Abstract
Ubiquitin-specific proteases (UBPs), the largest group of deubiquitinating enzymes (DUBs), play pivotal roles in various aspects of plant physiology including growth, development, and stress response by maintaining the ubiquitin molecule pool or removing ubiquitin from targeted proteins. While numerous studies exist on UBPs across various plant species, studies focusing on the Fagaceae family remain scarce. In this study, 20 UBP genes were identified in Quercus robur and phylogenetically classified into 12 groups, supported by domain organization and conserved motif composition. The gene structures and chromosomal localizations of these genes were elucidated. To understand the evolution of the QrUBP gene family, synteny analysis was conducted among Q. robur and five other plant species. Notably, four QrUBP genes (QrUBP3, QrUBP12A, QrUBP16, and QrUBP23) were found to have at least four isogenous gene pairs, implying important roles in the phylogenetic process of the UBP gene family. Moreover, cis-acting elements analysis reveals that the QrUBP promoters contain a large number of hormone-response elements and stress-response elements. The RT-qPCR analysis of roots, stems, and leaves indicates that some of the QrUBP genes were expressed ubiquitously, while others were organ-specific. For example, QrUBP15* was primarily expressed in roots, while QrUBP8 showed tissue-specific expression in stems. Additionally, comprehensive physicochemical and subcellular localization analyses were conducted. Collectively, this comprehensive study provides insights into the UBP gene family in Q. robur, laying a solid foundation for future investigations elucidating the functional roles of QrUBP genes in plant growth and stress responses.
Similar content being viewed by others
Data availability
The data of this study are available upon reasonable request to the first author or the author for correspondence.
References
Aung K, Hu J (2012) Differential roles of Arabidopsis dynamin-related proteins DRP3A, DRP3B, and DRP5B in organelle division. J Integr Plant Biol. https://doi.org/10.1111/j.1744-7909.2012.01174.x
Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME suite. Nucleic Acids Res 43:W39–W49. https://doi.org/10.1093/nar/gkv416
Berardini TZ, Reiser L, Li D et al (2015) The arabidopsis information resource: making and mining the “gold standard” annotated reference plant genome. Genesis 53:474–485. https://doi.org/10.1002/dvg.22877
Buchfink B, Reuter K, Drost H-G (2021) Sensitive protein alignments at tree-of-life scale using diamond. Nat Methods 18:366–368. https://doi.org/10.1038/s41592-021-01101-x
Callis J (2014) The ubiquitination machinery of the ubiquitin system. Arabidopsis Book 12:e0174. https://doi.org/10.1199/tab.0174
Cao Y, Li Y, Wang L et al (2022) Evolution and function of ubiquitin-specific proteases (UBPs): insight into seed development roles in plants. Int J Biol Macromol 221:796–805. https://doi.org/10.1016/j.ijbiomac.2022.08.163
Carpena M, Pereira AG, Prieto MA, Simal-Gandara J (2020) Wine aging technology: fundamental role of wood barrels. Foods 9:1160. https://doi.org/10.3390/foods9091160
Chao J, Li Z, Sun Y et al (2021) MG2C: a user-friendly online tool for drawing genetic maps. Mol Hortic 1:16. https://doi.org/10.1186/s43897-021-00020-x
Chen L, Yang W, Liu S et al (2023) Genome-wide analysis and identification of light-harvesting chlorophyll a/b binding (LHC) gene family and BSMV-VIGS silencing TaLHC86 reduced salt tolerance in wheat. Int J Biol Macromol 242:124930. https://doi.org/10.1016/j.ijbiomac.2023.124930
Chung CH, Baek SH (1999) Deubiquitinating enzymes: their diversity and emerging roles. Biochem Biophys Res Commun 266:633–640. https://doi.org/10.1006/bbrc.1999.1880
Clague MJ, Coulson JM, Urbé S (2012) Cellular functions of the DUBs. J Cell Sci 125:277–286. https://doi.org/10.1242/jcs.090985
Cui X, Lu F, Li Y et al (2013) Ubiquitin-specific proteases UBP12 and UBP13 act in circadian clock and photoperiodic flowering regulation in Arabidopsis. Plant Physiol 162:897–906. https://doi.org/10.1104/pp.112.213009
