Skip to main content
SpringerLink
Log in

Variation in cucumber (Cucumis sativus L.) fruit size and shape results from multiple components acting pre-anthesis and post-pollination

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Morphological, QTL, and gene expression analyses indicate variation in cucumber fruit size and shape results from orientation, timing, and extent of cell division and expansion, and suggest candidate gene factors.

Variation in cucumber (Cucumis sativus L.) fruit size and shape is highly quantitative, implicating interplay of multiple components. Recent studies have identified numerous fruit size and shape quantitative trait loci (QTL); however, underlying factors remain to be determined. We examined ovary and fruit development of two sequenced cucumber genotypes with extreme differences in fruit size and shape, Chinese Long ‘9930’ (CL9930), and pickling type ‘Gy14’. Differences were observed in several independent factors that can influence size and shape: ovule number, rate and period of cell division in longitudinal and cross section in ovaries and fruit, timing and rate of fruit expansion in length and diameter, and cell shape. Level and timing of expression of select fruit growth stage marker genes and candidate fruit size gene homologs associated with cucumber fruit size and shape QTL were examined from 5-day pre-anthesis to 20-day post-pollination. Our results indicate that variation in fruit size and shape results from differences in cell number and shape in longitudinal and cross section, driven in turn by differences in orientation, timing, and duration of cell division and expansion, both pre- and post-anthesis, and suggest candidate genes contributing to determination of cucumber fruit size and shape.

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
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

dpa:

Days pre-anthesis

dpp:

Days post-pollination

RIL:

Recombinant inbred line

References

  • Alba R, Payton P, Fei ZJ, McQuinn R, Debbie P, Martin GB, Tanksley SD, Giovannoni JJ (2005) Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development. Plant Cell 17:2954–2965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ando K, Grumet R (2010) Transcriptional profiling of rapidly growing cucumber fruit by 454 pyrosequencing analysis. J Am Soc Hortic Sci 135:291–302

    Google Scholar 

  • Ando K, Carr KM, Grumet R (2012) Transcriptome analysis of early cucumber fruit growth identifies distinct gene modules associated with phases of development. BMC Genom 13:518

    Article  CAS  Google Scholar 

  • Ando K, Carr KM, Colle M, Mansfeld BN, Grumet R (2015) Exocarp properties and transcriptomic analysis of cucumber (Cucumis sativus) fruit expressing resistance to Phytophthora capsici. PLoS One 10:e0142133. doi:10.1371/journal.pone.0142133

    Article  PubMed  PubMed Central  Google Scholar 

  • 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. xishuangbannaensis Qi et Yuan). Theor Appl Genet 128:25–39

    Article  CAS  PubMed  Google Scholar 

  • Bohner J, Bangerth F (1988) Cell number, cell size and hormone levels in semi-isogenic mutants of Lycopersicon pimpinellifolium differing in fruit size. Physiol Plant 72:316–320

    Article  CAS  Google Scholar 

  • Boonkorkaew P, Hikosaka S, Sugiyama N (2008) Effect of pollination on cell division, cell enlargement, and endogenous hormones in fruit development in a gynoecious cucumber. Sci Hortic 116:1–7

    Article  CAS  Google Scholar 

  • Carabelli M, Turchi L, Ruzza V, Morelli G, Ruberti I (2013) Homeodomain-leucine zipper II family of transcription factors to the limelight. Central regulators of plant development. Plant Signal Behav 8:25447

    Article  Google Scholar 

  • Chang Y, Sun R, Sun H, Zhao Y, Han Y, Chen D, Wang Y, Zhang X, Han Z (2014) Mapping of quantitative trait loci corroborates independent genetic control of apple size and shape. Sci Hortic 174:126–132

    Article  Google Scholar 

  • Cheng GW, Breen PJ (1992) Cell count and size in relation to fruit size among strawberry cultivars. J Am Soc Hortic Sci 117:946–950

    Google Scholar 

  • Cui L, Li J, Zhang T, Guo Q, Xu J, Lou Q, Chen J (2014) Identification and expression analysis of D-type cyclin genes in early developing fruit of cucumber (Cucumis sativus L.). Plant Mol Biol Rep 32:209–218

