Genome-Wide Identification and Expression Analysis of the 4-Coumarate: CoA Ligase Gene Family in Solanum tuberosum
Abstract
:1. Introduction
2. Results
2.1. Identification of 4CL Gene Family Members in Potato
2.2. Phylogenetic Analysis of Potato 4CL Gene Family
2.3. Analysis of the Gene Structures of the Potato 4CL Gene Family
2.4. Tandem Duplication of St4CL and Collinearity Analysis of the 4CL Gene Family among Different Species
2.5. Analysis of Promoter Cis-Acting Elements in the St4CL Gene Family
2.6. Expression Regulation Analysis and Protein Interaction Network Analysis
2.7. Expression of St4CLs under Different Treatments and St4CL5 Subcellular Localization
3. Discussion
4. Materials and Methods
4.1. Identification of 4CL Gene Family Members in Potato
4.2. Multiple Sequence Alignment and Construction of the Phylogenetic Tree
4.3. Gene Structure Analysis and Motif Detection of St4CL Gene Family
4.4. Tandem Gene Detection and Gene Collinearity Analysis of St4CL Gene Family
4.5. Analysis of Cis-Acting Elements in the Promoters of St4CL Gene Family
4.6. St4CL Genes Tissue Expression Analysis and Protein Interaction Network Analysis
4.7. Plant Material and Abiotic Stress Treatment
4.8. RT-qPCR Analysis and St4CL5 Subcellular Localization
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Hamberger, B.; Hahlbrock, K. The 4-coumarate: CoA ligase gene family in Arabidopsis thaliana comprises one rare, sinapate-activating and three commonly occurring isoenzymes. Proc. Natl. Acad. Sci. USA 2004, 101, 2209–2214. [Google Scholar] [CrossRef] [Green Version]
- Allina, S.M.; Pri-Hadash, A.; Theilmann, D.A.; Ellis, B.E.; Douglas, C.J. 4-Coumarate: Coenzyme A ligase in hybrid poplar: Properties of native enzymes, cDNA cloning, and analysis of recombinant enzymes. Plant Physiol. 1998, 116, 743–754. [Google Scholar] [CrossRef] [Green Version]
- Loscher, R.; Heide, L. Biosynthesis of p-hydroxybenzoate from p-coumarate and p-coumaroyl-coenzyme A in cell-free extracts of Lithospermum erythrorhizon cell cultures. Plant Physiol. 1994, 106, 271–279. [Google Scholar] [CrossRef] [Green Version]
- Li, Y.; Kim, J.I.; Pysh, L.; Chapple, C. Four isoforms of Arabidopsis 4-coumarate: CoA ligase have overlapping yet distinct roles in phenylpropanoid metabolism. Plant Physiol. 2015, 169, 2409–2421. [Google Scholar] [CrossRef] [Green Version]
- Lindl, T.; Kreuzaler, F.; Hahlbrock, K. Synthesis of p-coumaroyl coenzyme A with a partially purified p-coumarate: CoA ligase from cell suspension cultures of soybean (Glycine max). Biochim. Biophys. Acta (BBA) Enzymol. 1973, 302, 457–464. [Google Scholar] [CrossRef]
- Gross, G.G.; Zenk, M.H. Isolation and properties of hydroxycinnamate: CoA ligase from lignifying tissue of Forsthia. Eur. J. Biochem. 1974, 42, 453–459. [Google Scholar] [CrossRef] [PubMed]
- Yang, Y.H.; Yang, M.R.; Chen, J.Y.; Liu, Z.Y.; Zhang, Y.X.; Zhang, Z.Y.; Li, R.F. Two 4-coumarate: Coenzyme A ligase genes involved in acteoside and flavonoids biosynthesis in Rehmannia glutinosa. Ind. Crops Prod. 2022, 185, 115–117. [Google Scholar] [CrossRef]
- Li, M.; Guo, L.; Wang, Y.; Li, Y.; Jiang, X.; Liu, Y.; Xie, D.; Gao, L.; Xia, T. Molecular and biochemical characterization of two 4-coumarate: CoA ligase genes in tea plant (Camellia sinensis). Plant Mol. Biol. 2022, 109, 579–593. [Google Scholar] [CrossRef]
