter, 5 for the ratio of length to diameter, 4 for the ratio of placenta diameter to fruit diameter, 16 for principal component scores of elliptic Fourier descriptors related to fruit shape, 2 for wart size and 3 for wart density. Some QTLs were detected in the same chromosomal regions at different fruit stages and for different morphological traits. In particular, several QTLs with large effects on fruit size were located in nearly the same regions as genes for resistance to powdery mildew and downy mildew, indicating that the linkage between fruit shape and the resistance genes is likely to limit breeding efficiency. The results of this study will contribute to the development of informative DNA markers tightly linked to genes for requisite fruit morphological traits, which are urgently required for efficient breeding of new cultivars.

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

  • Bo K, Ma Z, Chen J, Weng Y (2015) Molecular mapping reveals structural rearrangements and quantitative trait loci underlying traits with local adaptation in semi-wild Xishuangbanna cucumber (Cucumis sativus L. var. xishuangbannanesis Qi et Yuan). Theor Appl Genet 128:25–39

    Article  CAS  PubMed  Google Scholar 

  • Broman KW, Sen S (2009) A guide to QTL mapping with R/qtl. Springer, New York

    Book  Google Scholar 

  • Call AD, Wehner TC (2010) Gene list 2010 for cucumber. Cucurbit Genet Coop Rep 33–34:69–103

    Google Scholar 

  • Call AD, Criswell AD, Wehner TC, Klosinska U, Kozik EU (2012) Screening cucumber for resistance to downy mildew caused by Pseudoperonospora cubensis (Berk. and Curt.) Rostov. Crop Sci 52:577–592

    CAS  Google Scholar 

  • Cavagnaro PF, Senalik DA, Yang L, Simon PW, Harkins TT, Kodira CD, Huang S, Weng Y (2010) Genome-wide characterization of simple sequence repeats in cucumber (Cucumis sativus L.). BMC Genom 11:569

    Article  Google Scholar 

  • Chitwood DH, Headland LR, Kumar R, Peng J, Maloof JN, Sinha NR (2012) The developmental trajectory of leaflet morphology in wild tomato species. Plant Physiol 158:1230–1240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clement J, Novas N, Gazquez J-A, Manzano-Agugliaro F (2013) An active contour computer algorithm for the classification of cucumbers. Comput Electron Agric 92:75–81

    Article  Google Scholar 

  • Cui JY, Miao H, Ding LH, Wehner TC, Liu PN, Wang Y, Zhang SP, Gu XF (2016) A new glabrous gene (csgl3) identified in trichome development in cucumber (Cucumis sativus L.). PLoS ONE 11:e0148422

    Article  PubMed  PubMed Central  Google Scholar 

  • Dhillon NPS, Pushpinder PS, Ishiki K (1999) Evaluation of landraces of cucumber (Cucumis sativus L.) for resistance to downy mildew (Pseudoperonospora cubensis). Plant Genet Resour Newsl 119:59–61

    Google Scholar 

  • Fanourakis NE, Simon PW (1987) Analysis of genetic linkage in the cucumber. J Hered 78:238–242

    Article  Google Scholar 

  • Fazio G, 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

    Article  CAS  PubMed  Google Scholar 

  • Freeman H (1974) Computer processing of line-drawing images. ACM Comput Surv 6:57–97

    Article  Google Scholar 

  • Fukino N, Yoshioka Y, Kubo N, Hirai M, Sugiyama M, Sakata Y, Matsumoto S (2008) Development of 101 novel SSR markers and construction of an SSR-based genetic linkage map of cucumber (Cucumis sativus L.). Breed Sci 58:475–483

    Article  CAS  Google Scholar 

  • Fukino N, Yoshioka Y, Sugiyama M, Sakata Y, Matsumoto S (2013) Identification and validation of powdery mildew (Podosphaera xanthii)-resistant loci in recombinant inbred lines of cucumber (Cucumis sativus L.). Mol Breed 32:267–277

    Article  CAS  Google Scholar 

  • Iwata H, Ukai Y (2002) SHAPE: a computer program package for quantitative evaluation of biological shapes based on elliptic Fourier descriptors. J Hered 93:384

