Evolution and expression analysis of the sorghum ubiquitin-conjugating enzyme family
Liqiang Jia
A B , QiuFang Zhao A and Shu Chen A
+ Author Affiliations
- Author Affiliations
A Key Laboratory of Tropical Fruit Biology (Ministry of Agriculture), South Subtropical Crop Research Institute, Chinese Academy of Tropical Agricultural Science, Zhanjiang 524091, China.
B Corresponding author. Email: liqiangj@zju.edu.cn
Functional Plant Biology 46(3) 236-247 https://doi.org/10.1071/FP18184
Submitted: 13 July 2018 Accepted: 2 October 2018 Published: 25 October 2018
Abstract
Ubiquitin-conjugating enzymes (UBCs), which catalyse the transfer of ubiquitin to substrate or E3 ligases, are key enzymes in ubiquitination modifications of target proteins. Current knowledge regarding the sorghum (Sorghum bicolor (L.) Moench) ubiquitin-conjugating enzyme (SbUBC) family remains very limited. We identified 53 UBC-encoding genes in the sorghum genome and divided these into 18 groups according to their phylogenetic relationship with Arabidopsis thaliana (L.) Heynh., which was further supported by conserved motif and gene structure analyses. Different expression levels under a variety of abiotic stresses suggested that these might participate in distinct signalling pathways and that they underwent functional divergence during evolution. Furthermore, several SbUBC genes responded to single treatments, and individual SbUBC genes responded to multiple treatments, suggesting that sorghum UBCs may mediate crosstalk among different signalling pathways. Overall, the results provide valuable information for better understanding the classification and putative functions of sorghum UBC-encoding genes.
Additional keywords: abiotic stress, expression profiles, genomic characterisation, Sorghum bicolor, UBC family.
References
Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ (2006) pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiology 141, 1000–1011.| pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene.Crossref | GoogleScholarGoogle Scholar |
Bahmani R, Kim D, Lee BD, Hwang S (2017) Over-expression of tobacco UBC1 encoding a ubiquitin-conjugating enzyme increases cadmium tolerance by activating the 20S/26S proteasome and by decreasing Cd accumulation and oxidative stress in tobacco (Nicotiana tabacum). Plant Molecular Biology 94, 433–451.
| Over-expression of tobacco UBC1 encoding a ubiquitin-conjugating enzyme increases cadmium tolerance by activating the 20S/26S proteasome and by decreasing Cd accumulation and oxidative stress in tobacco (Nicotiana tabacum).Crossref | GoogleScholarGoogle Scholar |
Bianconi ME, Dunning LT, Moreno-Villena JJ, Osborne CP, Christin PA (2018) Gene duplication and dosage effects during the early emergence of C4 photosynthesis in the grass genus Alloteropsis. Journal of Experimental Botany 69, 1967–1980.
| Gene duplication and dosage effects during the early emergence of C4 photosynthesis in the grass genus Alloteropsis.Crossref | GoogleScholarGoogle Scholar |
Bowers J, Chapman B, Rong J, Paterson A (2003) Unravelling angiosperm genome evolution events. Nature 422, 433–438.
| Unravelling angiosperm genome evolution events.Crossref | GoogleScholarGoogle Scholar |
Burroughs AM, Jaffee M, Iyer LM, Aravind L (2008) Anatomy of the E2 ligase fold: implications for enzymology and evolution of ubiquitin/Ub-like protein conjugation. Journal of Structural Biology 162, 205–218.
| Anatomy of the E2 ligase fold: implications for enzymology and evolution of ubiquitin/Ub-like protein conjugation.Crossref | GoogleScholarGoogle Scholar |
Chen CC, Chen YY, Tang IC, Liang HM, Lai CC, Chiou JM, Yeh KC (2011) Arabidopsis SUMO E3 ligase SIZ1 is involved in excess copper tolerance. Plant Physiology 156, 2225–2234.