- Gui, J.; Shen, J.; Li, L. Functional characterization of evolutionarily divergent 4-coumarate: Coenzyme A ligases in rice. Plant Physiol. 2011, 157, 574–586. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.; Guo, L.; Zhao, Y.; Zhao, X.; Yuan, Z. Systematic Analysis and Expression Profiles of the 4-Coumarate: CoA Ligase (4CL) Gene Family in Pomegranate (Punica granatum L.). Int. J. Mol. Sci. 2022, 23, 3509. [Google Scholar] [CrossRef] [PubMed]
- Ehlting, J.; Büttner, D.; Wang, Q.; Douglas, C.J.; Somssich, I.E.; Kombrink, E. Three 4-coumarate: Coenzyme A ligases in Arabidopsis thaliana represent two evolutionarily divergent classes in angiosperms. Plant J. 1999, 19, 9–20. [Google Scholar] [CrossRef]
- Zhang, C.; Ma, T.; Luo, W.; Xu, J.; Liu, J.; Wan, D. Identification of 4CL genes in desert poplars and their changes in expression in response to salt stress. Genes 2015, 6, 901–917. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schröder, J. Protein sequence homology between plant 4-coumarate: CoA ligase and firefly luciferase. Nucleic Acids Res. 1989, 17, 460. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jackson, D.R.; Tu, S.S.; Nguyen, M.; Barajas, J.F.; Schaub, A.J.; Krug, D.; Pistorius, D.; Luo, R.; Müller, R.; Tsai, S. Structural insights into anthranilate priming during type II polyketide biosynthesis. ACS Chem. Biol. 2016, 11, 95–103. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xu, Q.; Dunbrack, R.L. ProtCID: A data resource for structural information on protein interactions. Nat. Commun. 2020, 11, 711. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gulick, A.M.; Starai, V.J.; Horswill, A.R.; Homick, K.M.; Escalante-Semerena, J.C. The 1.75 Å crystal structure of acetyl-CoA synthetase bound to adenosine-5′-propylphosphate and coenzyme A. Biochemistry 2003, 42, 2866–2873. [Google Scholar] [CrossRef]
- Ehlting, J.; Shin, J.J.; Douglas, C.J. Identification of 4-coumarate: Coenzyme A ligase (4CL) substrate recognition domains. Plant J. 2001, 27, 455–465. [Google Scholar] [CrossRef] [Green Version]
- Chowdhury, M.E.K.; Choi, B.; Cho, B.; Kim, J.B.; Park, S.U.; Natarajan, S.; Lim, H.; Bae, H. Regulation of 4CL, encoding 4-coumarate: Coenzyme A ligase, expression in kenaf under diverse stress conditions. Plant Omics 2013, 6, 254–262. [Google Scholar]
- Müller-Xing, R.; Xing, Q.; Goodrich, J. Footprints of the sun: Memory of UV and light stress in plants. Front. Plant Sci. 2014, 5, 474. [Google Scholar]
- Sun, H.; Li, Y.; Feng, S.; Zou, W.; Guo, K.; Fan, C.; Si, S.; Peng, L. Analysis of five rice 4-coumarate: Coenzyme A ligase enzyme activity and stress response for potential roles in lignin and flavonoid biosynthesis in rice. Biochem. Biophys. Res. Commun. 2013, 430, 1151–1156. [Google Scholar] [CrossRef]
- Chen, X.; Wang, H.; Li, X.; Ma, K.; Zhan, Y.; Zeng, F. Molecular cloning and functional analysis of 4-Coumarate: CoA ligase 4 (4CL-like 1) from Fraxinus mandshurica and its role in abiotic stress tolerance and cell wall synthesis. BMC Plant Biol. 2019, 19, 231. [Google Scholar] [CrossRef] [Green Version]
