, Volume 237, Issue 3, pp 681–691 | Cite as

Expression of CsSEF1 gene encoding putative CCCH zinc finger protein is induced by defoliation and prolonged darkness in cucumber fruit

Original Article


To find a marker gene for photoassimilate limitation in cucumber fruit, genes induced in young fruit by total defoliation were cloned using the subtraction method. Almost every clone matched perfectly to a member of cucumber unigene ver. 3 of the Cucurbit Genomics Database. From the clones obtained, six genes were selected and the effect of defoliation on their expression was analyzed. In particular, expression of a gene that is highly homologous to the cucumber gene CsSEF1 (CAI30889) encoding putative CCCH zinc finger protein, which is reported to be induced at somatic embryogenesis in suspension culture, was enhanced by the treatment by about 50 times. The sequencing of the full-length cDNA and BLAST search in the Cucurbit Genomics Database indicated that our cloned gene is identical to CsSEF1. In control fruit, the expression of CsSEF1 did not change markedly in terms of development. By contrast, the expression of CsSEF1 was enhanced by prolonged darkness at the transcript level. This increase in the expression of CsSEF1 was temporally correlated with the decline in the fruit respiration rate. In mature leaves under prolonged darkness, enhanced expression was observed in the asparagine synthetase gene, but not in CsSEF1. These results suggest that the asparagine synthetase gene can be a good marker for sugar starvation and that CsSEF1 might be involved in the signal transduction pathway from photoassimilate limitation to growth cessation in cucumber fruit.


CsSEF1 Cucumber Fruit growth Photoassimilate Respiration Tandem CCCH zinc finger 





Days after anthesis


Gibberellic acid


Quantitative reverse transcriptase–polymerase chain reaction


Rapid amplification of cDNA ends


Tandem CCCH zinc finger


Untranslated region



We thank Dr. Yoshiteru Sakata of the Institute of Vegetable and Tea Science, National Agriculture and Food Research Organization, for kindly offering the seeds of the cucumber cultivar ‘Tokiwa’. This work was supported by Grant-in-Aid for Scientific Research (C) (22580285) on Priority Areas from the Ministry of Education, Culture, Sports, Science and Technology of Japan to TA.


