SpringerLink
Log in

Genome-Wide Identification, Characterization, and Expression Profiling of Eukaryotic-Specific UBP Family Genes in Brassica rapa

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Ubiquitin-specific protease (UBP) family is the largest group of deubiquitinates playing a key role in eukaryotes. Presently, we identified 41 UBP genes from Brassica rapa which were classified into three groups via phylogenetic analysis. Structural and motif analysis revealed that these genes have diverse exon–intron structures and share an equal number of conserved motifs within the same group. Cis-regulatory elements were identified for salicylic acid, abscisic acid, gibberellin, methyl jasmonate, auxin, low temperature, anaerobic, defense and stress, light, and drought. Furthermore, six br-miRNAs named br-miRN159a, br-miRN159b, br-miRN159c, br-miRN159d, br-miRN324a, and br-miRN324b were found targeting BrUBP13.1, BrUBP13.2, BrUBP12.1, BrUBP12.2, BrUBP12.3, and BrUBP17. BrUBP genes were highly expressed in stem, root, silique, flower, leaf, and callus tissues; however, leaf qRT-PCR results indicated that the genes expression was high under SA and drought stresses. Our findings provide the novel foundations for future genetic and physiological studies of BrUBPs in Brassica rapa.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Spain)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • An Z, Liu Y, Ou Y, Li J, Zhang B, Sun D, Sun Y, Tang W (2018) Regulation of the stability of RGF1 receptor by the ubiquitin-specific proteases UBP12/UBP13 is critical for root meristem maintenance. PNAS 115:1123–1128

    CAS  PubMed  PubMed Central  Google Scholar 

  • Atanassov BS, Koutelou E, Dent SY (2011) The role of deubiquitinating enzymes in chromatin regulation. FEBS Lett 585:2016–2023

    CAS  PubMed  Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    CAS  PubMed  Google Scholar 

  • Butler JE, Kadonaga JT (2002) The RNA polymerase II core promoter: a key component in the regulation of gene expression. Genes Dev 16:2583–2592

    CAS  PubMed  Google Scholar 

  • Cai X, Wang Z, Hou Y, Liu C, Hendy A, **ng J, Chen X-L (2020) Systematic characterization of the ubiquitin-specific proteases in Magnaporthe oryzae. Phytopathol Res 2:1–12

    CAS  Google Scholar 

  • Chen R, Zhang L, Zhong B, Tan B, Liu Y, Shu H-B (2010) The ubiquitin-specific protease 17 is involved in virus-triggered type I IFN signaling. Cell Res 20:802–811

    CAS  PubMed  Google Scholar 

  • Clague MJ, Coulson JM, Urbé S (2012) Cellular functions of the DUBs. J Cell Sci 125:277–286

    CAS  PubMed  Google Scholar 

  • Derkacheva M, Liu S, Figueiredo DD, Gentry M, Mozgova I, Nanni P, Tang M, Mannervik M, Köhler C, Hennig L (2016) H2A deubiquitinases UBP12/13 are part of the Arabidopsis polycomb group protein system. Nat Plants 2:1–10

    Google Scholar 

  • Dhandapani V, Ramchiary N, Paul P, Kim J, Choi SH, Lee J, Hur Y, Lim YP (2011) Identification of potential microRNAs and their targets in Brassica rapa L. Mol Cells 32:21–37

    CAS  PubMed  PubMed Central  Google Scholar 

  • Doelling JH, Yan N, Kurepa J, Walker J, Vierstra RD (2001) The ubiquitin-specific protease UBP14 is essential for early embryo development in Arabidopsis thaliana. Plant J 27:393–405

    CAS  PubMed  Google Scholar 

  • Dreher K, Callis J (2007) Ubiquitin, hormones and biotic stress in plants. Ann Bot 99:787–822

    CAS  PubMed  PubMed Central  Google Scholar 

  • Du L, Li N, Chen L, Xu Y, Li Y, Zhang Y, Li C, Li Y (2014) The ubiquitin receptor DA1 regulates seed and organ size by modulating the stability of the ubiquitin-specific protease UBP15/SOD2 in Arabidopsis. Plant Cell 26:665–677