- Li, X.; Wu, Z.; Xiao, S.; Wang, A.; Hua, X.; Yu, Q.; Liu, Y.; Peng, L.; Yang, Y.; Wang, J. Characterization of abscisic acid (ABA) receptors and analysis of genes that regulate rutin biosynthesis in response to ABA in Fagopyrum tataricum. Plant Physiol. Biochem. 2020, 157, 432–440. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.; Guo, L.P.; Xie, T.; Yang, J.; Tang, J.F.; Li, X.; Wang, X.; Huang, L.Q. Different secondary metabolic responses to MeJA treatment in shikonin-proficient and shikonin-deficient cell lines from Arnebia euchroma (Royle) Johnst. Plant Cell Tissue Organ Cult. (PCTOC) 2014, 119, 587–598. [Google Scholar] [CrossRef]
- Lavhale, S.G.; Kalunke, R.M.; Giri, A.P. Structural, functional and evolutionary diversity of 4-coumarate-CoA ligase in plants. Planta 2018, 248, 1063–1078. [Google Scholar] [CrossRef]
- Fritzemeier, K.; Cretin, C.; Kombrink, E.; Rohwer, F.; Taylor, J.; Scheel, D.; Hahlbrock, K. Transient induction of phenylalanine ammonia-lyase and 4-coumarate: CoA ligase mRNAs in potato leaves infected with virulent or avirulent races of Phytophthora infestans. Plant Physiol. 1987, 85, 34–41. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Becker-Andre, M.; Schulze-Lefert, P.; Hahlbrock, K. Structural comparison, modes of expression, and putative cis-acting elements of the two 4-coumarate: CoA ligase genes in potato. J. Biol. Chem. 1991, 266, 8551–8559. [Google Scholar] [CrossRef] [PubMed]
- Song, Z.; Yang, Q.; Dong, B.; Li, N.; Wang, M.; Du, T.; Liu, N.; Niu, L.; Jin, H.; Meng, D. Melatonin enhances plant stress tolerance by promoting flavonoid enrichment, focusing on luteolin for salt stress. J. Exp. Bot. 2022, 73, 5992–6008. [Google Scholar] [CrossRef]
- Pham, G.M.; Hamilton, J.P.; Wood, J.C.; Burke, J.T.; Zhao, H.; Vaillancourt, B.; Ou, S.; Jiang, J.; Buell, C.R. Construction of a chromosome-scale long-read reference genome assembly for potato. GigaScience 2020, 9, a100. [Google Scholar] [CrossRef]
- Mo, F.; Li, L.; Zhang, C.; Yang, C.; Chen, G.; Niu, Y.; Si, J.; Liu, T.; Sun, X.; Wang, S. Genome-wide analysis and expression profiling of the phenylalanine ammonia-lyase gene family in Solanum tuberosum. Int. J. Mol. Sci. 2022, 23, 6833. [Google Scholar] [CrossRef]
- Zhao, P.; Ye, M.; Wang, R.; Wang, D.; Chen, Q. Systematic identification and functional analysis of potato (Solanum tuberosum L.) bZIP transcription factors and overexpression of potato bZIP transcription factor StbZIP-65 enhances salt tolerance. Int. J. Biol. Macromol. 2020, 161, 155–167. [Google Scholar] [CrossRef]
- Matringe, M.; Camadro, J.M.; Labbe, P.; Scalla, R. Protoporphyrinogen oxidase as a molecular target for diphenyl ether herbicides. Biochem. J. 1989, 260, 231–235. [Google Scholar] [CrossRef] [PubMed]
- Ma, X.; Xu, Y.; Zhao, H.; Huo, Z.; Wang, S.; Zhong, F. Identification of Tomato 4CL Gene Family and Expression Analysis under Nitrogen Treatment. Biotechnol. Bull. 2022, 38, 163. [Google Scholar]
- Yamaguchi-Shinozaki, K.; Shinozaki, K. Organization of cis-acting regulatory elements in osmotic-and cold-stress-responsive promoters. Trends Plant Sci. 2005, 10, 88–94. [Google Scholar] [CrossRef] [PubMed]
- Yoshida, T.; Fujita, Y.; Sayama, H.; Kidokoro, S.; Maruyama, K.; Mizoi, J.; Shinozaki, K.; Yamaguchi Shinozaki, K. AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J. 2010, 61, 672–685. [Google Scholar] [CrossRef]