    Article  CAS  PubMed  Google Scholar 

  • Iwata H, Niikura S, Matsuura S, Takano Y, Ukai Y (1998) Evaluation of variation of root shape of Japanese radish (Raphanus sativus L.) based on image analysis using elliptic Fourier descriptors. Euphytica 102:143–149

    Article  Google Scholar 

  • Kennard WC, Havey MJ (1995) Quantitative trait analysis of fruit quality in cucumber: QTL detection, confirmation, and comparison with mating-design variation. Theor Appl Genet 91:53–61

    PubMed  Google Scholar 

  • Kooistra E (1968) Powdery mildew resistance in cucumber. Euphytica 17:236–244

    Google Scholar 

  • Kruglyak L, Lander ES (1995) A nonparametric approach for mapping quantitative trait loci. Genetics 139:1421–1428

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kuhl FP, Giardina CR (1982) Elliptic Fourier features of a closed contour. Comput Graph Image Process 18:236–258

    Article  Google Scholar 

  • Lebeda A, Prasil J (1994) Susceptibility of Cucumis sativus cultivars to Pseudoperonospora cubensis. Acta Phytopathol Entomol Hung 29:89–94

    Google Scholar 

  • Li Q, Cao C, Zhang C, Zheng S, Wang Z, Wang L, Ren Z (2015) The identification of Cucumis sativus Glabrous 1 (CsGL1) required for the formation of trichomes uncovers a novel function for the homeodomain-leucine zipper I gene. J Exp Bot 66:2515–2526

    Article  CAS  PubMed  Google Scholar 

  • Lootens P, Van Waes J, Carlier L (2007) Description of the morphology of roots of Chicorium intybus L. partim by means of image analysis: comparison of elliptic Fourier descriptors and classical parameters. Comput Electron Agric 58:164–173

    Article  Google Scholar 

  • Morishita M, Sugiyama K, Saito T, Sakata Y (2003) Powdery mildew resistance in cucumber. Jpn Agric Res Q 37:7–14

    Article  Google Scholar 

  • Neykov S, Dobrev D (1987) Introduced cucumber cultivars relatively resistant to Pseudoperonospora cubensis in Bulgaria. Acta Hortic 220:115–119

    Google Scholar 

  • Olczak-Woltman H, Marcinkowska J, Niemirowicz-Szczytt K (2011) The genetic basis of resistance to downy mildew in Cucumis spp.-latest developments and prospects. J Appl Genet 52:249–255

    Article  PubMed  PubMed Central  Google Scholar 

  • Pan Y, Bo K, Cheng Z, Weng Y (2015) The loss-of-function GLABROUS 3 mutation in cucumber is due to LTR-retrotransposon insertion in a class IV HD-ZIP transcription factor gene CsGL3 that is epistatic over CsGL1. BMC Plant Biol 15:302

    Article  PubMed  PubMed Central  Google Scholar 

  • Pan Y, Liang X, Gao M, Liu H, Meng H, Weng Y, Cheng Z (2017) Round fruit shape in WI7239 cucumber is controlled by two interacting quantitative trait loci with one putatively encoding a tomato SUN homolog. Theor Appl Genet 130:573–586

    Article  CAS  PubMed  Google Scholar 

  • Ren Y, Zhang Z, Liu J, Staub JE, Han Y, Cheng Z, Li X, Lu J, Miao H, Kang H, Xie B, Gu X, Wang X, Du Y, Jin W, Huang S (2009) An integrated genetic and cytogenetic map of the cucumber genome. PLoS ONE 4:e5795

    Article  PubMed  PubMed Central  Google Scholar 

  • Rohlf FJ, Archie JW (1984) A comparison of Fourier methods for the description of wing shape in mosquitoes (Diptera: Culicidae). Syst Zool 33:302–317

    Article  Google Scholar 

  • Sakata Y, Sugiyama M (2002) Characteristics of Japanese cucurbits. Acta Hortic 588:195–203