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dykes IM, Emanueli C (2017) Transcriptional and post-transcriptional gene regulation by long non-coding RNA. Genom Proteom Bioinf 15:177–186

    Google Scholar 

  • El-Esawi MA (2015) Taxonomic relationships and biochemical genetic characterization of Brassica resources: Towards a recent platform for germplasm improvement and utilization. Annu Res Rev Biol 15:1–11

    Google Scholar 

  • El-Esawi MA (2017) Genetic diversity and evolution of Brassica genetic resources: from morphology to novel genomic technologies–a review. Plant Genet Res 15:388–399

    Google Scholar 

  • Ewan R, Pangestuti R, Thornber S, Craig A, Carr C, O’Donnell L, Zhang C, Sadanandom A (2011) Deubiquitinating enzymes AtUBP12 and AtUBP13 and their tobacco homologue NtUBP12 are negative regulators of plant immunity. New Phytol 191:92–106

    CAS  PubMed  Google Scholar 

  • Frappier L, Verrijzer CP (2011) Gene expression control by protein deubiquitinases. Curr Opin Genet Dev 21:207–213

    CAS  PubMed  Google Scholar 

  • Guerrero J, Regedanz E, Lu L, Ruan J, Bisaro DM, Sunter G (2020) Manipulation of the plant host by the Geminivirus AC2/C2 protein, a central player in the infection cycle. Front Plant Sci 591:135

    Google Scholar 

  • Gutierrez C, Chemmama IE, Mao H, Yu C, Echeverria I, Block SA, Rychnovsky SD, Zheng N, Sali A, Huang L (2020) Structural dynamics of the human COP9 signalosome revealed by cross-linking mass spectrometry and integrative modeling. PNAS 117:4088–4098

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harper JW, Schulman BA (2021) Cullin-RING ubiquitin ligase regulatory circuits: a quarter century beyond the F-box hypothesis. Annu Rev Biochem 90:403–429

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425–479

    CAS  PubMed  Google Scholar 

  • Huang SQ, **ang AL, Che LL, Chen S, Li H, Song JB, Yang ZM (2010) A set of miRNAs from Brassica napus in response to sulphate deficiency and cadmium stress. Plant Biotechnol J 8:887–899

    CAS  PubMed  Google Scholar 

  • Ishida M, Hara M, Fukino N, Kakizaki T, Morimitsu Y (2014) Glucosinolate metabolism, functionality and breeding for the improvement of Brassicaceae vegetables. Breed Sci 64:48–59

    CAS  PubMed  PubMed Central  Google Scholar 

  • Isono E, Nagel M-K (2014) Deubiquitylating enzymes and their emerging role in plant biology. Front Plant Sci 5:56

    PubMed  PubMed Central  Google Scholar 

  • Jang S-M, Redon CE, Aladjem MI (2018) Chromatin-bound cullin-ring ligases: regulatory roles in DNA replication and potential targeting for cancer therapy. Front Mol Biosci 5:19

    PubMed  PubMed Central  Google Scholar 

  • Jeong JS, Jung C, Seo JS, Kim J-K, Chua N-H (2017) The deubiquitinating enzymes UBP12 and UBP13 positively regulate MYC2 levels in jasmonate responses. Plant Cell 29:1406–1424

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kliza K, Husnjak K (2020) Resolving the complexity of ubiquitin networks. Front Mol Biosci 7:21

    CAS  PubMed  PubMed Central  Google Scholar 

  • Komatsu K, Hashimoto M, Ozeki J, Yamaji Y, Maejima K, Senshu H, Himeno M, Okano Y, Kagiwada S, Namba S (2010) Viral-induced systemic necrosis in plants involves both programmed cell death and the inhibition of viral multiplication, which are regulated by independent pathways. Mol Plant Microbe Interact 23:283–293

    CAS  PubMed  Google Scholar 

  • Kurilla A, Toth T, Dorgai L, Darula Z, Lakatos T, Silhavy D, Kerenyi Z, Dallmann G (2020) Nectar-and stigma exudate-specific expression of an acidic chitinase could partially protect certain apple cultivars against fire blight disease. Planta 251:1–16

