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Novel loci fsd6.1 and Csgl3 regulate ultra-high fruit spine density in cucumber

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Quantitative Trait Loci (QTL) analysis of multiple populations in multiple environments revealed that the fsd6.2 locus, which includes the candidate gene Csgl3, controls high fruit spine density in natural cucumbers. GWAS identified a novel locus fsd6.1, which regulates ultra-high fruit spine density in combination with Csgl3, and evolved during cucumber domestication.

Abstract

Fruit spine density, a domestication trait, largely influences the commercial value of cucumbers. However, the molecular basis of fruit spine density in cucumber remains unclear. In this study, four populations were derived from five materials, which included three with low fruit spine density, one with high fruit spine density, and one with ultra-high fruit spine density. Fruit spine densities were measured in 15 environments over a span of 6 years. The distributions were bimodal suggesting that fruit spine density is controlled by a major-effect QTL. QTL analysis determined that the same major-effect QTL, fsd6.2, is present in four populations. Fine map** indicated that Csgl3 is the candidate gene at the fsd6.2 locus. Phylogenetic and geographical distribution analyses revealed that Csgl3 originated from China, which has the highest genetic diversity for fruit spine density. One novel minor-effect QTL, fsd6.1, was detected in the HR and HP populations derived from the cross between 65G and 02245. In addition, GWAS identified a novel locus that colocates with fsd6.1. Inspection of a candidate region of about 18 kb in size using pairwise LD correlations, combined with genetic diversity and phylogenetic analysis of fsd6.1 in natural populations, indicated that Csa6G421750 is the candidate gene responsible for ultra-high fruit spine density in cucumber. This study provides new insights into the origin of fruit spine density and the evolution of high/ultra-high fruit spine density during cucumber domestication.

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References

  • Bloomer RH, Lloyd AM, Symonds VV (2014) The genetic architecture of constitutive and induced trichome density in two new recombinant inbred line populations of Arabidopsis thaliana: phenotypic plasticity, epistasis, and bidirectional leaf damage response. BMC Plant Biol 14:220–222

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bo KL, Wang H, Pan YP, Behera TK, Pandey S, Wen CL, Wang YH, Simon PW, Li YH, Chen JF, Weng Y (2016) SHORT HYPOCOTYL1 encodes a SMARCA3-Like chromatin remodeling factor regulating elongation. Plant Physiol 172:1273–1292

    CAS  PubMed  PubMed Central  Google Scholar 

  • Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL map** in experimental crosses. Bioinformatics 19:889–890

    Article  CAS  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • Chen C, Liu M, Jiang L, Liu X, Zhao J, Yan S (2014) Transcriptome profiling reveals roles of meristem regulators and polarity genes during fruit trichome development in cucumber (Cucumis sativus L.). J Exp Bot 65:4943–4958

    Article  CAS  Google Scholar 

  • Chen CH, Yin S, Liu XW et al (2016) The WD-repeat protein CsTTG1 regulates fruit wart formation through interaction with the Homeodomain–Leucine Zipper I protein Mict1. Plant Physiol 171:1156–1168

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cui JY, Miao H, Ding LH et al (2016) A new glabrous gene (csgl3) identified in trichome development in cucumber (Cucumis sativus L.). PLoS ONE 11:e0148422

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Gan Y, Kumimoto R, Liu C, Ratcliffe O, Yu H, Broun P (2006) GLABROUS INFLORESCENCE STEMS modulates the regulation by gibberellins of epidermal differentiation and shoot maturation in Arabidopsis. Plant Cell 18:1383–1395

    Article  CAS  Google Scholar 

  • Gan Y, Liu C, Yu H, Broun P (2007) Integration of cytokinin and gibberellin signaling by Arabidopsis transcription factors GIS, ZFP8 and GIS2 in the regulation of epidermal cell fate. Development 134:2073–2081

    Article  CAS  Google Scholar 

  • Grebe M (2012) The patterning of epidermal hairs in Arabidopsis—updated. Curr Opin Plant Biol 15:31–37