    Article  Google Scholar 

  • Sakata Y, Kubo N, Morishita M, Kitadani E, Sugiyama M, Hirai M (2006) QTL analysis of powdery mildew resistance in cucumber (Cucumis sativus L.). Theor Appl Genet 112:243–250

    Article  CAS  PubMed  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  CAS  PubMed  Google Scholar 

  • Serquen F, Bacher J, Staub JE (1997) Mapping and QTL analysis of horticultural traits in a narrow cross in cucumber (Cucumis sativus L.) using random-amplified polymorphic DNA markers. Mol Breed 3:257–268

    Article  CAS  Google Scholar 

  • Shetty NV, Wehner TC (1998) Evaluation of oriental trellis cucumbers for production in North Carolina. HortScience 33:891–896

    Google Scholar 

  • Shimizu S, Kanazawa K, Kato A (1963) Studies on the breeding of cucumber for resistance to downy mildew. Part 2. Difference of resistance to downy mildew among the cucumber varieties and the utility of the cucumber variety resistance to downy mildew. Bull Hort Res Sta A 2:47–64 (in Japanese with English abstract)

    Google Scholar 

  • Shimomura K, Horie H, Sugiyama M, Kawazu Y, Yoshioka Y (2016) Quantitative evaluation of cucumber fruit texture and shape traits reveals extensive diversity and differentiation. Sci Hortic 199:133–141

    Article  Google Scholar 

  • Smith P (1948) Powdery mildew resistance in cucumber. Phytopathology 39:1027–1028

    Google Scholar 

  • Staub J, Barczynska H, van Kleineww D, Palmer M, Lakowska E, Dijkhuizen A (1989) Evaluation of cucumber germplasm for six pathogens. In: Thomas CE (ed) Proceedings of Cucurbitaceae, vol 89, pp 149–153

  • Tanaka Y, Kuwaduru N, Nagata S (2012) Diallel analysis of root shape in Japanese radish ‘Sakurajima daikon’. Hortic Res 11:295–300

    Article  Google Scholar 

  • van Eck JW, van der Heijiden GWAM, Polder G (1998) Accurate measurement of size and shape of cucumber fruit with image analysis. J Agric Eng Res 70:335–343

    Article  Google Scholar 

  • Wang S, Basten CJ, Zeng ZB (2007) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm

  • Wang YL, Nie JT, Chen HM, Guo CL, Pan J, He HL, Pan JS, Cai R (2016) Identification and mapping of Tril, a homeodomain-leucine zipper gene involved in multicellular trichome initiation in Cucumis sativus. Theor Appl Genet 129:305–316

    Article  PubMed  Google Scholar 

  • Wehner TD, Shetty NV (1997) Downy mildew resistance of the cucumber germplasm collection in North Carolina field tests. Crop Sci 37:1331–1340

    Article  Google Scholar 

  • Wei Q, Wang Y, Qin X, Zhang Y, Zhang Z, Wang J, Li J, Lou Q, Chen J (2014) An SNP-based saturated genetic map and QTL analysis of fruit-related traits in cucumber using specific-length amplified fragment (SLAF) sequencing. BMC Genom 15:1–10

    Google Scholar 

  • Weng Y, Colle M, Wang Y, Yang L, Rubinstein M, Sherman A, Ophir R, Grumet R (2015) QTL mapping in multiple populations and development stages reveals dynamic quantitative trait loci for fruit size in cucumbers of different market classes. Theor Appl Genet 128:1747–1763

    Article  CAS  PubMed  Google Scholar 

  • Yang S, Miao H, Zhang S, Cheng Z, Zhou J, Dong S, Wehner T, Gu X (2011) Genetic analysis and mapping of gl-2 gene in cucumber (Cucumis sativus L.). Acta Hortic Sin 38:1685–1692

    CAS  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 13:1–14

    Article  Google Scholar 

  • Yang X, Zhang W, He H, Nie J, Bie B, Zhao J, Ren G, Li Y, Zhang D, Pan J, Cai R (2014) Tuberculate fruit gene Tu encodes a C2H2 zinc finger protein that is required for the warty fruit phenotype in cucumber (Cucumis sativus L.). Plant J 78:1034–1046