    Article  CAS  Google Scholar 

  • Dahan Y, Rosenfeld R, Zadiranov V, Irihimovitch V (2010) A proposed conserved role for an avocado fw2.2-like gene as a negative regulator of fruit cell division. Planta 232:663–676

    Article  CAS  PubMed  Google Scholar 

  • Das D, St. Onge KR, Voesenek LACJ, Pierik R, Sasidharan R (2016) Ethylene- and shade-induced hypocotyl elongation share transcriptome patterns and functional regulators. Plant Physiol 172:718–733

    CAS  PubMed  PubMed Central  Google Scholar 

  • Diaz A, Zarouri B, Fergany M, Eduardo I, Alvarez JM, Pico B, Monforte AJ (2014) Mapping and introgression of QTL involved in fruit shape and transgressive segregation into ‘Piel de Sapo’ melon (Cucumis melo L.). PLoS One 9:e104188. doi:10.1371/journal.pone.0104188

    Article  PubMed  PubMed Central  Google Scholar 

  • Eduardo I, Arus P, Monforte AJ, Obando J, Fernandez-Trujillo JP, Martinez JA, Alarcon AL, Alvarez JM, van der Knapp E (2007) Estimating the genetic architecture of fruit quality traits in melon using a genomic library of near isogenic lines. J Am Soc Hortic Sci 132:80–89

    Google Scholar 

  • Fanwoua J, de Visser PHB, Heuvelink E, Yin X, Struik PC, Marcelis LFM (2013) A dynamic model of tomato fruit growth integrating cell division, cell growth and endoreduplication. Funct Plant Biol 40:1098–1114

    Article  Google Scholar 

  • Fernandez-Silva I, Moreno E, Essafi A, Fergany M, Garcia-Mas J, Martín-Hernandez AM, Alvarez JM, Monforte AJ (2010) Shaping melons: agronomic and genetic characterization of QTLs that modify melon fruit morphology. Theor Appl Genet 121:931–940

    Article  PubMed  Google Scholar 

  • Frary A, Nesbitt TC, Frary A, Grandillo S, van der Knapp E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tanksley SD (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88

    Article  CAS  PubMed  Google Scholar 

  • Fu FQ, Mao WH, Shi K, Zhou YH, Asami T, Yu JQ (2008) A role of brassinosteroids in early fruit development in cucumber. J Exp Bot 9:2299–2308

    Article  Google Scholar 

  • Fu FQ, Mao WH, Shi K, Zhou YH, Yu JQ (2010) Spatio-temporal changes in cell division, endoreduplication and expression of cell cycle-related genes in pollinated and plant growth substances-treated ovaries of cucumber. Plant Biol 12:98–107

    Article  CAS  PubMed  Google Scholar 

  • Gillaspy G, Ben-David H, Gruissem W (1993) Fruits: a developmental perspective. Plant Cell 5:1439–1451

    Article  PubMed  PubMed Central  Google Scholar 

  • Grumet R, Colle M (2016) Genomic analysis of cucurbit fruit growth. In: Grumet R, Katzir N, Garcia-Mas J (eds) Genetics and genomics of Cucurbitaceae. Plant genetics and genomics: crops and models. Springer, Berlin. doi:10.1007/7397_2016_4

  • Hammami SBM, Manrique T, Rapoport HF (2011) Cultivar-based fruit size in olive depends on different tissue and cellular processes throughout growth. Sci Hortic 130:445–451

    Article  Google Scholar 

  • Higashi K, Hosoya K, Ezura H (1999) Histological analysis of fruit development between two melon (Cucumis melo L. reticulatus) genotypes setting a different size of fruit. J Exp Bot 50:1593–1597

    Article  CAS  Google Scholar 

  • Hu DL, Richards P, Alexeev A (2011) The growth of giant pumpkins: how extreme weight influences shape. Internat J Nonlinear Mech 46:637–647

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Jackson D (1992) In situ hybridization in plants. In: Gurr SJ, McPherson M, Bowles DF (eds) Molecular plant pathology: a practical approach. Oxford University Press, Oxford, pp 163–174