  1. Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signaling. Nature 448:938–942PubMedCrossRefGoogle Scholar
  2. Barreau C, Paillard L, Osborne HB (2005) AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res 33:7138–7150PubMedCrossRefGoogle Scholar
  3. Blackshear PJ, Phillips RS, Lai WS (2005) Tandem CCCH zinc finger proteins in mRNA binding. In: Luchi S, Kuldell N (eds) Zinc finger proteins: from atomic contact to cellular function. Kluwer Academic/Plenum Publishers, Austin, Texas, pp 80–90CrossRefGoogle Scholar
  4. Blasing OE, Gibson Y, Grunther M, Hohne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible W-R, Stitt M (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17:3257–3281PubMedCrossRefGoogle Scholar
  5. Carballo E, Lai WS, Blackshear PJ (1998) Feedback inhibition of macrophage tumor necrosis factor-∝ production by tristetrapolin. Science 281:1001–1005PubMedCrossRefGoogle Scholar
  6. Carrick DM, Lai WS, Blackshear PJ (2004) The tandem CCCH zinc finger protein tristetraprolin and its relevance to cytokine mRNA turnover and arthritis. Arthritis Res Ther 6:248–264PubMedCrossRefGoogle Scholar
  7. Chen M, Thelen JJ (2011) Plastid uridine salvage activity is required for photoassimilate allocation and partitioning in Arabidopsis. Plant Cell 23:2991–3006PubMedCrossRefGoogle Scholar
  8. Contento AL, Kim SJ, Bassham DC (2004) Transcriptome profiling of the response of Arabidopsis suspension culture cells to Suc starvation. Plant Physiol 135:2330–2347PubMedCrossRefGoogle Scholar
  9. Craft AS, Lorentz OA (1944) Fruit growth and food transport in cucurbits. Plant Physiol 19:131–138CrossRefGoogle Scholar
  10. De J, Lai WS, Thorn JM, Goldsworthy SM, Liu X, Blackwell TK, Blackshear PJ (1999) Identification of four CCCH zinc finger proteins in Xenopus, including a novel vertebrate protein with four zinc fingers and severely restricted expression. Gene 228:133–145PubMedCrossRefGoogle Scholar
  11. Delaney KJ, Xu R, Zhang J, Li QQ, Yun KY, Falcone DL, Hunt AG (2006) Calmodulin interacts with and regulates the RNA-binding activity of an Arabidopsis polyadenylation factor subunit. Plant Physiol 140:1507–1521PubMedCrossRefGoogle Scholar
  12. Frommer WB, Ninnemann O (1995) Heterologous expression of genes in bacterial, fungal, animal and plant cells. Annu Rev Plant Physiol Plant Mol Biol 46:419–444CrossRefGoogle Scholar
  13. Giaquinta RT (1983) Phloem loading of sucrose. Annu Rev Plant Physiol 34:347–387CrossRefGoogle Scholar
  14. Gifford RM, Evans LT (1981) Photosynthesis, carbon partitioning, and yield. Annu Rev Plant Physiol 32:485–509CrossRefGoogle Scholar
  15. Goldschmidt EF, Huber SC (1992) Regulation of photosynthesis by end-product accumulation in leaves of plants storeing starch, sucrose, and hexose sugars. Plant Physiol 99:1443–1448PubMedCrossRefGoogle Scholar
  16. Grabowska A, Winsniewska A, Tagashira N, Malepszy S, Filipecki M (2009) Characterization of CsSEF1 gene encoding putative CCCH-type zinc finger protein expressed during cucumber somatic embryogenesis. J Plant Physiol 166:310–323PubMedCrossRefGoogle Scholar
  17. Ho LC (1988) Metabolism and compartmentation of imported sugars in sink organs in relation to sink strength. Annu Rev Plant Physiol Plant Mol Biol 39:355–378CrossRefGoogle Scholar
  18. Ho LC, Grange RI, Picken AJ (1987) An analysis of the accumulation of water and dry matter in tomato fruit. Plant Cell Environ 10:157–162Google Scholar
  19. Hudson BP, Martinez-Yamout MA, Dyson HJ, Wright PE (2004) Recognition of the mRNA AU-rich element by the zinc finger domain of TIS11d. Nat Struct Mol Biol 11:257–264PubMedCrossRefGoogle Scholar
  20. Kato T, Oda H (1977) Studies on the control of physiological disorders in fruit vegetable crops under plastic films. VIII. On the occurrence of abnormal fruits in cucumber plants. (II) On the development of carrot type and bottle gourd type fruits, so-called sakibosori and shiributo fruits in Japan. (Japanese text with English abstract) Res Rep Kochi Univ 26 (Agric Sci):175–182Google Scholar
  21. Kong Z, Li M, Yang W, Xu W, Xue Y (2006) A novel nuclear-localized CCCH-type zinc finger protein, OsDOs, is involved in delaying leaf senescence in rice. Plant Physiol 141:1376–1388PubMedCrossRefGoogle Scholar
  22. Lai WS, Carballo E, Thorn JM, Kennington EA, Blackshear PJ (2000) Interactions of CCCH zinc finger proteins with mRNA. Binding of tristeraprolin-related zinc finger proteins to AU-rich elements and destabilization of mRNA. J Biol Chem 275:17827–17837PubMedCrossRefGoogle Scholar
  23. Lai WS, Kennington EA, Blackshear PJ (2003) Tristeraprolin and its family members can promote the cell-free deadenylation of AU-rich element-containing mRNA by poly(A) ribonuclease. Mol Cell Biol 23:3798–3812PubMedCrossRefGoogle Scholar
  24. Lai WS, Parker JS, Grissom SF, Stumpo DJ, Blackshear PC (2006) Novel mRNA targets for tristetraprolin (TTP) identified by global analysis of stabilized transcripts in TTP-deficient fibroblasts. Mol Cell Biol 26:9196–9208PubMedCrossRefGoogle Scholar
  25. Lalonde S, Wipf D, Frommer WB (2004) Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annu Rev Plant Biol 55:341–372PubMedCrossRefGoogle Scholar
  26. Lam HM, Hsieh MH, Coruzzi G (1998) Reciprocal regulation of distinct asparagine synthetase genes by light and metabolites in A. thaliana. Plant J 16:345–353PubMedCrossRefGoogle Scholar