| Arabidopsis SUMO E3 ligase SIZ1 is involved in excess copper tolerance.Crossref | GoogleScholarGoogle Scholar |
Chung E, Cho CW, So HA, Kang JS, Chung YS, Lee JH (2013) Overexpression of VrUBC1, a mung bean E2 ubiquitin-conjugating enzyme, enhances osmotic stress tolerance in Arabidopsis. PLoS One 8, e66056
| Overexpression of VrUBC1, a mung bean E2 ubiquitin-conjugating enzyme, enhances osmotic stress tolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Criqui MC, de Almeida Engler J, Camasses A, Capron A, Parmentier Y, Inze D, Genschik P (2002) Molecular characterization of plant ubiquitin-conjugating enzymes belonging to the UbcP4/E2-C/UBCx/UbcH10 gene family. Plant Physiology 130, 1230–1240.
| Molecular characterization of plant ubiquitin-conjugating enzymes belonging to the UbcP4/E2-C/UBCx/UbcH10 gene family.Crossref | GoogleScholarGoogle Scholar |
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. The Plant Cell 24, 233–244.
| Arabidopsis ubiquitin conjugase UBC32 is an ERAD component that functions in brassinosteroid-mediated salt stress tolerance.Crossref | GoogleScholarGoogle Scholar |
Dong B, Rengel Z, Delhaize E (1998) Uptake and translocation of phosphate by pho2 mutant and wild-type seedlings of Arabidopsis thaliana. Planta 205, 251–256.
| Uptake and translocation of phosphate by pho2 mutant and wild-type seedlings of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Dong C, Hu H, Jue D, Zhao Q, Chen H, Xie J, Jia L (2016) The banana E2 gene family: genomic identification, characterization, expression profiling analysis. Plant Science 245, 11–24.
| The banana E2 gene family: genomic identification, characterization, expression profiling analysis.Crossref | GoogleScholarGoogle Scholar |
Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Research 42, D222–D230.
| Pfam: the protein families database.Crossref | GoogleScholarGoogle Scholar |
Gao Y, Wang Y, Xin H, Li S, Liang Z (2017) Involvement of ubiquitin-conjugating enzyme (E2 gene family) in ripening process and response to cold and heat stress of Vitis vinifera. Scientific Reports 7, 13290
| Involvement of ubiquitin-conjugating enzyme (E2 gene family) in ripening process and response to cold and heat stress of Vitis vinifera.Crossref | GoogleScholarGoogle Scholar |
Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Research 40, D1178–D1186.
| Phytozome: a comparative platform for green plant genomics.Crossref | GoogleScholarGoogle Scholar |
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.
| New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.Crossref | GoogleScholarGoogle Scholar |
Hodson C, Purkiss A, Miles JA, Walden H (2014) Structure of the human FANCL RING-Ube2T complex reveals determinants of cognate E3–E2 selection. Structure (London, England) 22, 337–344.
| Structure of the human FANCL RING-Ube2T complex reveals determinants of cognate E3–E2 selection.Crossref | GoogleScholarGoogle Scholar |
Hofmann RM, Pickart CM (2001) In vitro assembly and recognition of Lys-63 polyubiquitin chains. The Journal of Biological Chemistry 276, 27936–27943.
| In vitro assembly and recognition of Lys-63 polyubiquitin chains.Crossref | GoogleScholarGoogle Scholar |
Jones D, Crowe E, Stevens TA, Candido EP (2002) Functional and phylogenetic analysis of the ubiquitylation system in Caenorhabditis elegans: ubiquitin-conjugating enzymes, ubiquitin-activating enzymes, and ubiquitin-like proteins. Genome Biol. 3, RESEARCH0002
Jue D, Sang X, Lu S, Dong C, Zhao Q, Chen H, Jia L (2015) Genome-wide identification, phylogenetic and expression analyses of the ubiquitin-conjugating enzyme gene family in maize. PLoS One 10, e0143488
| Genome-wide identification, phylogenetic and expression analyses of the ubiquitin-conjugating enzyme gene family in maize.Crossref | GoogleScholarGoogle Scholar |
Katoh K, Rozewicki J, Yamada KD (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics
| MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization.Crossref | GoogleScholarGoogle Scholar |
Kerscher O, Felberbaum R, Hochstrasser M (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annual Review of Cell and Developmental Biology 22, 159–180.