    Google Scholar 

  • Jiang L, Yan S, Yang W, Li Y, Xiz Y, Xia M, Cheng Z, Wang Q, Yan L, Song X, Liu R, Zhang X (2015) Transcriptomic analysis reveals the roles of microtubule-related genes and transcription factors in fruit length regulation in cucumber (Cucumis sativus L.). Sci Rep 5:8031. doi:10.1038/srep08031

    Article  PubMed  PubMed Central  Google Scholar 

  • Johnson LK, Malladi A (2011) Differences in cell number facilitate fruit size variation in rabbiteye blueberry genotypes. J Am Soc Hortic Sci 136:10–15

    Google Scholar 

  • Kende H, van der Knaap E, Cho HT (1998) Deepwater rice: a model plant to study stem elongation. Plant Physiol 118:1105–1110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koyama T, Okada T, Kitajima S, Ohme-Takagi M (2003) Isolation of tobacco ubiquitin-conjugating enzyme cDNA in a yeast two-hybrid system with tobacco ERF3 as bait and its characterization of specific interaction. J Exp Bot 54:1175–1181

    Article  CAS  PubMed  Google Scholar 

  • Li J, Wu Z, Cui L, Zhang T, Guo Q, Xu J, Jia L, Lou Q, Huang S, Li Z, Chen J (2014) Transcriptome comparison of global distinctive features between pollination and parthenocarpic fruit set reveals transcriptional phytohormone cross-talk in cucumber (Cucumis sativus L.). Plant Cell Physiol 55:1325–1342

    Article  CAS  PubMed  Google Scholar 

  • Liu JP, Van Eck J, Cong B, Tanksley SD (2002) A new class of regulatory genes underlying the cause of pear-shaped tomato fruit. Proc Nat Acad Sci USA 99:13302–13306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marcelis LFM (1993) Effect of assimilate supply on growth of individual cucumber fruits. Physiol Plant 87:313–320

    Article  CAS  Google Scholar 

  • Marcelis LFM, Hofman-Eijer LRB (1993) Cell division and expansion in the cucumber fruit. J Hortic Sci 68:665–671

    Article  Google Scholar 

  • Miao H, Gu XF, Zhang SP (2011) Mapping QTLs for fruit-associated traits in Cucumis sativus L. Sci Agric Sin 44:531–540

    Google Scholar 

  • Monforte AJ, Diaz A, Cano-Delgado A, van der Knaap E (2014) The genetic basis of fruit morphology in horticultural crops: lessons from tomato and melon. J Exp Bot 65:4625–4637

    Article  CAS  PubMed  Google Scholar 

  • Nakata Y, Taniguchi G, Takazaki S, Ode-Uda N, Miyahara K, Ohshima Y (2012) Comparative analysis of cells and proteins of pumpkin plants for the control of fruit size. J Biosci Bioeng 114:334–341

    Article  CAS  PubMed  Google Scholar 

  • Nerson H (2005) Effects of fruit shape and plant density on seed yield and quality of squash. Sci Hortic 105:293–304

    Article  Google Scholar 

  • Ohta M, Matsui K, Hiratsu K, Shinshi H, Ohme-Takagi M (2001) Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. Plant Cell 13:1959–1968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olmstead JW, Whiting MD, Iezzoni AF (2007) Genotypic differences in sweet cherry fruit size are primarily a function of cell number. J Am Soc Hortic Sci 132:697–703

    Google Scholar 

  • Pan Y, Liang X, Gao M, Liu H, Meng H, 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 

  • Perin C, Hagen L, Giovinazzo N, Besombes D, Dogimont C, Pitrat M (2002) Genetic control of fruit shape acts prior to anthesis in melon (Cucumis melo L.). Mol Genet Genom 266:933–941

    Article  CAS  Google Scholar 

  • Qi J, Liu X, Shen D, Miao H, Xie B, Li X, Zeng P, Wang S, Shang Y, Gu X, Du Y, Li Y, Lin T, Yuan J, Yang X, Chen J, Chen H, Xiong X, Huang K, Fei Z, Mao L, Tian L, Stadler T, Renner SS, Kamoun S, Lucas WJ, Zhang Z, Huang S (2013) A genomic variation map provides insights into the genetic basis of cucumber domestication and diversity. Nat Genet 45:1510–1515