  27. Lee S-J, Jung HJ, Kang H, Kim SY (2012) Arabidopsis zinc finger proteins AtC3H49/AtTZF3 and AtC3H20/AtTZF2 are involved in ABA and JA responses. Plant Cell Physiol 53:673–686PubMedCrossRefGoogle Scholar
  28. Li Z, Thomas TL (1998) PEI1, an embryo-specific zinc finger protein gene required for heart-stage embryo formation in Arabidopsis. Plant Cell 10:383–398PubMedGoogle Scholar
  29. Li J, Jia D, Chen X (2001) HUA1 a regulator of stamen and carpel identities in Arabidopsis, code for a nuclear RNA-binding protein. Plant Cell 13:2269–2281PubMedGoogle Scholar
  30. Lin P-C, Pomeranz MC, Jikumaru Y, Kang SG, Hah C, Fujioka S, Kamiya Y, Jang J-C (2011) The Arabidopsis tandem zinc finger protein AtTZF1 affects ABA- and GA-mediated growth, stress and gene expression responses. Plant J 65:253–268PubMedCrossRefGoogle Scholar
  31. Marcelis LFM, Heuvelink E, Baan Hofman-Eijer LR, Den Bakker J, Xue LB (2004) Flower and fruit abortion in sweet pepper in relation to source and sink strength. J Exp Bot 406:2261–2268CrossRefGoogle Scholar
  32. Mello CC, Schubert C, Draper B, Zhang W, Lobel R, Priess JR (1996) The PIE-1 protein and germline specification in C. elegans. Nature 382:710–712PubMedCrossRefGoogle Scholar
  33. Nie XF, Maclean KN, Kumar V, McKay IA, Bustin SA (1995) ERF-2, the human homologue of murine Tis11d early response gene. Gene 152:285–286PubMedCrossRefGoogle Scholar
  34. Nobel PS (2009) Physicochemical and environmental plant physiology. Academic Press, London, pp 439–505Google Scholar
  35. Nunes-Nesi A, Fernie AR, Stitt M (2010) Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol Plant 3:973–996PubMedCrossRefGoogle Scholar
  36. Pharr DM, Sox HN, Smart EL, Lower RL (1977) Identification and distribution of soluble saccharides in pickling cucumber plants and their fate in fermentation. J Amer Soc Hort Sci 102:406–409Google Scholar
  37. Pomeranz M, Hah C, Lin P-C, Kang SG, Finer JJ, Blackshear PJ, Jang J-C (2010) The Arabidopsis tandem zinc finger protein AtTZF1 traffics between nucleus and cythplasmic foci and binds both DNA and RNA. Plant Physiol 152:151–165PubMedCrossRefGoogle Scholar
  38. Pomeranz M, Finer J, Jang J-C (2011) Putative molecular mechanism underlying tandem CCCH zinc finger protein mediated plant growth, stress and gene expression responses. Plant Signal Behav 6:647–651PubMedCrossRefGoogle Scholar
  39. Price J, Laxmi A, St Martin SK, Jang JC (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16:2128–2150PubMedCrossRefGoogle Scholar
  40. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  41. Reed AJ, Singletary GW (1989) Roles of carbohydrate supply and phytohormones in maize kernel abortion. Plant Physiol 91:986–992PubMedCrossRefGoogle Scholar
  42. Rolland F, Baena-Gonzales E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709PubMedCrossRefGoogle Scholar
  43. Ruan Y-L, Jin Y, Yang Y-J, Li G-J, Boyer JS (2010) Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Mol Plant 3:942–955PubMedCrossRefGoogle Scholar
  44. Schmitz RJ, Hong L, Michaels S, Amasino RM (2005) FRIGIDA-ESSENTIAL 1 interacts genetically with FRIGIDA AND FRIGIDA-LIKE 1 to promote the winter-annual habit of A. thaliana. Development 132:5471–5478PubMedCrossRefGoogle Scholar
  45. Tamura K, Sanada Y, Tase K, Komatsu T, Yoshida M (2011) Pp6-FEH1 encodes an enzyme for degradation of highly polymerized levan and is transcriptionally induced by defoliation in timothy (Phleum pratense L.). J Exp Bot 62:3421–3431PubMedCrossRefGoogle Scholar
  46. Tazuke A, Sakiyama R (1991) Relationships between growth in volume and respiration of cucumber fruit attached on the vine. J Japan Soc Hort Sci 59:745–750Google Scholar
  47. Thompson MJ, Lai WS, Talor GA, Blackshear PJ (1996) Cloning and characterization of two yeast genes encoding members of the CCCH class zinc finger proteins: zinc finger-mediated impairment of cell growth. Gene 174:225–233PubMedCrossRefGoogle Scholar
  48. Thorne JH (1985) Phloem unloading of C and N assimilates in developing seeds. Annu Rev Plant Physiol 36:317–343CrossRefGoogle Scholar
  49. Thum KE, Shin MJ, Palenchar PM, Kouranov A, Coruzzi GM (2004) Genome-wide investigation of light and carbon signaling in Arabidopsis. Genome Biol 5:R10PubMedCrossRefGoogle Scholar
  50. Turgeon R, Wolf S (2009) Phloem transport: cellular pathways and molecular trafficking. Annu Rev Plant Biol 60:207–221PubMedCrossRefGoogle Scholar
  51. Wang D, Guo Y, Wu C, Yang G, Li Y, Zheng C (2008) Genome-wide analysis of CCCH zinc finger family in Arabidopsis and rice. BMC Genomics 9:44. doi: 10.1186/1471-2164-9-44 PubMedCrossRefGoogle Scholar
  52. Windt CW, Gerkema E, Van As H (2009) Most water in the tomato truss is imported through the xylem, not the phloem: a nuclear magnetic resonance flow imaging study. Plant Physiol 151:830–842PubMedCrossRefGoogle Scholar
  53. Wubs AM, Ma Y, Heuvelink E, Marcelis LFM (2009) Genetic differences in fruit-set patterns are determined by differences in fruit sink strength and a source : sink threshold for fruit set. Ann Bot 104:957–964PubMedCrossRefGoogle Scholar
  54. Zhou Y, Chan K, Wang TL, Hedley CL, Offler CE, Patrick JW (2009) Intracellular sucrose communicates metabolic demand to sucrose transporters in developing pea cotyledons. J Exp Bot 60:71–85PubMedCrossRefGoogle Scholar
  55. Zinselmeier C, Jeong B-R, Boyer JS (1999) Starch and the control of kernel number in maize at low water potentials. Plant Physiol 121:25–35PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.College of AgricultureIbaraki UniversityIbarakiJapan

Personalised recommendations