    Google Scholar 

  • Li Y, Zheng L, Corke F, Smith C, Bevan MW (2008) Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes Dev 22:1331–1336

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu K, Yuan C, Feng S, Zhong S, Li H, Zhong J, Shen C, Liu J (2017) Genome-wide analysis and characterization of Aux/IAA family genes related to fruit ripening in papaya (Carica papaya L.). BMC Genom 18:1–11

    Google Scholar 

  • Liu W, Xu L, Wang Y, Shen H, Zhu X, Zhang K, Chen Y, Yu R, Limera C, Liu L (2015) Transcriptome-wide analysis of chromium-stress responsive microRNAs to explore miRNA-mediated regulatory networks in radish (Raphanus sativus L.). Sci Rep 5:1–17

    Google Scholar 

  • Liu Y, Schiff M, Serino G, Deng X-W, Dinesh-Kumar S (2002) Role of SCF ubiquitin-ligase and the COP9 signalosome in the N gene–mediated resistance response to Tobacco mosaic virus. Plant Cell 14:1483–1496

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Wang F, Zhang H, He H, Ma L, Deng XW (2008) Functional characterization of the Arabidopsis ubiquitin-specific protease gene family reveals specific role and redundancy of individual members in development. Plant J 55:844–856

    CAS  PubMed  Google Scholar 

  • March E, Farrona S (2018) Plant deubiquitinases and their role in the control of gene expression through modification of histones. Front Plant Sci 8:2274

    PubMed  PubMed Central  Google Scholar 

  • Moon YK, Hong J-P, Cho Y-C, Yang S-J, An G, Kim WT (2009) Structure and expression of OsUBP6, an ubiquitin-specific protease 6 homolog in rice (Oryza sativa L.). Mol Cells 28:463–472

    CAS  PubMed  Google Scholar 

  • Nassrallah A, Rougée M, Bourbousse C, Drevensek S, Fonseca S, Iniesto E, Ait-Mohamed O, Deton-Cabanillas A-F, Zabulon G, Ahmed I (2018) DET1-mediated degradation of a SAGA-like deubiquitination module controls H2Bub homeostasis. Elife 7:e37892

    PubMed  PubMed Central  Google Scholar 

  • Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP (2014) ABA control of plant macroelement membrane transport systems in response to water deficit and high salinity. New Phytol 202:35–49

    PubMed  Google Scholar 

  • Pan F, Wu M, Hu W, Liu R, Yan H, **ang Y (2019) Genome-wide identification and expression analyses of the bZIP transcription factor genes in moso bamboo (Phyllostachys edulis). Int J Mol Sci 20:2203

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pauli E-K, Chan YK, Davis ME, Gableske S, Wang MK, Feister KF, Gack MU (2014) The ubiquitin-specific protease USP15 promotes RIG-I: mediated antiviral signaling by deubiquitylating TRIM25. Sci Signal 7:3

    Google Scholar 

  • Peng J, Schwartz D, Elias JE, Thoreen CC, Cheng D, Marsischky G, Roelofs J, Finley D, Gygi SP (2003) A proteomics approach to understanding protein ubiquitination. Nat Biotechnol 21:921–926

    CAS  PubMed  Google Scholar 

  • Pickart CM (2004) Back to the future with ubiquitin. Cell 116:181–190

    CAS  PubMed  Google Scholar 

  • Pieterse CM, Van Loon L (2004) NPR1: the spider in the web of induced resistance signaling pathways. Curr Opin Plant Biol 7:456–464

    CAS  PubMed  Google Scholar 

  • Que Y, Xu Z, Wang C, Lv W, Yue X, Xu L, Tang S, Dai H, Wang Z (2020) The putative deubiquitinating enzyme MoUbp4 is required for infection-related morphogenesis and pathogenicity in the rice blast fungus Magnaporthe oryzae. Curr Genet 66:561–576

    CAS  PubMed  Google Scholar 

  • Ramachandran S, Ciulli A (2021) Building ubiquitination machineries: E3 ligase multi-subunit assembly and substrate targeting by PROTACs and molecular glues. Curr Opin Struct Biol 67:110–119

