Genes & Genomics

, Volume 40, Issue 3, pp 233–241 | Cite as

Characterization and comparative expression analysis of CUL1 genes in rice

  • Sang-Hoon Kim
  • Og-Geum Woo
  • Hyunsoo Jang
  • Jae-Hoon Lee
Research Article


Cullin-RING E3 ubiquitin ligase (CRL) complex is known as the largest family of E3 ligases. The most widely characterized CRL, SCF complex (CRL1), utilizes CUL1 as a scaffold protein to assemble the complex components. To better understand CRL1-mediated cellular processes in rice, three CUL1 genes (OsCUL1s) were isolated in Oryza sativa. Although all OsCUL1 proteins exhibited high levels of amino acid similarities with each other, OsCUL1-3 had a somewhat distinct structure from OsCUL1-1 and OsCUL1-2. Basal expression levels of OsCUL1-3 were much lower than those of OsCUL1-1 and OsCUL1-2 in all selected samples, showing that OsCUL1-1 and OsCUL1-2 play predominant roles relative to OsCUL1-3 in rice. OsCUL1-1 and OsCUL1-2 genes were commonly upregulated in dry seeds and by ABA and salt/drought stresses, implying their involvement in ABA-mediated processes. These genes also showed similar expression patterns in response to various hormones and abiotic stresses, alluding to their functional redundancy. Expression of the OsCUL1-3 gene was also induced in dry seeds and by ABA-related salt and drought stresses, implying their participation in ABA responses. However, its expression pattern in response to hormones and abiotic stresses was somehow different from those of the OsCUL1-1 and OsCUL1-2 genes. Taken together, these findings suggest that the biological role and function of OsCUL1-3 may be distinct from those of OsCUL1-1 and OsCUL1-2. The results of expression analysis of OsCUL1 genes in this study will serve as a useful platform to better understand overlapping and distinct roles of OsCUL1 proteins and CRL1-mediated cellular processes in rice plants.


OsCUL1 CRL Ubiquitination Hormones Abiotic stresses 



This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2016R1D1A1B03930213), by Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries (IPET) through Agri-Bio industry Technology Development Program funded by Ministry of Agriculture, Food and Rural Affairs (MAFRA) (115081-2), and by the Strategic Initiative for Microbiomes in Agriculture and Food, Ministry of Agriculture, Food and Rural Affairs, Republic of Korea (916007021HD040).

Compliance with ethical standards

Conflict of interest

Sang-Hoon Kim declares that he does not have conflict of interest. Og-Geum Woo declares that she does not have conflict of interest. Hyunsoo Jang declares that he does not have conflict of interest. Jae-Hoon Lee declares that he does not have conflict of interest.

Ethical approval

This article does not contain any studies with human subjects or animals performed by any of the authors.

Supplementary material

13258_2017_622_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 16 KB)