    Article  CAS  Google Scholar 

  • Guan Y (2008) Map** and cloning of related gene for fruit spines formation in cucumber. Ph.D. Thesis. Shanghai Jiao Tong University (in Chinese)

  • Hülskamp M (2004) Plant trichomes: a model for cell differentiation. Nat Rev Mol Cell Biol 5:471–480

    Article  Google Scholar 

  • Hülskamp M, Schnittger A, Folkers U (1999) Pattern formation and cell differentiation: trichomes in Arabidopsis as a genetic model system. Int Rev Cytol 186:147–178

    Article  Google Scholar 

  • Kenneth JL, Thomas DS, 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  Google Scholar 

  • Li YH, Yang LM, Pathak M, Li DW, He XM, Weng Y (2011) Fine genetic map** of cp: a recessive gene for compact (dwarf) plant architecture in cucumber, Cucumis sativus L. Theor Appl Genet 123:973–983

    Article  Google Scholar 

  • Li YH, Wen CL, Weng YQ (2013) Fine map** 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

    Article  CAS  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 homeo domain leucine zipper I gene. J Exp Bot 66:2515–2526

    Article  CAS  Google Scholar 

  • Liu XW, Bartholomew E, Cai YL, Ren HZ (2016) Trichome-related mutants provide a new perspective on multicellular trichome initiation and development in cucumber (Cucumis sativus L.). Front. Plant Sci 7:1187

    Google Scholar 

  • Machado A, Wu Y, Yang Y, Llewellyn DJ, Dennis ES (2009) The MYB transcription factor GhMYB25 regulates early fibre and trichome development. Plant J 59:52–62

    Article  CAS  Google Scholar 

  • Miao H, Zhang SP, Wang XW, Zhang ZH, Li M, Mu SQ, Cheng ZC, Zhang RW, Huang SW, **e BY, Fang ZY, Zhang ZX, Weng Y, Gu XF (2011) A linkage map of cultivated cucumber (Cucumis sativus L.) with 248 microsatellite marker loci and seven genes for horticulturally important traits. Euphytica 172:167–176

    Article  Google Scholar 

  • Pan YP, Bo KL, Cheng ZH, Weng YQ (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 15:1–15

    Article  CAS  Google Scholar 

  • Pan YP, Qu SP, Bo KL, Gao ML, Haider KR, Weng YQ (2017) QTL map** of domestication and diversifying selection related traits in round-fruited semi-wild **shuangbanna cucumber (Cucumis sativus, L. var. xishuangbannanesis). Theor Appl Genet 130:1531–1548

    Article  CAS  Google Scholar 

  • Pattanaik S, Patra B, Singh SK, Yuan L (2014) An overview of the gene regulatory network controlling trichome development in the model plant, Arabidopsis. Front Plant Sci 5:259–266

    Article  Google Scholar 

  • Qi JJ, Liu X, Shen D et al (2013) A genomic variation map provides insights into the genetic basis of cucumber domestication and diversity. Nat Genet 45:1510–1515

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Schellmann S, Hülskamp M (2005) Epidermal differentiation: trichomes in Arabidopsis as a model system. Int J Dev Biol 49:579–584

    Article  Google Scholar 

  • Tian HN, Wang XL, Guo HG et al (2017) NTL8 regulates trichome formation in arabidopsis by directly activating R3 MYB genes TRY and TCL1. Plant Physiol 174:2363–2375

    Article  CAS  Google Scholar 

  • Turner SD (2014) qqman: an R package for visualizing GWAS results using QQ and Manhattan plots. bioRxiv, 005165. http://dx.doi.org/10.1101/005165

  • Vakalounakis DJ (1992) Heart leaf, a recessive leaf shape markers in cucumber: linkage with disease resistance and other traits. J Hered 83:217–220

    Article  Google Scholar 

  • Walters SA, Shetty NV, Wehner TC (2001) Segregation and linkage of several genes in cucumber. J Am Soc Hortic Sci 126:442–450

    CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • **, genetic diversity, and transcriptome profiling reveals that the auxin transporter gene ns plays an important role in cucumber fruit spine development. Theor Appl Genet. https://doi.org/10.1007/s00122-018-3074-x

    Article  PubMed  PubMed Central  Google Scholar 

  • Xue XY, Zhao B, Chao LM, Chen DY, Cui WR, Mao YB, Wang LJ, Chen XY (2014) Interaction between two timing microRNAs controls trichome distribution in Arabidopsis. PLoS Genet 10:e1004266

    Article  Google Scholar 

  • Yang CX, Li HX, Zhang JH, Luo ZD, Gong PJ, Zhang CJ, Li JH, Wang TT, Zhang YY, Lu YE, Ye ZB (2011) A regulatory gene induces trichome formation and embryo lethality in tomato. Proc Natl Acad Sci USA 108:11836–11841

    Article  CAS  Google Scholar 

  • Yang LM, Koo DH, Li Y, Zhang X, Luan F, Havey MJ, Jiang J, Weng Y (2012) Chromosome rearrangements during domestication of cucumber as revealed from high-density genetic map** and draft genome assembly. Plant J 71:895–906

    Article  CAS  Google Scholar 

  • Yang X, Zhang W, He H et al (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  Google Scholar 

  • Yang S, Cai YL, Liu XW, Dong MM, Zhang YQ, Chen SY et al (2018) Csmyb6-cstry module regulates fruit trichome initiation in cucumber. J Exp Bot 69:1887–1902

    Article  CAS  Google Scholar 

  • Yuan XJ, Pan JS, Cai R, Guan Y, Liu LZ, Zhang WW, Li Z, He LH, Zhang C, Si LT, Zhu LH (2008) Genetic map** 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 HY, Wang LN, Zheng SS et al (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  Google Scholar 

  • Zhang SP, Liu SL, Miao H et al (2016b) Molecular map** and candidate gene analysis for numerous spines on the fruit of cucumber. J Hered 107:471–477

    Article  CAS  Google Scholar 

  • Zhao JL, Pan JS, Guan Y, Zhang WW, Bie BB, Wang YL, He HL, Lian HL, Cai R (2015) Micro-trichome as a class I homeodomain-leucine zipper gene regulates multicellular trichome development in Cucumis sativus. J Integr Plant Biol 57:925–935

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Dr. Graham Collins, formerly of the University of Adelaide, South Australia, for English editing of the manuscript. We thank LetPub for its linguistic assistance during the preparation of this manuscript. This work was supported by the National Key Research and Development Program of China [2016YFD0101705], the Earmarked Fund for Modern Agro-industry Technology Research System [CARS-25], Science and Technology Innovation Program of the Chinese Academy of Agricultural Science (CAAS-ASTIP-IVFCAAS), the National Natural Science Foundation of China (31572146), and the Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, Ministry of Agriculture, China.

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KB performed the experiments, analyzed experimental data, and wrote the paper. HM helped analyze data and collected the data for LM2012S and LM2012F. MW collected the data for LM2013S and LM2013F. XX collected the data for YR2014F, YR2015S, and YR2015F. ZS collected the data for CG lines. QX and LS collected the data for HR2016S, HR2016F, HP2016S, and HP2016F. WW and SW collected the data for HR2017S, HR2017F, HP2017S, and HP2017F. SZ and XG provided valuable research design. All authors read and approved the final manuscript.

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Correspondence to Sheng** Zhang or **ngfang Gu.

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

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Communicated by Michael J. Havey.

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Bo, K., Miao, H., Wang, M. et al. Novel loci fsd6.1 and Csgl3 regulate ultra-high fruit spine density in cucumber. Theor Appl Genet 132, 27–40 (2019). https://doi.org/10.1007/s00122-018-3191-6

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  • DOI: https://doi.org/10.1007/s00122-018-3191-6

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