Darriba D, Posada D, Kozlov AM et al (2020) ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Mol Biol Evol 37:291–294. https://doi.org/10.1093/molbev/msz189
De Poot SAH, Tian G, Finley D (2017) Meddling with fate: the proteasomal deubiquitinating enzymes. J Mol Biol 429:3525–3545. https://doi.org/10.1016/j.jmb.2017.09.015
Doelling JH, Phillips AR, Soyler-Ogretim G et al (2007) The ubiquitin-specific protease subfamily UBP3/UBP4 is essential for pollen development and transmission in Arabidopsis. Plant Physiol 145:801–813. https://doi.org/10.1104/pp.106.095323
Doelling JH, Yan N, Kurepa J et al (2001) The ubiquitin-specific protease UBP14 is essential for early embryo development in Arabidopsis thaliana: AtUBP14 is essential for embryogenesis. Plant J 27:393–405. https://doi.org/10.1046/j.1365-313X.2001.01106.x
Du L, Li N, Chen L et al (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. https://doi.org/10.1105/tpc.114.122663
Ducousso A, Bordacs S (2003) Quercus robur/Quercus petraea. International Plant Genetic Resources Institute, Rome
El-Gebali S, Mistry J, Bateman A et al (2019) The Pfam protein families database in 2019. Nucleic Acids Res 47:D427–D432. https://doi.org/10.1093/nar/gky995
Ewan R, Pangestuti R, Thornber S et al (2011) Deubiquitinating enzymes AtUBP12 and AtUBP13 and their tobacco homologue NtUBP12 are negative regulators of plant immunity. New Phytol 191:92–106. https://doi.org/10.1111/j.1469-8137.2011.03672.x
Farag S, El-Emary N, Niwa M (1998) Gallotannins from Quercus robur cultivated in Egypt. Bull Pharm Sci Assiut 21:1–6. https://doi.org/10.21608/bfsa.1998.67765
Gross CT, McGinnis W (1996) DEAF-1, a novel protein that binds an essential region in a deformed response element. EMBO J 15:1961–1970. https://doi.org/10.1002/j.1460-2075.1996.tb00547.x
Hallgren J, Tsirigos KD, Pedersen MD et al (2022) DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks. Bioinformatics 50:9
Horton P, Park K-J, Obayashi T et al (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587. https://doi.org/10.1093/nar/gkm259
Isono E, Nagel M-K (2014) Deubiquitylating enzymes and their emerging role in plant biology. Front Plant Sci 5:56. https://doi.org/10.3389/fpls.2014.00056
Karamat U, Tabusam J, Khan MKU et al (2023) Genome-wide identification, characterization, and expression profiling of eukaryotic-specific UBP family genes in Brassica rapa. J Plant Growth Regul 42:3552–3567. https://doi.org/10.1007/s00344-022-10820-0
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Komander D, Clague MJ, Urbé S (2009) Breaking the chains: structure and function of the deubiquitinases. Nat Rev Mol Cell Biol 10:550–563. https://doi.org/10.1038/nrm2731
Kozlov AM, Darriba D, Flouri T et al (2019) RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35:4453–4455. https://doi.org/10.1093/bioinformatics/btz305
Lee C-M, Li M-W, Feke A et al (2019) GIGANTEA recruits the UBP12 and UBP13 deubiquitylases to regulate accumulation of the ZTL photoreceptor complex. Nat Commun 10:3750. https://doi.org/10.1038/s41467-019-11769-7
Li W-F, Perry PJ, Prafulla NN, Schmidt W (2010) Ubiquitin-specific protease 14 (UBP14) is involved in root responses to phosphate deficiency in Arabidopsis. Mol Plant 3:212–223. https://doi.org/10.1093/mp/ssp086
Liu Y, Wang F, Zhang H et al (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. https://doi.org/10.1111/j.1365-313X.2008.03557.x
Liu Z, Zhang Y, Zheng Y et al (2023) Genome-wide identification glutathione-S-transferase gene superfamily in Daphnia pulex and its transcriptional response to nanoplastics. Int J Biol Macromol 230:123112. https://doi.org/10.1016/j.ijbiomac.2022.123112
Lutterbach B, Sun D, Schuetz J, Hiebert SW (1998) The MYND motif is required for repression of basal transcription from the multidrug resistance 1 promoter by the t(8;21) fusion protein. Mol Cell Biol 18:3604–3611. https://doi.org/10.1128/MCB.18.6.3604