  1. Bandurska H, Niedziela J, Chadzinikolau T (2013) Separate and combined responses to water deficit and UV-B radiation. Plant Sci 213:98–105CrossRefPubMedGoogle Scholar
  2. Brummell DA, Harpster MH, Dunsmuir P (1999) Differential expression of expansin gene family members during growth and ripening of tomato fruit. Plant Mol Biol 39:161–169CrossRefPubMedGoogle Scholar
  3. Bulatov E, Ciulli A (2015) Targeting Cullin-ring E3 ubiquitin ligases for drug discovery: structure, assembly and small-molecule modulation. Biochem J 467:365–386CrossRefPubMedPubMedCentralGoogle Scholar
  4. Callis J (2014) The ubiquitination machinery of the ubiquitin system. Arabidopsis Book 12:e0174CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cascardo JC, Buzeli RA, Almeida RS, Otoni WC, Fontes EP (2001) Differential expression of the soybean BiP gene family. Plant Sci 160:273–281CrossRefPubMedGoogle Scholar
  6. Chen S, Hajirezaei M, Börnke F (2005) Differential expression of sucrose-phosphate synthase isoenzymes in tobacco reflects their functional specialization during dark-governed starch mobilization in source leaves. Plant Physiol 139:1163–1174CrossRefPubMedPubMedCentralGoogle Scholar
  7. Chen Y, Xu Y, Luo W, Li W, Chen N, Zhang D, Chong K (2013) The F-box protein OsFBK12 targets OsSAMS1 for degradation and affects pleiotropic phenotypes, including leaf senescence, in rice. Plant Physiol 163:1673–1685CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chen A, Chen X, Wang H, Liao D, Gu M, Qu H, Sun S, Xu G (2014) Genome-wide investigation and expression analysis suggest diverse roles and genetic redundancy of Pht1 family genes in response to Pi deficiency in tomato. BMC Plant Biol 14:61CrossRefPubMedPubMedCentralGoogle Scholar
  9. Feng S, Shen Y, Sullivan JA, Rubio V, Xiong Y, Sun TP, Deng XW (2004) Arabidopsis CAND1, an unmodified CUL1-interacting protein, is involved in multiple developmental pathways controlled by ubiquitin/proteasome-mediated protein degradation. Plant Cell 16:1870–1882CrossRefPubMedPubMedCentralGoogle Scholar
  10. Gilkerson J, Hu J, Brown J, Jones A, Sun TP, Callis J (2009) Isolation and characterization of cul1-7, a recessive allele of CULLIN1 that disrupts SCF function at the C terminus of CUL1 in Arabidopsis thaliana. Genetics 181:945–963CrossRefPubMedPubMedCentralGoogle Scholar
  11. Gingerich DJ, Hanada K, Shiu SH, Vierstra RD (2007) Large-scale, lineage-specific expansion of a bric-a-brac/tramtrack/broad complex ubiquitin-ligase gene family in rice. Plant Cell 19:2329–2348CrossRefPubMedPubMedCentralGoogle Scholar
  12. Goldenberg SJ, Cascio TC, Shumway SD, Garbutt KC, Liu J, Xiong Y, Zheng N (2004) Structure of the Cand1-Cul1-Roc1 complex reveals regulatory mechanisms for the assembly of the multisubunit cullin-dependent ubiquitin ligases. Cell 119:517–528CrossRefPubMedGoogle Scholar
  13. Gray WM, del Pozo JC, Walker L, Hobbie L, Risseeuw E, Banks T, Crosby WL, Yang M, Ma H, Estelle M (1999) Identification of an SCF ubiquitin–ligase complex required for auxin response in Arabidopsis thaliana. Genes Dev 13:1678–1691CrossRefPubMedPubMedCentralGoogle Scholar
  14. Han SH, Yoo SC, Lee BD, An G, Paek NC (2015) Rice FLAVIN-BINDING, KELCH REPEAT, F-BOX 1 (OsFKF1) promotes flowering independent of photoperiod. Plant Cell Environ 38:2527–2540CrossRefPubMedGoogle Scholar
  15. He Y, Wang C, Higgins J, Yu J, Zong J, Lu P, Zhang D, Liang W (2016) MEIOTIC F-BOX is essential for male meiotic DNA double strand break repair in rice. Plant Cell 28:1879–1893CrossRefPubMedPubMedCentralGoogle Scholar
  16. Hellmann H, Hobbie L, Chapman A, Dharmasiri S, Dharmasiri N, del Pozo C, Reinhardt D, Estelle M (2003) Arabidopsis AXR6 encodes CUL1 implicating SCF E3 ligases in auxin regulation of embryogenesis. EMBO J 22:3314–3325Google Scholar
