, Volume 147, Issue 5–6, pp 391–400 | Cite as

Genome-wide identification, phylogenetic and expression analysis of the maize HECT E3 ubiquitin ligase genes

  • Yunfeng Li
  • Lihong Zhai
  • Jingsheng Fan
  • Jiaxin Ren
  • Wenrong Gong
  • Xin Wang
  • Jun HuangEmail author
Original Paper


HECT (homologous to the E6AP carboxyl terminus) ubiquitin ligase genes (E3s) are enzymes with diverse functions influencing plant growth, development, and responses to abiotic stresses. However, there is relatively little information available regarding the maize HECT E3 gene family. In the present study, 12 maize HECT E3 genes (ZmUPL1 to ZmUPL12) were identified at the whole-genome level. The phylogenetic relationships, structures, and expression levels of the maize HECT E3 genes were then analyzed. On the basis of the constructed maximum likelihood phylogenetic tree, the HECT E3 genes were divided into six groups. The quantitative real-time polymerase chain reaction assay results revealed that all of the maize ZmUPL genes were expressed in most of the examined tissues and were responsive to three abiotic stresses. Considered together, the study results may provide a useful foundation for future investigations of maize stress-tolerance genes as well as functional analyses of the E3 enzymes in diverse agriculturally important crop species.


HECT E3 ubiquitin ligase Zea mays L. ZmUPL Gene expression 



This research was supported by the National Key Research and Development Program of China (2018YFD0100106), the Keypoint Research and Invention Program of Guangdong Province (2018B020202013), the Natural Science Foundation of Guangdong Province of China (2018A030313865).

Author contributions

J.H. and L.Z. designed and supervised the study. Y.L. and J.H. analyzed the data. Y.L. and J.F. performed the experiments. Y.L., W.G., L.Z. and J.H. prepared the manuscript. All authors read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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