    CAS  PubMed  Google Scholar 

  • Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration-and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009

    CAS  PubMed  Google Scholar 

  • Shan T, Rong W, Xu H, Du L, Liu X, Zhang Z (2016) The wheat R2R3-MYB transcription factor TaRIM1 participates in resistance response against the pathogen Rhizoctonia cerealis infection through regulating defense genes. Sci Rep 6:1–14

    Google Scholar 

  • Tong C, Wang X, Yu J, Wu J, Li W, Huang J, Dong C, Hua W, Liu S (2013) Comprehensive analysis of RNA-seq data reveals the complexity of the transcriptome in Brassica rapa. BMC Genom 14:1–10

    Google Scholar 

  • Tuccoli A, Poliseno L, Rainaldi G (2006) miRNAs regulate miRNAs: coordinated transcriptional and post-transcriptional regulation. Cell Cycle 5:2473–2476

    CAS  PubMed  Google Scholar 

  • van den Burg HA, Tsitsigiannis DI, Rowland O, Lo J, Rallapalli G, MacLean D, Takken FL, Jones JD (2008) The F-box protein ACRE189/ACIF1 regulates cell death and defense responses activated during pathogen recognition in tobacco and tomato. Plant Cell 20:697–719

    PubMed  PubMed Central  Google Scholar 

  • Varshavsky A (1997) The ubiquitin system. Trends Biochem Sci 22:383–387

    CAS  PubMed  Google Scholar 

  • Vierstra RD (2009) The ubiquitin–26S proteasome system at the nexus of plant biology. Nat Rev Mol 10:385–397

    CAS  Google Scholar 

  • Wang D-H, Song W, Wei S-W, Zheng Y-F, Chen Z-S, Han J-D, Zhang H-T, Luo J-C, Qin Y-M, Xu Z-H (2018a) Characterization of the ubiquitin C-terminal hydrolase and ubiquitin-specific protease families in rice (Oryza sativa). Front Plant Sci 9:1636

    PubMed  PubMed Central  Google Scholar 

  • Wang F, Li L, Liu L, Li H, Zhang Y, Yao Y, Ni Z, Gao J (2012) High-throughput sequencing discovery of conserved and novel microRNAs in Chinese cabbage (Brassica rapa L. ssp. pekinensis). Mol Genet Genom 287:555–563

    CAS  Google Scholar 

  • Wang L, Zhao W, Zhang M, Wang P, Zhao K, Zhao X, Yang S, Gao C (2013) USP4 positively regulates RIG-I-mediated antiviral response through deubiquitination and stabilization of RIG-I. J Virol 87:4507–4515

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Zhang H, Liu C, **ng J, Chen X-L (2018b) A deubiquitinating enzyme Ubp14 is required for development, stress response, nutrient utilization, and pathogenesis of Magnaporthe oryzae. Front Microbiol 9:769

    PubMed  PubMed Central  Google Scholar 

  • Wei J-W, Huang K, Yang C, Kang C-S (2017) Non-coding RNAs as regulators in epigenetics. Oncol Rep 37:3–9

    PubMed  Google Scholar 

  • Wei N, Serino G, Deng X-W (2008) The COP9 signalosome: more than a protease. Trends in Biochem Sci 33:592–600

    CAS  Google Scholar 

  • Wilkinson KD (1997) Regulation of ubiquitin-dependent processes by deubiquitinating enzymes. FASEB J 11:1245–1256

    CAS  PubMed  Google Scholar 

  • Wilkinson KD (2000) Ubiquitination and deubiquitination: targeting of proteins for degradation by the proteasome. Semin Cell Dev Biol 25:141–148

    Google Scholar 

  • Winter J, Jung S, Keller S, Gregory RI, Diederichs S (2009) Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 11:228–234

    CAS  PubMed  Google Scholar 

  • Wu R, Shi Y, Zhang Q, Zheng W, Chen S, Du L, Lu C (2019) Genome-wide identification and characterization of the UBP gene family in moso bamboo (Phyllostachys edulis). Int J Mol Sci 20:4309