| Modification of proteins by ubiquitin and ubiquitin-like proteins.Crossref | GoogleScholarGoogle Scholar |
Kraft E, Stone SL, Ma L, Su N, Gao Y, Lau OS, Deng XW, Callis J (2005) Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis. Plant Physiology 139, 1597–1611.
| Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
| MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar |
Lau SO, Deng XW (2009) Effect of Arabidopsis COP10 ubiquitin E2 enhancement activity across E2 families and functional conservation among its canonical homologues. The Biochemical Journal 418, 683–690.
| Effect of Arabidopsis COP10 ubiquitin E2 enhancement activity across E2 families and functional conservation among its canonical homologues.Crossref | GoogleScholarGoogle Scholar |
Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Research 40, D302–D305.
| SMART 7: recent updates to the protein domain annotation resource.Crossref | GoogleScholarGoogle Scholar |
Li W, Schmidt W (2010) A lysine-63-linked ubiquitin chain-forming conjugase, UBC13, promotes the developmental responses to iron deficiency in Arabidopsis roots. The Plant Journal 62, 330–343.
| A lysine-63-linked ubiquitin chain-forming conjugase, UBC13, promotes the developmental responses to iron deficiency in Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar |
Lin L, Tang H, Compton RO, Lemke C, Rainville LK, Wang X, Rong J, Rana MK, Paterson AH (2011a) Comparative analysis of Gossypium and Vitis genomes indicates genome duplication specific to the Gossypium lineage. Genomics 97, 313–320.
| Comparative analysis of Gossypium and Vitis genomes indicates genome duplication specific to the Gossypium lineage.Crossref | GoogleScholarGoogle Scholar |
Lin Y, Jiang H, Chu Z, Tang X, Zhu S, Cheng B (2011b) Genome-wide identification, classification and analysis of heat shock transcription factor family in maize. BMC Genomics 12, 76
| Genome-wide identification, classification and analysis of heat shock transcription factor family in maize.Crossref | GoogleScholarGoogle Scholar |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PC and the 2–ΔΔCT method. Methods (San Diego, Calif.) 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PC and the 2–ΔΔCT method.Crossref | GoogleScholarGoogle Scholar |
Makita Y, Shimada S, Kawashima M, Kondou-Kuriyama T, Toyoda T, Matsui M (2015) MOROKOSHI: transcriptome database in Sorghum bicolor. Plant & Cell Physiology 56, e6
| MOROKOSHI: transcriptome database in Sorghum bicolor.Crossref | GoogleScholarGoogle Scholar |
Michelle C, Vourc’h P, Mignon L, Andres CR (2009) What was the set of ubiquitin and ubiquitin-like conjugating enzymes in the eukaryote common ancestor? Journal of Molecular Evolution 68, 616–628.
| What was the set of ubiquitin and ubiquitin-like conjugating enzymes in the eukaryote common ancestor?Crossref | GoogleScholarGoogle Scholar |
Millyard L, Lee J, Zhang C, Yates G, Sadanandom A (2016) The ubiquitin conjugating enzyme, TaU4 regulates wheat defence against the phytopathogen Zymoseptoria tritici. Scientific Reports 6, 35683
| The ubiquitin conjugating enzyme, TaU4 regulates wheat defence against the phytopathogen Zymoseptoria tritici.Crossref | GoogleScholarGoogle Scholar |
Miura K, Lee J, Jin JB, Yoo CY, Miura T, Hasegawa PM (2009) Sumoylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signaling. Proceedings of the National Academy of Sciences of the United States of America 106, 5418–5423.
| Sumoylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signaling.Crossref | GoogleScholarGoogle Scholar |
Miura K, Lee J, Gong Q, Ma S, Jin JB, Yoo CY, Miura T, Sato A, Bohnert HJ, Hasegawa PM (2011) SIZ1 regulation of phosphate starvation-induced root architecture remodeling involves the control of auxin accumulation. Plant Physiology 155, 1000–1012.