Mady MS, Ibrahim RR, El-Sayed EK et al (2023) UHPLC-MS profiles and antidiarrheal activity of Quercus coccinea munch. and Quercus robur L. employing in vivo technique. Front Pharmacol 14:1120146. https://doi.org/10.3389/fphar.2023.1120146
Majumdar P, Nath U (2020) De-ubiquitinases on the move: an emerging field in plant biology. Plant Biol J 22:563–572. https://doi.org/10.1111/plb.13118
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. https://doi.org/10.3389/fpls.2017.02274
Masselink H, Bernards R (2000) The adenovirus E1A binding protein BS69 is a corepressor of transcription through recruitment of N-CoR. Oncogene 19:1538–1546. https://doi.org/10.1038/sj.onc.1203421
Mevissen TET, Komander D (2017) Mechanisms of deubiquitinase specificity and regulation. Annu Rev Biochem 86:159–192. https://doi.org/10.1146/annurev-biochem-061516-044916
Mishra B, Gupta DK, Pfenninger M et al (2018) A reference genome of the European beech (Fagus sylvatica L.). GigaScience 7. https://doi.org/10.1093/gigascience/giy063
Pandey A, Sharma P, Mishra D et al (2023) Genome-wide identification of the fibrillin gene family in chickpea (Cicer arietinum L.) and its response to drought stress. Int J Biol Macromol 234:123757. https://doi.org/10.1016/j.ijbiomac.2023.123757
Plomion C, Aury J-M, Amselem J et al (2018) Oak genome reveals facets of long lifespan. Nature Plants 4:440–452. https://doi.org/10.1038/s41477-018-0172-3
Potter SC, Luciani A, Eddy SR et al (2018) HMMER web server: 2018 update. Nucleic Acids Res 46:W200–W204. https://doi.org/10.1093/nar/gky448
Ramakrishna G, Singh A, Kaur P et al (2022) Genome wide identification and characterization of small heat shock protein gene family in pigeonpea and their expression profiling during abiotic stress conditions. Int J Biol Macromol 197:88–102. https://doi.org/10.1016/j.ijbiomac.2021.12.016
Reyes-Turcu FE, Ventii KH, Wilkinson KD (2009) Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem 78:363–397. https://doi.org/10.1146/annurev.biochem.78.082307.091526
de Rigo D, San-Miguel-Ayanz J, Caudullo G et al (eds) (2016) European atlas of forest tree species. Publications Office of the European Union, Luxembourg
Rombauts S, Dehais P, Van Montagu M, Rouze P (1999) PlantCARE, a plant cis-acting regulatory element database. Nucleic Acids Res 27:295–296. https://doi.org/10.1093/nar/27.1.295
Sadanandom A, Bailey M, Ewan R et al (2012) The ubiquitin–proteasome system: central modifier of plant signalling. New Phytol 196:13–28. https://doi.org/10.1111/j.1469-8137.2012.04266.x
Schroeder H, Cronn R, Yanbaev Y et al (2016) Development of molecular markers for determining continental origin of wood from white oaks (Quercus L. sect. Quercus). PLoS ONE 11:e0158221. https://doi.org/10.1371/journal.pone.0158221
Singh M, Singh A, Yadav N, Yadav DK (2022) Current perspectives of ubiquitination and SUMOylation in abiotic stress tolerance in plants. Front Plant Sci 13:993194. https://doi.org/10.3389/fpls.2022.993194
Skelly MJ (2022) The emerging roles of deubiquitinases in plant proteostasis. Essays Biochem 66:147–154. https://doi.org/10.1042/EBC20210060
Sork VL, Cokus SJ, Fitz-Gibbon ST et al (2022) High-quality genome and methylomes illustrate features underlying evolutionary success of oaks. Nat Commun 13:2047. https://doi.org/10.1038/s41467-022-29584-y
Sun Y, Guo J, Zeng X et al (2022) Chromosome-scale genome assembly of Castanopsis tibetana provides a powerful comparative framework to study the evolution and adaptation of Fagaceae trees. Mol Ecol Resour 22:1178–1189. https://doi.org/10.1111/1755-0998.13539
Wang D-H, Song W, Wei S-W et al (2018) Characterization of the ubiquitin C-terminal hydrolase and ubiquitin-specific protease families in rice (Oryza sativa). Front Plant Sci 9:1636. https://doi.org/10.3389/fpls.2018.01636
Wang Y, Tang H, DeBarry JD et al (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49–e49. https://doi.org/10.1093/nar/gkr1293