  17. Hobbie L, McGovern M, Hurwitz LR, Pierro A, Liu NY, Bandyopadhyay A, Estelle M (2000) The axr6 mutants of Arabidopsis thaliana define a gene involved in auxin response and early development. Development 127:23–32Google Scholar
  18. Hotton SK, Callis J (2008) Regulation of cullin RING ligases. Annu Rev Plant Biol 59:467–489CrossRefPubMedGoogle Scholar
  19. Hua Z, Vierstra RD (2011) The cullin-RING ubiquitin-protein ligases. Annu Rev Plant Biol 62:299–334CrossRefPubMedGoogle Scholar
  20. Huang TT, D’Andrea AD (2006) Regulation of DNA repair by ubiquitylation. Nat Rev Mol Cell Biol 7:323–334CrossRefPubMedGoogle Scholar
  21. Kahloul S, HajSalah El, Beji I, Boulaflous A, Ferchichi A, Kong H, Mouzeyar S, Bouzidi MF (2013) Structural, expression and interaction analysis of rice SKP1-like genes. DNA Res 20:67–78CrossRefPubMedGoogle Scholar
  22. Kim HJ, Kieber JJ, Schaller GE (2013) The rice F-box protein KISS ME DEADLY2 functions as a negative regulator of cytokinin signalling. Plant Signal Behav 8:e26434CrossRefPubMedPubMedCentralGoogle Scholar
  23. Lee JH, Kim WT (2011) Regulation of abiotic stress signal transduction by E3 ubiquitin ligases in Arabidopsis. Mol Cells 31:201–208CrossRefPubMedPubMedCentralGoogle Scholar
  24. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406CrossRefPubMedPubMedCentralGoogle Scholar
  25. Liu Q, Ning Y, Zhang Y, Yu N, Zhao C, Zhan X, Wu W, Chen D, Wei X, Wang GL, Cheng S, Cao L (2017) OsCUL3a negatively regulates cell death and immunity by degrading OsNPR1 in rice. Plant Cell 29:345–359CrossRefPubMedPubMedCentralGoogle Scholar
  26. Metzger MB, Pruneda JN, Klevit RE, Weissman AM (2014) RING-type E3 ligases: master manipulators of E2 ubiquitin-conjugating enzymes and ubiquitination. Biochim Biophys Acta 1843:47–60CrossRefPubMedGoogle Scholar
  27. Moon J, Zhao Y, Dai X, Zhang W, Gray WM, Huq E, Estelle M (2007) A new CULLIN 1 mutant has altered responses to hormones and light in Arabidopsis. Plant Physiol 143:684–696CrossRefPubMedPubMedCentralGoogle Scholar
  28. Mukhopadhyay D, Riezman H (2007) Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315:201–205CrossRefPubMedGoogle Scholar
  29. Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (2014) The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Front Plant Sci 5:170CrossRefPubMedPubMedCentralGoogle Scholar
  30. Okamura M, Aoki N, Hirose T, Yonekura M, Ohto C, Ohsugi R (2011) Tissue specificity and diurnal change in gene expression of the sucrose phosphate synthase gene family in rice. Plant Sci 181:159–166CrossRefPubMedGoogle Scholar
  31. Olzman JA, Chin LS (2008) Parkin-mediated K63-linked polyubiquitination: a signal for targeting misfolded proteins to the aggresome autophagy pathway. Autophagy 4:85–87CrossRefGoogle Scholar
  32. Oñate-Sánchez L, Vicente-Carbajosa J (2008) DNA-free RNA isolation protocols for Arabidopsis thaliana, including seeds and siliques. BMC Res Notes 1:93CrossRefPubMedPubMedCentralGoogle Scholar
  33. Petroski MD, Deshaies RJ (2005) Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 6:9–20CrossRefPubMedGoogle Scholar
  34. Piisilä M, Keceli MA, Brader G, Jakobson L, Jõesaar I, Sipari N, Kollist H, Palva ET, Kariola T (2015) The F-box protein MAX2 contributes to resistance to bacterial phytopathogens in Arabidopsis thaliana. BMC Plant Biol 15:53CrossRefPubMedPubMedCentralGoogle Scholar
  35. Piper RC, Lehner P (2011) Endosomal transportation via ubiquitination. Trends Cell Biol 21:647–655CrossRefPubMedPubMedCentralGoogle Scholar
  36. Rajabbeigi E, Eichholz I, Beesk N, Ulrichs C, Kroh LW, Rohn S, Huyskens-Keil S (2013) Interaction of drought stress and UV-B radiation—impact on biomass production and flavonoid metabolism in lettuce (Lactuca sativa L.). J Appl Bot Food Qual 86:190–197Google Scholar
  37. Razem FA, Baron K, Hill RD (2006) Turning on gibberellin and abscisic acid signaling. Curr Opin Plant Biol 9:454–459CrossRefPubMedGoogle Scholar
  38. Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16:276–277CrossRefPubMedGoogle Scholar
