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Identification and Expression Analysis of D-type Cyclin Genes in Early Developing Fruit of Cucumber (Cucumis sativus L.)

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Abstract

Plant D-type cyclin genes (CYCDs) are important regulators of cell division. However, little is known on their participation during the early developmental stage of cucumber fruit. In this study, cucumber CYCD genes were identified and characterized. The expression levels of these genes during early fruit development were assessed from 0 to 8 days after anthesis (DAA). The results revealed the presence of 13 different CYCD genes, which were named according to identity percentages of the corresponding orthologs in Arabidopsis thaliana and poplar. The genomic organization of each subgroup CYCD was similar to their orthologs in A. thaliana and poplar. The expression levels of CsCYCD genes were analyzed in cucumber fruits under different treatments including natural parthenocarpic fruit, pollinated fruit, and N-(2-chloro-4-pyidyl)-N′-phenyurea (CPPU)-induced parthenocarpic fruit. The highest expression levels of most CsCYCDs genes were at four DAA in natural parthenocarpic and pollinated fruits. Interestingly, the expression patterns of 8 of 13 CsCYCD genes in natural parthenocarpic fruit were similar to those in pollinated fruit, but different from those in CPPU-induced parthenocarpic fruit. Collectively, the results of this study provide insights on the CYCDs involved in cucumber parthenocarpic fruit development.

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References

  • Ando K, Carr K, Grumet R (2012) Transcriptome analyses of early cucumber fruit growth identifies distinct gene modules associated with phases of development. BMC Genomics 13(1):518–534

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ben-Cheikh W, Perez-Botella J, Tadeo FR, Talon M, Primo-Millo E (1997) Pollination increases gibberellin levels in developing ovaries of seeded varieties of citrus. Plant Physiol 114(2):557–564

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bohner J, Bangerth F (1988) Effects of fruit set sequence and defoliation on cell number, cell size and phytomone levels of tomato fruits (Lycopersicon esculentum Mill.) with a truss. Plant Growth Regul 7:141–155

    CAS  Google Scholar 

  • Boniotti MB, Gutierrez C (2001) A cell-cycle-regulated kinase activity phosphorylates plant retinoblastoma protein and contains, in Arabidopsis, a CDKA/cyclin D complex. Plant J 28(3):341–350

    Article  CAS  PubMed  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):1–7

    Article  CAS  Google Scholar 

  • Boonstra J (2003) Progression through the G1-phase of the on-going cell cycle. J Cell Biochem 90(2):244–252

    Article  CAS  PubMed  Google Scholar 

  • Buendía-Monreal M, Rentería-Canett I, Guerrero-Andrade O, Bravo-Alberto CE, Martínez-Castilla LP, García E, Vázquez-Ramos JM (2011) The family of maize D-type cyclins: genomic organization, phylogeny and expression patterns. Physiol Plant 143(3):297–308

    Article  PubMed  Google Scholar 

  • Cockcroft CE, den Boer BGW, Healy JMS, Murray JAH (2000) Cyclin D control of growth rate in plants. Nature 405(6786):575–579

    Article  CAS  PubMed  Google Scholar 

  • Collins C, Dewitte W, Murray JAH (2012) D-type cyclins control cell division and developmental rate during Arabidopsis seed development. J Exp Bot 63(10):3571–3586

    Article  CAS  PubMed  Google Scholar 

  • De Veylder L, de Almeida Engler J, Burssens S, Manevski A, Lescure B, Van Montagu M, Engler G, Inzé D (1999) A new D-type cyclin of Arabidopsis thaliana expressed during lateral root primordia formation. Planta 208(4):453–462

    Article  PubMed  Google Scholar 

  • Dewitte W, Riou-Khamlichi C, Scofield S, Healy JMS, Jacqmard A, Kilby NJ, Murray JAH (2003) Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell 15(1):79–92

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dewitte W, Scofield S, Alcasabas AA, Maughan SC, Menges M, Braun N, Collins C, Nieuwland J, Prinsen E, Sundaresan V (2007) Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proc Nati Acad Sci USA 104(36):14537–14542

    Article  CAS  Google Scholar 

  • Ewen ME, Sluss HK, Sherr CJ, Matsushime H, Kato J, Livingston DM (1993) Functional interactions of the retinoblastoma protein with mammalian D-type cyclins. Cell 73(3):487

    Article  CAS  PubMed  Google Scholar 

  • Feng C, Chen M, Xu C, Bai L, Yin X, Li X, Allan AC, Ferguson IB, Chen K (2012) Transcriptomic analysis of Chinese bayberry (Myrica rubra) fruit development and ripening using RNA-Seq. BMC Genomics 13(1):19–34

    Article  CAS  PubMed Central  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 59(9):2299–2308

    Article  CAS  PubMed  Google Scholar 

  • Fu F, Mao W, Shi K, Zhou Y, Yu J (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(1):98–107

    Article  CAS  PubMed  Google Scholar 

  • Gillaspy G, Ben-David H, Gruissem W (1993) Fruits: a developmental perspective. Plant Cell 5(10):1439–1451

    PubMed Central  PubMed  Google Scholar 

  • Guo A-Y, Zhu Q-H, Chen X, Luo J-C (2007) GSDS: a gene structure display server. Yi Chuan 29(8):1023–1026

    Article  CAS  PubMed  Google Scholar 

  • Hu Y, Bao F, Li J (2008) Promotive effect of brassinosteroids on cell division involves a distinct CycD3-induction pathway in Arabidopsis. Plant J 24(5):693–701

    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. Nat Genet 41(12):1275–1281