Wilkins MR, Gasteiger E, Bairoch A et al (1998) Protein identification and analysis tools in the ExPASy server. 2-D Proteome analysis protocols. Humana Press, New Jersey, pp 531–552
Wilkinson KD (2000) Ubiquitination and deubiquitination: targeting of proteins for degradation by the proteasome. Semin Cell Dev Biol 11:141–148. https://doi.org/10.1006/scdb.2000.0164
Wu R, Shi Y, Zhang Q et al (2019) Genome-wide identification and characterization of the UBP gene family in Moso Bamboo (Phyllostachys edulis). IJMS 20:4309. https://doi.org/10.3390/ijms20174309
Xing Y, Liu Y, Zhang Q, et al (2019) Hybrid de novo genome assembly of Chinese chestnut (Castanea mollissima). GigaScience 8:giz112. https://doi.org/10.1093/gigascience/giz112
Xu M, Jin P, Liu T et al (2021) Genome-wide identification and characterization of UBP gene family in wheat (Triticum aestivum L.). PeerJ 9:e11594. https://doi.org/10.7717/peerj.11594
Xu Y, Jin W, Li N et al (2016) UBIQUITIN-SPECIFIC PROTEASE 14 interacts with ULTRAVIOLET-B INSENSITIVE 4 to regulate endoreduplication and cell and organ growth in Arabidopsis. Plant Cell tpc.00007.2016. https://doi.org/10.1105/tpc.16.00007
Yan N, Doelling JH, Falbel TG et al (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. https://doi.org/10.1104/pp.124.4.1828
Yu X-Q, Su W, Zhang H et al (2023) Genome-wide analysis of autophagy-related gene family and PagATG18a enhances salt tolerance by regulating ROS homeostasis in poplar. Int J Biol Macromol 224:1524–1540. https://doi.org/10.1016/j.ijbiomac.2022.10.240
Yuan G, Sun D, Wang Y et al (2022) Genome-wide identification and expression analysis of NIN-like protein (NLP) genes reveals their potential roles in the response to nitrate signaling in watermelon. Hortic Plant J 8:602–614. https://doi.org/10.1016/j.hpj.2022.06.010
Zhang Z (2022) KaKs_Calculator 3.0: calculating selective pressure on coding and non-coding sequences. Genom Proteom Bioinform 20:536–540. https://doi.org/10.1016/j.gpb.2021.12.002
Zhao J, Zhou H, Li X (2013) Ubiquitin-specific protease16 interacts with a heavy metal associated isoprenylated plant protein27 and modulates cadmium tolerance. Plant Signal Behav 8:e25680. https://doi.org/10.4161/psb.25680
Zhao J, Zhou H, Zhang M et al (2016) Ubiquitin-specific protease 24 negatively regulates abscisic acid signalling in Arabidopsis thaliana. Plant Cell Environ 39:427–440. https://doi.org/10.1111/pce.12628
Zheng W, Du L (2021) The DUB family in Populus: identification, characterization, evolution and expression patterns. BMC Genom 22:541. https://doi.org/10.1186/s12864-021-07844-3
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. https://doi.org/10.1007/s11103-017-0633-5
Zhou L, Feng T, Xu S, Gao F, Lam TT, Wang Q, Wu T, Huang H, Zhan L, Li L, Guan Y, Dai Z, Yu G (2022) ggmsa: a visual exploration tool for multiple sequence alignment and associated data. Brief Bioinform 3(4):bbac222. https://doi.org/10.1093/bib/bbac222
Zhou H, Zhao J, Yang Y et al (2013) Ubiquitin-specific protease16 modulates salt tolerance in Arabidopsis by regulating Na+/H+ antiport activity and serine hydroxymethyltransferase stability. Plant Cell 24:5106–5122. https://doi.org/10.1105/tpc.112.106393
Acknowledgements
The author would like to express their gratitude to Chunhua Pan who assisted them in high performance computers, as well as to the anonymous reviewers who contributed to improve the manuscript.
Funding
The study was funded by the National Natural Science Foundation of China (32070548) and the National Key Research and Development Program of China (2021YFD2200800).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors have no conflict of interest.
Additional information
Communicated by Carlson.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) 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.
About this article
Cite this article
Song, K., Zhang, B. & Du, L. Genome-wide identification and analysis of UBP gene family in Quercus robur. Trees (2024). https://doi.org/10.1007/s00468-024-02519-4
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00468-024-02519-4