| SIZ1 regulation of phosphate starvation-induced root architecture remodeling involves the control of auxin accumulation.Crossref | GoogleScholarGoogle Scholar |
Novatchkova M, Tomanov K, Hofmann K, Stuible H-P, Bachmair A (2012) Update on sumoylation: defining core components of the plant SUMO conjugation system by phylogenetic comparison. New Phytologist 195, 23–31.
| Update on sumoylation: defining core components of the plant SUMO conjugation system by phylogenetic comparison.Crossref | GoogleScholarGoogle Scholar |
Paterson A, Bowers J, Chapman B (2004) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proceedings of the National Academy of Sciences of the United States of America 101, 9903–9908.
| Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics.Crossref | GoogleScholarGoogle Scholar |
Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457, 551–556.
| The Sorghum bicolor genome and the diversification of grasses.Crossref | GoogleScholarGoogle Scholar |
Peng X, Zhao Y, Cao J, Zhang W, Jiang H, Li X, Ma Q, Zhu S, Cheng B (2012) CCCH-type zinc finger family in maize: genome-wide identification, classification and expression profiling under abscisic acid and drought treatments. PLoS One 7, e40120
| CCCH-type zinc finger family in maize: genome-wide identification, classification and expression profiling under abscisic acid and drought treatments.Crossref | GoogleScholarGoogle Scholar |
Takai R, Matsuda N, Nakano A, Hasegawa K, Akimoto C, Shibuya N, Minami E (2002) EL5, a rice N-acetylchitooligosaccharide elicitor-responsive RING-H2 finger protein, is a ubiquitin ligase which functions in vitro in co-operation with an elicitor-responsive ubiquitin-conjugating enzyme, OsUBC5b. The Plant Journal 30, 447–455.
| EL5, a rice N-acetylchitooligosaccharide elicitor-responsive RING-H2 finger protein, is a ubiquitin ligase which functions in vitro in co-operation with an elicitor-responsive ubiquitin-conjugating enzyme, OsUBC5b.Crossref | GoogleScholarGoogle Scholar |
Tang H, Lyons E, Pedersen B, Schnable J, Paterson A, Freeling M (2011) Screening synteny blocks in pairwise genome comparisons through integer programming. BMC Bioinformatics 12, 102
| Screening synteny blocks in pairwise genome comparisons through integer programming.Crossref | GoogleScholarGoogle Scholar |
Wan X, Mo A, Liu S, Yang L, Li L (2011) Constitutive expression of a peanut ubiquitin-conjugating enzyme gene in Arabidopsis confers improved water-stress tolerance through regulation of stress-responsive gene expression. Journal of Bioscience and Bioengineering 111, 478–484.
| Constitutive expression of a peanut ubiquitin-conjugating enzyme gene in Arabidopsis confers improved water-stress tolerance through regulation of stress-responsive gene expression.Crossref | GoogleScholarGoogle Scholar |
Wang X, Tang H, Bowers JE, Paterson AH (2009) Comparative inference of illegitimate recombination between rice and sorghum duplicated genes produced by polyploidization. Genome Research 19, 1026–1032.
| Comparative inference of illegitimate recombination between rice and sorghum duplicated genes produced by polyploidization.Crossref | GoogleScholarGoogle Scholar |
Wang Y, Wang W, Cai J, Zhang Y, Qin G, Tian S (2014) Tomato nuclear proteome reveals the involvement of specific E2 ubiquitin-conjugating enzymes in fruit ripening. Genome Biology 15, 548–555.
| Tomato nuclear proteome reveals the involvement of specific E2 ubiquitin-conjugating enzymes in fruit ripening.Crossref | GoogleScholarGoogle Scholar |
Wei K, Chen J, Wang Y, Chen Y, Chen S, Lin Y, Pan S, Zhong X, Xie D (2012) Genome-wide analysis of bZIP-encoding genes in maize. DNA Research 19, 463–476.
| Genome-wide analysis of bZIP-encoding genes in maize.Crossref | GoogleScholarGoogle Scholar |
Wen R, Newton L, Li G, Wang H, Xiao W (2006) Arabidopsis thaliana UBC13: implication of error-free DNA damage tolerance and Lys63-linked polyubiquitylation in plants. Plant Molecular Biology 61, 241–253.