    Article  CAS  PubMed  Google Scholar 

  • Huntley R, Healy S, Freeman D, Lavender P, de Jager S, Greenwood J, Makker J, Walker E, Jackman M, Xie Q (1998) The maize retinoblastoma protein homologue ZmRb-1 is regulated during leaf development and displays conserved interactions with G1/S regulators and plant cyclin D (CycD) proteins. Plant Mol Biol 37(1):155–169

    Article  CAS  PubMed  Google Scholar 

  • Kim IS, Okubo H, Fujieda K (1992) Endogenous levels of IAA in relation to parthenocarpy in cucumber (Cucumis sativus L.). Sci Hortic 52(1–2):1–8

    Article  CAS  Google Scholar 

  • Kono A, Umeda-Hara C, Adachi S, Nagata N, Konomi M, Nakagawa T, Uchimiya H, Umeda M (2007) The Arabidopsis D-type cyclin CYCD4 controls cell division in the stomatal lineage of the hypocotyl epidermis. Plant Cell 19(4):1265–1277

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Koroleva OA, Tomlinson M, Parinyapong P, Sakvarelidze L, Leader D, Shaw P, Doonan JH (2004) CycD1, a putative G1 cyclin from Antirrhinum majus, accelerates the cell cycle in cultured tobacco BY-2 cells by enhancing both G1/S entry and progression through S and G2 phases. Plant Cell 16(9):2364–2379

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kvarnheden A, Yao JL, Zhan X, O'Brien I, Morris BA (2000) Isolation of three distinct CycD3 genes expressed during fruit development in tomato. J Exp Bot 51(352):1789–1797

    Article  CAS  PubMed  Google Scholar 

  • Lewis DH, Burge GK, Hopping ME, Jameson PE (2006) Cytokinins and fruit development in the kiwifruit (Actinidia deliciosa). II. Effects of reduced pollination and CPPU application. Physiol Plant 98(1):187–195

    Article  Google Scholar 

  • Li Y, Yu JQ, Ye QJ, Zhu ZJ, Guo ZJ (2003) Expression of CycD3 is transiently increased by pollination and N-(2-chloro-4-pyridyl)-N′-phenylurea in ovaries of Lagenaria leucantha. J Exp Bot 54(385):1245–1251

    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(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • Meijer M, Murray JAH (2001) Cell cycle controls and the development of plant form. Curr Opin Plant Biol 4(1):44–49

    Article  CAS  PubMed  Google Scholar 

  • Menges M, Pavesi G, Morandini P, Bögre L, Murray JAH (2007) Genomic organization and evolutionary conservation of plant D-type cyclins. Plant Physiol 145(4):1558–1576

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Morgan DO (1997) Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu Rev Cell Dev Biol 13(1):261–291

    Article  CAS  PubMed  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5(7):621–628

    Article  CAS  PubMed  Google Scholar 

  • Nakagami H, Kawamura K, Sugisaka K, Sekine M, Shinmyo A (2002) Phosphorylation of retinoblastoma-related protein by the cyclin D/cyclin-dependent kinase complex is activated at the G1/S-phase transition in tobacco. Plant Cell 14(8):1847–1857

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nugent J, Alfa CE, Young T, Hyams JS (1991) Conserved structural motifs in cyclins identified by sequence analysis. J Cell Sci 99(3):669–674

    CAS  PubMed  Google Scholar 

  • Riou-Khamlichi C, Huntley R, Jacqmard A, Murray JAH (1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283(5407):1541–1544

    Article  CAS  PubMed  Google Scholar 

  • Sjut V, Bangerth F (2006) Effect of pollination or treatment with growth regulators on levels of extractable hormones in tomato ovaries and young fruits. Physiol Plant 53(1):76–78

    Article  Google Scholar 

  • Soni R, Carmichael JP, Shah ZH, Murray J (1995) A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell 7(1):85–103

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sorrell DA, Combettes B, Chaubet-Gigot N, Gigot C, Murray JAH (1999) Distinct cyclin D genes show mitotic accumulation or constant levels of transcripts in tobacco bright yellow-2 cells. Plant Physiol 119(1):343–352

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Takeno K, Ise H, Minowa H, Dounowaki T (1992) Fruit growth induced by benzyladenine in Cucumis sativus L.: influence of benzyladenine on cell division, cell enlargement and indole-3-acetic acid content. J Jap Soc Hort Sci 60:915–920

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739

    Article  CAS  PubMed  Google Scholar 

  • Uemukai K, Iwakawa H, Kosugi S, de Uemukai S, Kato K, Kondorosi E, Murray JAH, Ito M, Shinmyo A, Sekine M (2005) Transcriptional activation of tobacco E2F is repressed by co-transfection with the retinoblastoma-related protein: cyclin D expression overcomes this repressor activity. Plant Mol Biol 57(1):83–100

    Article  CAS  PubMed  Google Scholar 

  • Vandepoele K, Raes J, De Veylder L, Rouzé P, Rombauts S, Inzé D (2002) Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14(4):903–916

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang G, Kong H, Sun Y, Zhang X, Zhang W, Altman N, Ma H (2004) Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins. Plant Physiol 135(2):1084–1099

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This study was supported by funds from the National Natural Science Foundation of China grant (The 973 Program: 2012CB3904), the Youth Science and Technology Innovation Fund program of Nanjing Agricultural University (No. KJ2012013), the Fundamental Research of Nanjing Agricultural University (Y0201100253) program, and the Ph.D. Program Foundation of Ministry of Education of China (20120097120037).

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Correspondence to Jinfeng Chen.

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Cui, L., Li, J., Zhang, T. et al. 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 (2014). https://doi.org/10.1007/s11105-013-0637-5

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