  39. Risseeuw EP, Daskalchuk TE, Banks TW, Liu E, Cotelesage J, Hellmann H, Estelle M, Somers DE, Crosby WL (2003) Protein interaction analysis of SCF ubiquitin E3 ligase subunits from Arabidopsis. Plant J 34:753–767CrossRefPubMedGoogle Scholar
  40. Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006a) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309CrossRefPubMedPubMedCentralGoogle Scholar
  41. Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006b) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103:18822–18827CrossRefPubMedPubMedCentralGoogle Scholar
  42. Santner A, Estelle M (2010) The ubiquitin-proteasome system regulates plant hormone signaling. Plant J 61:1029–1040CrossRefPubMedPubMedCentralGoogle Scholar
  43. Sato Y, Takehisa H, Kamatsuki K, Minami H, Namiki N, Ikawa H, Ohyanagi H, Sugimoto K, Antonio BA, Nagamura Y (2013) RiceXPro version 3.0: expanding the informatics resource for rice transcriptome. Nucleic Acids Res 41:D1206-1213Google Scholar
  44. Shen WH, Parmentier Y, Hellmann H, Lechner E, Dong A, Masson J, Granier F, Lepiniec L, Estelle M, Genschik P (2002) Null mutation of AtCUL1 causes arrest in early embryogenesis in Arabidopsis. Mol Biol Cell 13:1916–1928Google Scholar
  45. Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 55:555–590CrossRefPubMedGoogle Scholar
  46. Song S, Dai X, Zhang WH (2012) A rice F-box gene, OsFbx352, is involved in glucose-delayed seed germination in rice. J Exp Bot 63:5559–5568CrossRefPubMedPubMedCentralGoogle Scholar
  47. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  48. Thomann A, Dieterle M, Genschik P (2005) Plant CULLIN-based E3s: phytohormones come first. FEBS Lett 579:3239–3245CrossRefPubMedGoogle Scholar
  49. Vierstra RD (2012) The expanding universe of ubiquitin and ubiquitin-like modifiers. Plant Physiol 160:2–14CrossRefPubMedPubMedCentralGoogle Scholar
  50. Wu JT, Lin HC, Hu YC, Chien CT (2005) Neddylation and deneddylation regulate Cul1 and Cul3 protein accumulation. Nat Cell Biol 7:1014–1020CrossRefPubMedGoogle Scholar
  51. Xu G, Ma H, Nei M, Kong H (2009) Evolution of F-box genes in plants: different modes of sequence divergence and their relationships with functional diversification. Proc Natl Acad Sci USA 106:835–840CrossRefPubMedPubMedCentralGoogle Scholar
  52. Xu C, Li M, Wu J, Guo H, Li Q, Zhang Y, Chai J, Li T, Xue Y (2013) Identification of a canonical SCFSLF complex involved in S-RNase-based self-incompatibility of Pyrus (Rosaceae). Plant Mol Biol 81:245–257CrossRefPubMedGoogle Scholar
  53. Yan YS, Chen XY, Yang K, Sun ZX, Fu YP, Zhang YM, Fang RX (2011) Overexpression of an F-box protein gene reduces abiotic stress tolerance and promotes root growth in rice. Mol Plant 4:190–197CrossRefPubMedGoogle Scholar
  54. Yu H, Wu J, Xu N, Peng M (2007) Roles of F-box proteins in plant hormone responses. Acta Biochim Biophys Sin 39:915–922CrossRefPubMedGoogle Scholar
  55. Zhang Y, Feng S, Chen F, Chen H, Wang J, McCall C, Xiong Y, Deng XW (2008) Arabidopsis DDB1-CUL4 ASSOCIATED FACTOR1 forms a nuclear E3 ubiquitin ligase with DDB1 and CUL4 that is involved in multiple plant developmental processes. Plant Cell 20:1437–1455CrossRefPubMedPubMedCentralGoogle Scholar
  56. Zheng J, Yang X, Harrell JM, Ryzhikov S, Shim EH, Lykke-Andersen K, Wei N, Sun H, Kobayashi R, Zhang H (2002) CAND1 binds to unneddylated CUL1 and regulates the formation of SCF ubiquitin E3 ligase complex. Mol Cell 10:1519–1526CrossRefPubMedGoogle Scholar
  57. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273Google Scholar

Copyright information

© The Genetics Society of Korea and Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.Department of Biology EducationPusan National UniversityBusanRepublic of Korea
  2. 2.Department of Integrated Biological SciencePusan National UniversityBusanRepublic of Korea

Personalised recommendations