- Zhao, S.; Ye, Z.; Stanton, R. Misuse of RPKM or TPM normalization when comparing across samples and sequencing protocols. RNA 2020, 26, 903–909. [Google Scholar] [CrossRef] [Green Version]
- Szklarczyk, D.; Gable, A.L.; Nastou, K.C.; Lyon, D.; Kirsch, R.; Pyysalo, S.; Doncheva, N.T.; Legeay, M.; Fang, T.; Bork, P. The STRING database in 2021: Customizable protein–protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Res. 2021, 49, D605–D612. [Google Scholar] [CrossRef]
- Szklarczyk, D.; Morris, J.H.; Cook, H.; Kuhn, M.; Wyder, S.; Simonovic, M.; Santos, A.; Doncheva, N.T.; Roth, A.; Bork, P. The STRING database in 2017: Quality-controlled protein—Protein association networks, made broadly accessible. Nucleic Acids Res. 2016, 45, 362–368. [Google Scholar] [CrossRef]
- Soubeyrand, E.; Johnson, T.S.; Latimer, S.; Block, A.; Kim, J.; Colquhoun, T.A.; Butelli, E.; Martin, C.; Wilson, M.A.; Basset, G.J. The peroxidative cleavage of kaempferol contributes to the biosynthesis of the benzenoid moiety of ubiquinone in plants. Plant Cell 2018, 30, 2910–2921. [Google Scholar] [CrossRef] [Green Version]
- Merzlyak, M.N.; Chivkunova, O.B. Light-stress-induced pigment changes and evidence for anthocyanin photoprotection in apples. J. Photochem. Photobiol. B Biol. 2000, 55, 155–163. [Google Scholar] [CrossRef]
- Crissa, D.; Weibing, S.; Peng, G.; Xiaohan, Y.; Xia, Y.; Xin, Z.; Jun, H.; Dandan, Z.; Zhanyou, X.; Nicole, L. Comparative genome analysis of lignin biosynthesis gene families across the plant kingdom. BMC Bioinform. 2009, 10, S3. [Google Scholar]
- Cukovic, D.; Ehlting, J.; VanZiffle, J.A.; Douglas, C.J. Structure and evolution of 4-coumarate: Coenzyme A ligase (4CL) gene families. Biol. Chem. 2001, 382, 645–654. [Google Scholar]
- Feng, X.; Wang, Y.; Zhang, N.; Gao, S.; Wu, J.; Liu, R.; Huang, Y.; Zhang, J.; Qi, Y. Comparative phylogenetic analysis of CBL reveals the gene family evolution and functional divergence in Saccharum spontaneum. BMC Plant Biol. 2021, 21, 395. [Google Scholar] [CrossRef]
- Lu, Y.; Zhao, P.; Zhang, A.; Wang, J.; Ha, M. Genome-Wide Analysis of HSP70s in Hexaploid Wheat: Tandem Duplication, Heat Response, and Regulation. Cells 2022, 11, 818. [Google Scholar] [CrossRef]
- Liu, Y.; Bahar, I. Sequence evolution correlates with structural dynamics. Mol. Biol. Evol. 2012, 29, 2253–2263. [Google Scholar] [CrossRef] [Green Version]
- Soltani, B.M.; Ehlting, J.; Hamberger, B.; Douglas, C.J. Multiple cis-regulatory elements regulate distinct and complex patterns of developmental and wound-induced expression of Arabidopsis thaliana 4CL gene family members. Planta 2006, 224, 1226–1238. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Guo, C.; Peng, J.; Li, C.; Wan, F.; Zhang, S.; Zhou, Y.; Yan, Y.; Qi, L.; Sun, K. ABRE-binding factors play a role in the feedback regulation of ABA signaling by mediating rapid ABA induction of ABA co-receptor genes. New Phytol. 2019, 221, 341–355. [Google Scholar] [CrossRef] [Green Version]
- Jin, X.; Xiong, A.; Peng, R.; Liu, J.; Gao, F.; Chen, J.; Yao, Q. OsAREB1, an ABRE-binding protein responding to ABA and glucose, has multiple functions in Arabidopsis. BMB Rep. 2010, 43, 34–39. [Google Scholar] [CrossRef]