  1. Bates PW, Vierstra RD (1999) UPL1 and 2, two 405 kDa ubiquitin-protein ligases from Arabidopsis thaliana related to the HECT-domain protein family. Plant J 20:183–195CrossRefGoogle Scholar
  2. Bernassola F, Karin M, Ciechanover A, Melino G (2008) The HECT family of E3 ubiquitin ligases: multiple players in cancer development. Cancer Cell 14:10–21CrossRefGoogle Scholar
  3. Brown P, Baxter L, Hickman R, Beynon J, Moore JD, Ott S (2013) MEME-LaB: motif analysis in clusters. Bioinformatics 29:1696–1697CrossRefGoogle Scholar
  4. Chauhan H, Khurana N, Agarwal P, Khurana JP, Khurana P (2013) A seed preferential heat shock transcription factor from wheat provides abiotic stress tolerance and yield enhancement in transgenic arabidopsis under heat stress environment. PLoS ONE 8:e79577CrossRefGoogle Scholar
  5. Chettoor AM, Givan SA, Cole RA, Coker CT, Unger-Wallace E, Vejlupkova Z, Vollbrecht E, Fowler JE, Evans MM (2014) Discovery of novel transcripts and gametophytic functions via RNA-seq analysis of maize gametophytic transcriptomes. Genome Biol 15:414CrossRefGoogle Scholar
  6. Cui F, Liu L, Zhao Q, Zhang Z, Li Q, Lin B, Wu Y, Tang S, Xie Q (2012) Arabidopsis ubiquitin conjugase UBC32 is an ERAD component that functions in brassinosteroid-mediated salt stress tolerance. Plant Cell 24:233–244CrossRefGoogle Scholar
  7. Dielen AS, Badaoui S, Candresse T, German-Retana S (2010) The ubiquitin/26S proteasome system in plant-pathogen interactions: a never-ending hide-and-seek game. Mol Plant Pathol 11:293–308CrossRefGoogle Scholar
  8. Downes BP, Stupar RM, Gingerich DJ, Vierstra RD (2003) The HECT ubiquitin-protein ligase (UPL) family in Arabidopsis: UPL3 has a specific role in trichome development. Plant J 35:729–742CrossRefGoogle Scholar
  9. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797CrossRefGoogle Scholar
  10. Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31:3784–3788CrossRefGoogle Scholar
  11. Henderson JM, Nisperos SV, Weeks J, Ghulam M, Marín I, Zayas RM (2015) Identification of HECT E3 ubiquitin ligase family genes involved in stem cell regulation and regeneration in planarians. Dev Biol 404:21–34CrossRefGoogle Scholar
  12. Hershko A (2005) The ubiquitin system for protein degradation and some of its roles in the control of the cell division cycle (Nobel lecture). Angew Chem Int Ed Engl 44:5932–5943CrossRefGoogle Scholar
  13. Huibregtse JM, Scheffner M, Beaudenon S, Howley PM (1995) A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc Natl Acad Sci USA 92:5249aCrossRefGoogle Scholar
  14. Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong SY, Lopez R, Hunter S (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240CrossRefGoogle Scholar
  15. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  16. Letunic I, Bork P (2019) Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 47:W256–W259CrossRefGoogle Scholar
  17. Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40:D302–D305CrossRefGoogle Scholar
  18. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (− Delta Delta C (T)) method. Methods 25:402–408CrossRefGoogle Scholar
  19. Marin I (2010) Animal HECT ubiquitin ligases: evolution and functional implications. BMC Evol Biol 10:56CrossRefGoogle Scholar
  20. Marin I (2013) Evolution of plant HECT ubiquitin ligases. PLoS ONE 8:e68536CrossRefGoogle Scholar
  21. Meng XW, Wang C, Rahman SU, Wang YX, Wang AL, Tao SH (2015) Genome-wide identification and evolution of HECT genes in soybean. Int J Mol Sci 16:8517–8535CrossRefGoogle Scholar
  22. Metzger MB, Hristova VA, Weissman AM (2012) HECT and RING finger families of E3 ubiquitin ligases at a glance. J Cell Sci 125:531–537CrossRefGoogle Scholar
  23. Moon J, Parry G, Estelle M (2004) The ubiquitin-proteasome pathway and plant development. Plant Cell 16:3181–3195CrossRefGoogle Scholar
  24. Morreale FE, Walden H (2016) Types of ubiquitin ligases. Cell 165:248CrossRefGoogle Scholar
  25. Mukhopadhyay D, Riezman H (2007) Proteasome-Independent functions of ubiquitin in endocytosis and signaling. Science 315:201–205CrossRefGoogle Scholar