| Arabidopsis thaliana UBC13: implication of error-free DNA damage tolerance and Lys63-linked polyubiquitylation in plants.Crossref | GoogleScholarGoogle Scholar |
Wen R, Torres-Acosta JA, Pastushok L, Lai X, Pelzer L, Wang H, Xiao W (2008) Arabidopsis UEV1D promotes Lysine-63-linked polyubiquitination and is involved in DNA damage response. The Plant Cell 20, 213–227.
| Arabidopsis UEV1D promotes Lysine-63-linked polyubiquitination and is involved in DNA damage response.Crossref | GoogleScholarGoogle Scholar |
Wenzel DM, Stoll KE, Klevit RE (2011) E2s: structurally economical and functionally replete. The Biochemical Journal 433, 31–42.
| E2s: structurally economical and functionally replete.Crossref | GoogleScholarGoogle Scholar |
Wilson RC, Edmondson SP, Flatt JW, Helms K, Twigg PD (2011) The E2–25K ubiquitin-associated (UBA) domain aids in polyubiquitin chain synthesis and linkage specificity. Biochemical and Biophysical Research Communications 405, 662–666.
| The E2–25K ubiquitin-associated (UBA) domain aids in polyubiquitin chain synthesis and linkage specificity.Crossref | GoogleScholarGoogle Scholar |
Winn PJ, Religa TL, Battey JN, Banerjee A, Wade RC (2004) Determinants of functionality in the ubiquitin conjugating enzyme family. Structure (London, England) 12, 1563–1574.
| Determinants of functionality in the ubiquitin conjugating enzyme family.Crossref | GoogleScholarGoogle Scholar |
Xu L, Menard 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. The Plant Journal 57, 279–288.
| 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.Crossref | GoogleScholarGoogle Scholar |
Ye Y, Rape M (2009) Building ubiquitin chains: E2 enzymes at work. Nature Reviews. Molecular Cell Biology 10, 755–764.
| Building ubiquitin chains: E2 enzymes at work.Crossref | GoogleScholarGoogle Scholar |
Zhang Y, Li T, Wang L, Zhao H (2015) Characterization of the ubiquitin-conjugating enzyme gene family in rice and evaluation of expression profiles under abiotic stresses and hormone treatments. PLoS One 10, e0122621
| Characterization of the ubiquitin-conjugating enzyme gene family in rice and evaluation of expression profiles under abiotic stresses and hormone treatments.Crossref | GoogleScholarGoogle Scholar |
Zhao Y, Zhou Y, Jiang H, Li X, Gan D, Peng X, Zhu S, Cheng B (2011) Systematic analysis of sequences and expression patterns of drought responsive members of the HD-Zip gene family in maize. PLoS One 6, e28488
| Systematic analysis of sequences and expression patterns of drought responsive members of the HD-Zip gene family in maize.Crossref | GoogleScholarGoogle Scholar |
Zhou GA, Chang RZ, Qiu LJ (2010) Overexpression of soybean ubiquitin-conjugating enzyme gene GmUBC2 confers enhanced drought and salt tolerance through modulating abiotic stress-responsive gene expression in Arabidopsis. Plant Molecular Biology 72, 357–367.
| Overexpression of soybean ubiquitin-conjugating enzyme gene GmUBC2 confers enhanced drought and salt tolerance through modulating abiotic stress-responsive gene expression in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Zhou B, Mural RV, Chen X, Oates ME, Connor RA, Martin GB, Gough J, Zeng L (2017) A subset of ubiquitin-conjugating enzymes is essential for plant immunity. Plant Physiology 173, 1371–1390.
| A subset of ubiquitin-conjugating enzymes is essential for plant immunity.Crossref | GoogleScholarGoogle Scholar |
Zolman BK, Monroe-Augustus M, Silva ID, Bartel B (2005) Identification and functional characterization of Arabidopsis PEROXIN4 and the interacting protein PEROXIN22. The Plant Cell 17, 3422–3435.
| Identification and functional characterization of Arabidopsis PEROXIN4 and the interacting protein PEROXIN22.Crossref | GoogleScholarGoogle Scholar |