- Leng, P.; Zhao, J. Transcription factors as molecular switches to regulate drought adaptation in maize. Theor. Appl. Genet. 2020, 133, 1455–1465. [Google Scholar] [CrossRef] [PubMed]
- Kianersi, F.; Abdollahi, M.R.; Mirzaie-Asl, A.; Dastan, D.; Rasheed, F. Identification and tissue-specific expression of rutin biosynthetic pathway genes in Capparis spinosa elicited with salicylic acid and methyl jasmonate. Sci. Rep. 2020, 10, 8884. [Google Scholar] [CrossRef] [PubMed]
- Awasthi, P.; Mahajan, V.; Jamwal, V.L.; Chouhan, R.; Kapoor, N.; Bedi, Y.S.; Gandhi, S.G. Characterization of the gene encoding 4-coumarate: CoA ligase in Coleus forskohlii. J. Plant Biochem. Biotechnol. 2019, 28, 203–210. [Google Scholar] [CrossRef]
- Sharma, A.; Shahzad, B.; Rehman, A.; Bhardwaj, R.; Landi, M.; Zheng, B. Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. Molecules 2019, 24, 2452. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Das, K.; Roychoudhury, A. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front. Environ. Sci. 2014, 2, 53. [Google Scholar] [CrossRef] [Green Version]
- Zhang, L.; Xing, D. Methyl jasmonate induces production of reactive oxygen species and alterations in mitochondrial dynamics that precede photosynthetic dysfunction and subsequent cell death. Plant Cell Physiol. 2008, 49, 1092–1111. [Google Scholar] [CrossRef] [Green Version]
- Huang, H.; Ullah, F.; Zhou, D.; Yi, M.; Zhao, Y. Mechanisms of ROS regulation of plant development and stress responses. Front. Plant Sci. 2019, 10, 800. [Google Scholar] [CrossRef] [PubMed]
- Agati, G.; Azzarello, E.; Pollastri, S.; Tattini, M. Flavonoids as antioxidants in plants: Location and functional significance. Plant Sci. 2012, 196, 67–76. [Google Scholar] [CrossRef]
- Gururani, M.A.; Upadhyaya, C.P.; Baskar, V.; Venkatesh, J.; Nookaraju, A.; Park, S.W. Plant growth-promoting rhizobacteria enhance abiotic stress tolerance in Solanum tuberosum through inducing changes in the expression of ROS-scavenging enzymes and improved photosynthetic performance. J. Plant Growth Regul. 2013, 32, 245–258. [Google Scholar] [CrossRef]
- Chen, X.; Su, W.; Zhang, H.; Zhan, Y.; Zeng, F. Fraxinus mandshurica 4-coumarate-CoA ligase 2 enhances drought and osmotic stress tolerance of tobacco by increasing coniferyl alcohol content. Plant Physiol. Biochem. 2020, 155, 697–708. [Google Scholar] [CrossRef]
- Zhao, D.; Luan, Y.; Shi, W.; Zhang, X.; Meng, J.; Tao, J. A Paeonia ostii caffeoyl-CoA O-methyltransferase confers drought stress tolerance by promoting lignin synthesis and ROS scavenging. Plant Sci. 2021, 303, 110765. [Google Scholar] [CrossRef]
- Zhong, J.; Qing, J.; Wang, Q.; Liu, C.; Du, H.; Liu, P.; Du, Q.; Du, L.; Wang, L. Genome-Wide Identification and Expression Analyses of the 4-Coumarate: CoA Ligase (4CL) Gene Family in Eucommia ulmoides. Forests 2022, 13, 1253. [Google Scholar] [CrossRef]
- Liu, T.; Yao, R.; Zhao, Y.; Xu, S.; Huang, C.; Luo, J.; Kong, L. Cloning, functional characterization and site-directed mutagenesis of 4-coumarate: Coenzyme A ligase (4CL) involved in coumarin biosynthesis in Peucedanum praeruptorum Dunn. Front. Plant Sci. 2017, 8, 4. [Google Scholar] [CrossRef] [Green Version]