  26. Pallant J (2013) SPSS survival manual: a step by step guide to data analysis using SPSS for Windows (version 12). Aust N Z J Public Health 37:597–598Google Scholar
  27. Pickart CM (2001) Mechanisms underlying ubiquitination. Annu Rev Biochem 70:503–533CrossRefGoogle Scholar
  28. Qiu SY (2016) Expression and functional analysis of the HECT-Type Ubiquitin-protein Ligases (UPL) gene family in Arabidopsis. Dissertation, Fujian Agriculture and Forestry University (in Chinese)Google Scholar
  29. Refy AE, Perazza D, Zekraoui L, Valay JG, Bechtold N, Brown S, Hülskamp M, Herzog M, Bonneville JM (2003) The Arabidopsis KAKTUS gene encodes a HECT protein and controls the number of endoreduplication cycles. Mol Genet Genom 270:403–414CrossRefGoogle Scholar
  30. Rotin D, Kumar S (2009) Physiological functions of the HECT family of ubiquitin ligases. Nat Rev Mol Cell Bio 10:398–409CrossRefGoogle Scholar
  31. Sadanandom A, Bailey M, Ewan R, Lee J, Nelis S (2012) The ubiquitin-proteasome system: central modifier of plant signalling. New Phytol 196:13–28CrossRefGoogle Scholar
  32. Santner A, Estelle M (2010) The ubiquitin-proteasome system regulates plant hormone signaling. Plant J 61:1029–1040CrossRefGoogle Scholar
  33. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, Chen W, Yan L, Higginbotham J, Cardenas M, Waligorski J, Applebaum E, Phelps L, Falcone J, Kanchi K, Thane T, Scimone A, Thane N, Henke J, Wang T, Ruppert J, Shah N, Rotter K, Hodges J, Ingenthron E, Cordes M, Kohlberg S, Sgro J, Delgado B, Mead K, Chinwalla A, Leonard S, Crouse K, Collura K, Kudrna D, Currie J, He R, Angelova A, Rajasekar S, Mueller T, Lomeli R, Scara G, Ko A, Delaney K, Wissotski M, Lopez G, Campos D, Braidotti M, Ashley E, Golser W, Kim H, Lee S, Lin J, Dujmic Z, Kim W, Talag J, Zuccolo A, Fan C, Sebastian A, Kramer M, Spiegel L, Nascimento L, Zutavern T, Miller B, Ambroise C, Muller S, Spooner W, Narechania A, Ren L, Wei S, Kumari S, Faga B, Levy MJ, McMahan L, Van Buren P, Vaughn MW, Ying K, Yeh CT, Emrich SJ, Jia Y, Kalyanaraman A, Hsia AP, Barbazuk WB, Baucom RS, Brutnell TP, Carpita NC, Chaparro C, Chia JM, Deragon JM, Estill JC, Fu Y, Jeddeloh JA, Han Y, Lee H, Li P, Lisch DR, Liu S, Liu Z, Nagel DH, McCann MC, SanMiguel P, Myers AM, Nettleton D, Nguyen J, Penning BW, Ponnala L, Schneider KL, Schwartz DC, Sharma A, Soderlund C, Springer NM, Sun Q, Wang H, Waterman M, Westerman R, Wolfgruber TK, Yang L, Yu Y, Zhang L, Zhou S, Zhu Q, Bennetzen JL, Dawe RK, Jiang J, Jiang N, Presting GG, Wessler SR, Aluru S, Martienssen RA, Clifton SW, McCombie WR, Wing RA, Wilson RK (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115CrossRefGoogle Scholar
  34. Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Plant Biol 55:555–590CrossRefGoogle Scholar
  35. Vierstra RD (1996) Proteolysis in plants: mechanisms and functions. Plant Mol Biol 32:275–302CrossRefGoogle Scholar
  36. Welchman RL, Gordon C, Mayer RJ (2005) Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nat Rev Mol Cell Biol 6:599–609CrossRefGoogle Scholar
  37. Xu L, Ménard R, Berr A, Fuchs J, Cognat V, Meyer D, Shen WH (2009) The E2 ubiquitin-conjugating enzymes, AtUBC1 and AtUBC2, play redundant roles and are involved in activation of FLC expression and repression of flowering in Arabidopsis thaliana. Plant J 57:279–288CrossRefGoogle Scholar
  38. Xu J, Xing S, Cui H, Chen X, Wang X (2016) Genome-wide identification and characterization of the apple (Malus domestica) HECT ubiquitin-protein ligase family and expression analysis of their responsiveness to abiotic stresses. Mol Genet Genomics 291:635–646CrossRefGoogle Scholar
  39. Yoshida Y, Tokunaga F, Chiba T, Iwai K, Tanaka K, Tai T (2003) Fbs2 is a new member of the E3 ubiquitin ligase family that recognizes sugar Chains. J Biol Chem 278:43877–43884CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Guangdong Provincial Key Laboratory of Plant Molecular BreedingSouth China Agricultural UniversityGuangzhouChina
  2. 2.Medical CollegeHubei University of Arts and ScienceXiangyangChina
  3. 3.College of AgricultureSouth China Agricultural UniversityGuangzhouChina

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