    Article  CAS  PubMed  Google Scholar 

  • Qin YM, Zhu YX (2011) How cotton fibers elongate: a tale of linear cell-growth mode. Curr Opin Plant Biol 14:106–111

    Article  CAS  PubMed  Google Scholar 

  • Ramamurthy RK, Waters BM (2015) Identification of fruit quality and morphology QTLs in melon (Cucumis melo) using a population derived from flexuosus and cantalupensis botanical groups. Euphytica 204:163–177

    Article  Google Scholar 

  • Robinson RW, Decker-Walters DS (1997) Cucurbits. Crop Production Science in Horticulture Series. CAB International, NY, p 226p

    Google Scholar 

  • Rosati A, Caporalia S, Hammami S, Moreno-Alías I, Paolettia A, Rapaport H (2011) Differences in ovary size among olive (Olea europaea L.) cultivars are mainly related to cell number, not to cell size. Sci Hortic 130:185–190

    Article  Google Scholar 

  • Rubinstein M, Katzenellenbogen M, Eshed R, Rozen A, Katzir N, Colle M, Yang L, Grumet R, Weng Y, Sherman A, Ophir R (2015) Ultrahigh-density linkage map for cultivated cucumber (Cucumis sativus L.) using a single-nucleotide polymorphism genotyping array. PLoS One 10(4):e0124101. doi:10.1371/journal.pone.0124101

    Article  PubMed  PubMed Central  Google Scholar 

  • Shi YH, Zhu SW, Mao XZ, Feng JX, Qin YM, Zhang L, Cheng J, Wei LP, Wang ZY, Zhu YX (2006) Transcriptome profiling, molecular biological, and physiological studies reveal a major role for ethylene in cotton fiber cell elongation. Plant Cell 18:651–664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinnott EW (1936) A developmental analysis of inherited shape differences in cucurbit fruits. Am Nat 70:245–254

    Article  Google Scholar 

  • Steindler C, Matteucci A, Sessa G, Weimar T, Ohgishi M, Aoyama T, Morelli G, Ruberti I (1999) Shade avoidance responses are mediated by the ATHB-2 HD zip protein, a negative regulator of gene expression. Development 126:4235–4245

    CAS  PubMed  Google Scholar 

  • Switzenberg JA, Beaudry RM, Grumet R (2015) Effect of CRC:etr1-1 transgene expression on ethylene production, sex expression, fruit set and fruit ripening in transgenic melon (Cucumis melo L.). Transgenic Res 24:497–507

    Article  CAS  PubMed  Google Scholar 

  • Tanksley SD (2004) The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. Plant Cell 16:S181–S189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian J, Zeng B, Lou SP, Li XG, Wu B, Li J (2016) Cloning, localization and expression analysis of two fw2.2-like genes in small- and large-fruited pear species. J Integr Agric 15:282–294

    Article  CAS  Google Scholar 

  • van der Knaap E, Tanksley SD (2001) Identification and characterization of a novel locus controlling early fruit development in tomato. Theor Appl Genet 103:353–358

    Article  Google Scholar 

  • van der Knapp E, Chakrabarti M, Chu YH, Clevenger JP, Illa-Brenguer E, Huang ZJ, Keyhaninejad N, Mu Q, Sun L, Wang YP, Wu S (2014) What lies beyond the eye: the molecular mechanisms regulating tomato fruit weight and shape. Front Plant Sci 5:227. doi:10.3389/fpls.2014.00227&#x2002

  • Varga A, Bruinsma J (1990) Dependence of ovary growth on ovule development in Cucumis sativus. Physiol Plant 80:43–50

    Article  Google Scholar 

  • Wang SC, Chang Y, Guo JJ, Zeng QN, Ellis BE, Chen JG (2011) Arabidopsis OVATE family proteins, a novel transcriptional repressor family, controls multiple aspects of plant growth and development. PLoS One 6:e23896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wechter WP, Levi A, Harris KR, Davis AR, Fei Z, Katzir N, Giovannoni JJ, Salman-Minkov A, Hernandez A, Thimmapuram J, Tadmor Y, Portnoy V, Trebitsh T (2008) Gene expression in developing watermelon fruit. BMC Genom 9:275