- Song, C.; Li, X.; Jia, B.; Liu, L.; Ou, J.; Han, B. De novo transcriptome sequencing coupled with co-expression analysis reveal the transcriptional regulation of key genes involved in the formation of active ingredients in Peucedanum praeruptorum Dunn under bolting period. Front. Genet. 2021, 12, 683037. [Google Scholar] [CrossRef]
- Lee, D.; Ellard, M.; Wanner, L.A.; Davis, K.R.; Douglas, C.J. The Arabidopsis thaliana 4-coumarate: CoA ligase (4CL) gene: Stress and developmentally regulated expression and nucleotide sequence of its cDNA. Plant Mol. Biol. 1995, 28, 871–884. [Google Scholar] [CrossRef] [PubMed]
- Sun, S.; Xiong, X.; Zhang, X.; Feng, H.; Zhu, Q.; Sun, J.; Li, Y. Characterization of the Gh4CL gene family reveals a role of Gh4CL7 in drought tolerance. BMC Plant Biol. 2020, 20, 125. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Andersen, J.R.; Zein, I.; Wenzel, G.; Darnhofer, B.; Eder, J.; Ouzunova, M.; Lübberstedt, T. Characterization of phenylpropanoid pathway genes within European maize (Zea mays L.) inbreds. BMC Plant Biol. 2008, 8, 2. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, D.; Douglas, C.J. Two divergent members of a tobacco 4-coumarate: Coenzyme A ligase (4CL) gene family (cDNA structure, gene inheritance and expression, and properties of recombinant proteins). Plant Physiol. 1996, 112, 193–205. [Google Scholar] [CrossRef]
- Wang, C.; Yu, J.; Cai, Y.; Zhu, P.; Liu, C.; Zhao, A.; Lü, R.; Li, M.; Xu, F.; Yu, M. Characterization and functional analysis of 4-coumarate: CoA ligase genes in mulberry. PLoS ONE 2016, 11, e155814. [Google Scholar]
- Nguyen, T.; Son, S.; Jordan, M.C.; Levin, D.B.; Ayele, B.T. Lignin biosynthesis in wheat (Triticum aestivum L.): Its response to waterlogging and association with hormonal levels. BMC Plant Biol. 2016, 16, 28. [Google Scholar] [CrossRef] [Green Version]
- Kumar, S.; Nei, M.; Dudley, J.; Tamura, K. MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief. Bioinform. 2008, 9, 299–306. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, C.; Chen, H.; Zhang, Y.; Thomas, H.R.; Frank, M.H.; He, Y.; Xia, R. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Mol. Plant. 2020, 13, 1194–1202. [Google Scholar] [CrossRef]
- Xu, D.; Lu, Z.; Jin, K.; Qiu, W.; Qiao, G.; Han, X.; Zhuo, R. SPDE: A multi-functional software for sequence processing and data extraction. Bioinformatics 2021, 37, 3686–3687. [Google Scholar] [CrossRef]
- Nan, Y.; Xie, Y.; Atif, A.; Wang, X.; Zhang, Y.; Tian, H.; Gao, Y. Identification and Expression Analysis of SLAC/SLAH Gene Family in Brassica napus L. Int. J. Mol. Sci. 2021, 22, 4671. [Google Scholar] [CrossRef]
- Morita, K.; Wang, F.; Jahn, K.; Hu, T.; Tanaka, T.; Sasaki, Y.; Kuipers, J.; Loghavi, S.; Wang, S.A.; Yan, Y. Clonal evolution of acute myeloid leukemia revealed by high-throughput single-cell genomics. Nat. Commun. 2020, 11, 5327. [Google Scholar] [CrossRef]
- Ding, H.; Blair, A.; Yang, Y.; Stuart, J.M. Biological process activity transformation of single cell gene expression for cross-species alignment. Nat. Commun. 2019, 10, 4899. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Deng, W.; Wang, Y.; Liu, Z.; Cheng, H.; Xue, Y. HemI: A toolkit for illustrating heatmaps. PLoS ONE 2014, 9, e111988. [Google Scholar] [CrossRef]