    Article  CAS  PubMed  Google Scholar 

  • Yoshioka Y, Iwata H, Ohsawa R, Ninomiya S (2004) Analysis of petal shape variation of Primula sieboldii by elliptic Fourier descriptors and principal component analysis. Ann Bot 94:657–664

    Article  PubMed  PubMed Central  Google Scholar 

  • Yoshioka Y, Ohsawa R, Iwata H, Ninomiya S, Fukuta N (2006) Quantitative evaluation of petal shape and picotee color pattern in lisianthus by image analysis. J Am Soc Hortic Sci 131:261–266

    Google Scholar 

  • Yoshioka Y, Sakata Y, Sugiyama M, Fukino N (2014) Identification of quantitative trait loci for downy mildew resistance in cucumber (Cucumis sativus L.). Euphytica 198:265–276

    Article  CAS  Google Scholar 

  • Yuan XJ, Li XZ, Pan JS, Wang G, Jiang S, Li XH, Deng SL, He HL, Si MX, Lai L, Wu AZ, Zhu LH, Cai R (2008a) Genetic linkage map construction and location of QTLs for fruit-related traits in cucumber. Plant Breed 127:180–188

    Article  CAS  Google Scholar 

  • Yuan XJ, Pan JS, Cai R, Guan Y, Liu LZ, Zhang WW, Li Z, He HL, Zhang C, Si LT, Zhu LH (2008b) 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 W, He H, Guan Y, Du H, Yuan L, Li Z, Yao D, Pan J, Cai R (2010) Identification and mapping of molecular markers linked to the tuberculate fruit gene in the cucumber (Cucumis sativus L). Theor Appl Genet 120:645–654

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Pan J, He H, Zhang C, Li Z, Zhao J, Yuan X, Zhu L, Huang S, Cai R (2012) Construction of a high density integrated genetic map for cucumber (Cucumis sativus L.). Theor Appl Genet 124:249–259

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Wang L, Zheng S, Liu Z, Wu X, Gao Z, Cao C, Li Q, Ren Z (2016a) A fragment substitution in the promoter of CsHDZIV11/CsGL3 is responsible for fruit spine density in cucumber (Cucumis sativus L.). Theor Appl Genet 129:1289–1301

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Liu S, Miao H, Wang M, Liu P, Wehner TC, Gu X (2016b) Molecular mapping and candidate gene analysis for numerous spines on the fruit of cucumber. J Hered 107:471–477

    Article  PubMed  Google Scholar 

  • Zijlstra S, Groot SPC (1992) Search for novel genes for resistance to powdery mildew (Sphaerotheca fuliginae) in cucumber (Cucumis sativus). Euphytica 64:31–37

    Google Scholar 

Download references

Acknowledgements

We thank F. Hori, S. Masuji, M. Shindo, M. Wakabayashi, Y. Taki, A. Suzuki and C. Yamada of the Institute of Vegetable and Floriculture Science, NARO, for technical assistance. This work was partly supported by JSPS KAKENHI Grant Number 26712004.

Author information

Authors and Affiliations

  1. Institute of Vegetable and Floriculture Science, National Agriculture and Food Research Organization (NARO), 360, Kusawa, Ano, Tsu, Mie, 514-2392, Japan

    Koichiro Shimomura, Nobuko Fukino, Mitsuhiro Sugiyama, Yoichi Kawazu & Yoshiteru Sakata

  2. Faculty of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki, 305-8572, Japan

    Yosuke Yoshioka

Authors
  1. Koichiro Shimomura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nobuko Fukino
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mitsuhiro Sugiyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yoichi Kawazu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yoshiteru Sakata
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yosuke Yoshioka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yosuke Yoshioka.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 19 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shimomura, K., Fukino, N., Sugiyama, M. et al. Quantitative trait locus analysis of cucumber fruit morphological traits based on image analysis. Euphytica 213, 138 (2017). https://doi.org/10.1007/s10681-017-1926-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10681-017-1926-0

Keywords

Search

Navigation