    Article  Google Scholar 

  • Wei Q, Wang Y, Qin X, Zhang Y, Zhang Z, Wang J, Li J, Lou Q, Chen J (2014) A SNP-based saturated genetic map and QTL analysis of fruit-related traits in cucumber using specific-length amplified fragments (SLAF) sequencing. BMC Genom 15:1158. doi:10.1186/1471-2164-15-1158

    Article  Google Scholar 

  • Wei Q, Qin X, Wang Y, Fu W, Li J, Lou Q, Chen J (2016) QTL analysis for cucumber fruit length by QTL-seq. https://pag.confex.com/pag/xxiv/webprogram/Paper19058.html

  • Weng Y, Colle M, Wang Y, Yang L, Rubenstein 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 

  • Wu S, Clevenger JP, Sun L, Visa S, Kamiya Y, Jikumaru Y, Blakeslee J, van der Knapp E (2015) The control of tomato fruit elongation orchestrated by sun, ovate, and fs8.1 in a wild relative of tomato. Plant Sci 238:95–104

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi M, Haji T, Miyake M, Yaegaki H (2002) Varietal differences in cell division and enlargement periods during peach (Prunus persica Batsch) fruit development. J Japan Soc Hortic Sci 71:155–163

    Article  Google Scholar 

  • Yang XY, Wang Y, Jiang W, Liu XL, Zhang XM, Yu HJ, Huang SW, Liu GQ (2013) Characterization and expression profiling of cucumber kinesin genes during early fruit development: revealing the roles of kinesins in exponential cell production and enlargement in cucumber fruit. J Exp Bot 64:4541–4557

    Article  CAS  PubMed  PubMed Central  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 (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 

  • Zhao J, Liu M, Jiang L, Ding L, Yan SS, Zhang J, Dong Z, Ren H, Zhang X (2014) Cucumber SUPERMAN has conserved function in stamen and fruit development and a distinct role in floral patterning. PLoS One 9:e86192. doi:10.1371/journal.pone.0086192

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Chen S, Song Y, Huang Y, Zhou S, Liu X, Zhou D-X (2015) The interaction between rice ERF3 and WOX11 promotes crown root development by regulating gene expression involved in cytokinin signaling. Plant Cell 27:2469–2483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Sue Hammar for technical assistance, Linda Hanson (MSU) for microscope use for cell number analysis, and Drs. Corny Barry and Ryan Warner for the helpful reviews of the manuscript. This research was in part supported by the US–Israel Binational Agricultural Research and Development (BARD) fund (Grant Number IS-4341-10).

Author information

Authors and Affiliations

  1. Graduate Program in Plant Breeding, Genetics and Biotechnology, Plant and Soil Science Building, Michigan State University, 1066 Bogue Street, East Lansing, MI, 48824, USA

    Marivi Colle, Yunyan Kang & Rebecca Grumet

  2. Department of Horticulture, University of Wisconsin, Madison, WI, 53706, USA

    Yiqun Weng

  3. USDA-ARS Vegetable Crops Research Unit, Horticulture Department, University of Wisconsin, Madison, WI, 53706, USA

    Yiqun Weng

  4. College of Horticulture, South China Agricultural University, Guangzhou, China

    Yunyan Kang

  5. Department of Fruit Trees Sciences, Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon Lezion, Israel

    Ron Ophir & Amir Sherman

Authors
  1. Marivi Colle
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yiqun Weng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yunyan Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ron Ophir
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Amir Sherman
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rebecca Grumet
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rebecca Grumet.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 16 kb)

Supplementary material 2 (PPTX 18855 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Colle, M., Weng, Y., Kang, Y. et al. Variation in cucumber (Cucumis sativus L.) fruit size and shape results from multiple components acting pre-anthesis and post-pollination. Planta 246, 641–658 (2017). https://doi.org/10.1007/s00425-017-2721-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-017-2721-9

Keywords

Search

Navigation