- Smoot, M.E.; Ono, K.; Ruscheinski, J.; Wang, P.; Ideker, T. Cytoscape 2.8: New features for data integration and network visualization. Bioinformatics 2011, 27, 431–432. [Google Scholar] [CrossRef] [Green Version]
- Feng, D.; Wang, Y.; Wu, J.; Lu, T.; Zhang, Z. Development and drought tolerance assay of marker-free transgenic rice with OsAPX2 using biolistic particle-mediated co-transformation. Crop J. 2017, 5, 271–281. [Google Scholar] [CrossRef]
- Huh, S.U. Optimization of immune receptor-related hypersensitive cell death response assay using agrobacterium-mediated transient expression in tobacco plants. Plant Methods 2022, 18, 57. [Google Scholar] [CrossRef] [PubMed]
Gene | Gene ID | CDS Length (bp) | No. of Exons | Protein | Subcellular Localization | ||
---|---|---|---|---|---|---|---|
Length (aa) | MW (Da) | pI | |||||
St4CL1 | Soltu.DM.02G004660 | 1659 | 1 | 552 | 61,037.47 | 7.55 | Organelle membrane |
St4CL2 | Soltu.DM.02G004670 | 1656 | 1 | 551 | 60,841.01 | 7.29 | Plasma membrane |
St4CL3 | Soltu.DM.02G020860 | 1728 | 2 | 575 | 64,250.28 | 8.16 | Plasma membrane |
St4CL4 | Soltu.DM.02G020870 | 1710 | 2 | 570 | 63,664.47 | 7.24 | Organelle membrane |
St4CL5 | Soltu.DM.03G003110 | 1851 | 3 | 616 | 68,009.17 | 7.14 | Plasma membrane |
St4CL6 | Soltu.DM.03G020790 | 1710 | 6 | 569 | 61,825.23 | 5.53 | Organelle membrane |
St4CL7 | Soltu.DM.03G032090 | 1638 | 5 | 545 | 59,636.17 | 5.49 | Plasma membrane |
St4CL8 | Soltu.DM.06G000670 | 1647 | 2 | 548 | 60,436.68 | 8.21 | Organelle membrane |
St4CL9 | Soltu.DM.06G024540 | 1647 | 6 | 548 | 60,099.43 | 5.43 | Organelle membrane |
St4CL10 | Soltu.DM.12G011270 | 1647 | 6 | 548 | 60,157.6 | 5.36 | Plasma membrane |
Motif | Length | Amino Acid Sequence |
---|---|---|
Motif 1 | 50 | EGWLHTGDJGYIDDDGYLYIVDRLKELIKYKGFQVAPAELEALLLSHPEI |
Motif 2 | 29 | SEDDPAALPYSSGTTGLPKGVVLTHRNLV |
Motif 3 | 29 | NTMGEICLRGPQIMKGYLNBPEATSKTID |
Motif 4 | 29 | DAAVVPMPDEZAGEVPVAFVVRSNGSTJT |
Motif 5 | 23 | EDEIIDFIAKQVPPYKRIKRVIF |
Motif 6 | 41 | YDLSSLRSVMSGAAPLGKELEEAFRKKFPNAKLGQGYGMTE |
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Nie, T.; Sun, X.; Wang, S.; Wang, D.; Ren, Y.; Chen, Q. Genome-Wide Identification and Expression Analysis of the 4-Coumarate: CoA Ligase Gene Family in Solanum tuberosum. Int. J. Mol. Sci. 2023, 24, 1642. https://doi.org/10.3390/ijms24021642
Nie T, Sun X, Wang S, Wang D, Ren Y, Chen Q. Genome-Wide Identification and Expression Analysis of the 4-Coumarate: CoA Ligase Gene Family in Solanum tuberosum. International Journal of Molecular Sciences. 2023; 24(2):1642. https://doi.org/10.3390/ijms24021642
Chicago/Turabian StyleNie, Tengkun, Xinxin Sun, Shenglan Wang, Dongdong Wang, Yamei Ren, and Qin Chen. 2023. "Genome-Wide Identification and Expression Analysis of the 4-Coumarate: CoA Ligase Gene Family in Solanum tuberosum" International Journal of Molecular Sciences 24, no. 2: 1642. https://doi.org/10.3390/ijms24021642
APA StyleNie, T., Sun, X., Wang, S., Wang, D., Ren, Y., & Chen, Q. (2023). Genome-Wide Identification and Expression Analysis of the 4-Coumarate: CoA Ligase Gene Family in Solanum tuberosum. International Journal of Molecular Sciences, 24(2), 1642. https://doi.org/10.3390/ijms24021642