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Y, ** W, Li N, Zhang W, Liu C, Li C, Li Y (2016) UBIQUITIN-SPECIFIC PROTEASE14 interacts with ULTRAVIOLET-B INSENSITIVE4 to regulate endoreduplication and cell and organ growth in Arabidopsis. Plant Cell 28:1200–1214

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic-and cold-stress-responsive promoters. Trends Plant Sci 10:88–94

    CAS  PubMed  Google Scholar 

  • Yan N, Doelling JH, Falbel TG, Durski AM, Vierstra RD (2000) The ubiquitin-specific protease family from Arabidopsis. At UBP1 and 2 are required for the resistance to the amino acid analog canavanine. Plant Physiol 124:1828–1843

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yu X, Wang H, Lu Y, de Ruiter M, Cariaso M, Prins M, van Tunen A, He Y (2012) Identification of conserved and novel microRNAs that are responsive to heat stress in Brassica rapa. J Exp Bot 63:1025–1038

    CAS  PubMed  Google Scholar 

  • Yu Y, Guo D, Li G, Yang Y, Zhang G, Li S, Liang Z (2019) The grapevine R2R3-type MYB transcription factor VdMYB1 positively regulates defense responses by activating the stilbene synthase gene 2 (VdSTS2). BMC Plant Biol 19:1–15

    Google Scholar 

  • Zhang H, Wang D, Zhong H, Luo R, Shang M, Liu D, Chen H, Fang L, **ao S (2015) Ubiquitin-specific protease 15 negatively regulates virus-induced type I interferon signaling via catalytically-dependent and-independent mechanisms. Sci Rep 5:1–16

    Google Scholar 

  • Zhang Y (2003) Transcriptional regulation by histone ubiquitination and deubiquitination. Genes Dev 17:2733–2740

    CAS  PubMed  Google Scholar 

  • Zhao J, Zhou H, Zhang M, Gao Y, Li L, Gao Y, Li M, Yang Y, Guo Y, Li X (2016) Ubiquitin-specific protease 24 negatively regulates abscisic acid signalling in Arabidopsis thaliana. Plant Cell Environ 39:427–440

    CAS  PubMed  Google Scholar 

  • Zhou H, Zhao J, Cai J, Patil SB (2017) UBIQUITIN-SPECIFIC PROTEASES function in plant development and stress responses. Plant Mol Biol 94:565–576

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are thankful to College of Horticulture, Hebei Agricultural University for providing help in this research work.

Author information

Author notes

  1. Umer Karamat and Javaria Tabusam have contributed equally to this work.

Authors and Affiliations

  1. College of Horticulture, Hebei Agricultural University, Baoding, 071000, China

    Umer Karamat, Javaria Tabusam, Muhammad Khalil Ullah Khan, Sumer Zulfiqar, Wenchao Du & Muhammad Awais Farooq

  2. Molecular Virology & Genome Editing Lab NIBGE, Faisalabad, Pakistan

    Muhammad Jawad Akbar Awan & Muhammad Awais Farooq

Authors
  1. Umer Karamat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Javaria Tabusam
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Muhammad Khalil Ullah Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Muhammad Jawad Akbar Awan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sumer Zulfiqar
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wenchao Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Muhammad Awais Farooq
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

UK and JT did all genome-wide and expression analysis; MKK, MJAA, and SZ wrote the paper; and WD and MAF edited, supervised, and approved the manuscript.

Corresponding authors

Correspondence to Umer Karamat or Muhammad Awais Farooq.

Ethics declarations

Conflict of interest

There is no declaration of competing interest.

Ethical Approval

We hereby confirm that this work is original and has not been published elsewhere, nor it is currently under consideration for publication elsewhere. We confirm that the manuscript has been read and approved by all the named authors and we understand that the Corresponding Author is the sole contact for the Editorial process.

Additional information

Handling Editor: Peter Poor.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Karamat, U., Tabusam, J., Khan, M.K.U. et al. Genome-Wide Identification, Characterization, and Expression Profiling of Eukaryotic-Specific UBP Family Genes in Brassica rapa. J Plant Growth Regul 42, 3552–3567 (2023). https://doi.org/10.1007/s00344-022-10820-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-022-10820-0

Keywords

Search

Navigation