Comprehensive Genome-Wide Analyses of Poplar R2R3-MYB Transcription Factors and Tissue-Specific Expression Patterns under Drought Stress
Abstract
:1. Introduction
2. Results
2.1. Identification and Characterization of Poplar R2R3-MYB Gene Family Members and Their Chromosomal Distribution
2.2. Physicochemical Property Analysis of Poplar R2R3-MYB Proteins
2.3. Analysis of Cis-Acting Elements in R2R3-MYB Genes
2.4. Phylogenetic Analysis of the Poplar R2R3-MYB Gene Family
2.5. Collinearity Analysis of R2R3-MYB Genes
2.6. Poplar R2R3-MYB Gene RNA-Seq Analysis
2.7. PdMYB2R Gene Cloning and the Expression Patterns of PdMYB2R Genes in Different Tissues
2.8. Analysis of the Expression Pattern of Poplar PdMYB2R Genes under Drought Stress
2.9. Subcellular Localization and Transcriptional Activation Activity
3. Discussion
3.1. Identification and Evolution of the Poplar R2R3-MYB Gene Family
3.2. Analysis of Functional Sites of Poplar R2R3-MYB Proteins
3.3. Tissue-Specific Expression Pattern of Poplar R2R3-MYB Genes under Drought Stress
4. Materials and Methods
4.1. Genomic Data Retrieval
4.2. Identification of R2R3-MYB Transcription Factors in Poplar
4.3. Chromosomal Location, Physicochemical Properties and Cis-Acting Element Analysis of R2R3-MYB Genes in Poplar
4.4. Multiple Sequence Alignment and Phylogenetic Analysis
4.5. PtrMYB2R Gene Expression Analysis
4.6. Genome Collinearity Analysis
4.7. Cloning of R2R3-MYB Genes from NL895 Poplar
4.8. Expression Pattern of R2R3 MYB Genes in Poplar NL895 under Drought Stress
4.9. Subcellular Localization of the R2R3-MYB Transcription Factor in Poplar
4.10. Transcriptional Activation Assay
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Haberstroh, S.; Werner, C. The role of species interactions for forest resilience to drought. Plant Biol. 2022, 24, 1098–1107. [Google Scholar] [CrossRef]
- Salmon, Y.; Dietrich, L.; Sevanto, S.; Hölttä, T.; Dannoura, M.; Epron, D. Drought impacts on tree phloem: From cell-level responses to ecological significance. Tree Physiol. 2019, 39, 173–191. [Google Scholar] [CrossRef] [Green Version]
- Qiu, J. China faces up to groundwater crisis. Nature 2010, 466, 308. [Google Scholar] [CrossRef] [Green Version]
- Wu, K.; Qu, Y.; Rong, H.; Han, X.; Tian, Y.; Xu, L. Identification and Expression Analysis of the Populus trichocarpa GASA-Gene Family. Int. J. Mol. Sci. 2022, 23, 1507. [Google Scholar] [CrossRef]
- Tuskan, G.A.; Difazio, S.; Jansson, S.; Bohlmann, J.; Grigoriev, I.; Hellsten, U.; Putnam, N.; Ralph, S.; Rombauts, S.; Salamov, A.; et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 2006, 313, 1596–1604. [Google Scholar]
- Ma, J.; Wan, D.; Duan, B.; Bai, X.; Bai, Q.; Chen, N.; Ma, T. Genome sequence and genetic transformation of a widely distributed and cultivated poplar. Plant Biotechnol. J. 2019, 17, 451–460. [Google Scholar] [CrossRef] [Green Version]
- Yao, T.; Zhang, J.; Xie, M.; Yuan, G.; Tschaplinski, T.J.; Muchero, W.; Chen, J.G. Transcriptional Regulation of Drought Response in Arabidopsis and Woody Plants. Front. Plant Sci. 2020, 11, 572137. [Google Scholar] [CrossRef] [PubMed]
- Roy, S. Function of MYB domain transcription factors in abiotic stress and epigenetic control of stress response in plant genome. Plant Signal Behav. 2016, 11, e1117723. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Z.; Zhang, L.; Liu, Y.; Shang, X.; Fang, S. Identification and Expression Analysis of R2R3-MYB Family Genes Associated with Salt Tolerance in Cyclocarya paliurus. Int. J. Mol. Sci. 2022, 23, 3429. [Google Scholar] [CrossRef] [PubMed]
- Wilkins, O.; Nahal, H.; Foong, J.; Provart, N.J.; Campbell, M.M. Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiol. 2009, 149, 981–993. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, Y.; Wen, J.; Xia, Y.; Zhang, L.; Du, H. Evolution and functional diversification of R2R3-MYB transcription factors in plants. Hortic. Res. 2022, 9, uhac058. [Google Scholar] [CrossRef] [PubMed]
- Lee, S.B.; Suh, M.C. Cuticular wax biosynthesis is up-regulated by the MYB94 transcription factor in Arabidopsis. Plant Cell Physiol. 2015, 56, 48–60. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Seo, P.J.; Lee, S.B.; Suh, M.C.; Park, M.J.; Go, Y.S.; Park, C.M. The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell 2011, 23, 1138–1152. [Google Scholar] [CrossRef] [Green Version]
- Jung, C.; Seo, J.S.; Han, S.W.; Koo, Y.J.; Kim, C.H.; Song, S.I.; Nahm, B.H.; Choi, Y.D.; Cheong, J.J. Overexpression of AtMYB44 enhances stomatal closure to confer abiotic stress tolerance in transgenic Arabidopsis. Plant Physiol. 2008, 146, 623–635. [Google Scholar] [CrossRef] [Green Version]
- Nguyen, N.H.; Cheong, J.J. AtMYB44 interacts with TOPLESS-RELATED corepressors to suppress protein phosphatase 2C gene transcription. Biochem. Biophys. Res. Commun. 2018, 507, 437–442. [Google Scholar] [CrossRef]
- Fang, Q.; Wang, X.; Wang, H.; Tang, X.; Liu, C.; Yin, H.; Ye, S.; Jiang, Y.; Duan, Y.; Luo, K. The poplar R2R3 MYB transcription factor PtrMYB94 coordinates with abscisic acid signaling to improve drought tolerance in plants. Tree Physiol. 2020, 40, 46–59. [Google Scholar] [CrossRef]
- Xu, C.; Fu, X.; Liu, R.; Guo, L.; Ran, L.; Li, C.; Tian, Q.; Jiao, B.; Wang, B.; Luo, K. PtoMYB170 positively regulates lignin deposition during wood formation in poplar and confers drought tolerance in transgenic Arabidopsis. Tree Physiol. 2017, 37, 1713–1726. [Google Scholar] [CrossRef] [Green Version]
- Song, Q.; Kong, L.; Yang, X.; Jiao, B.; Hu, J.; Zhang, Z.; Xu, C.; Luo, K. PtoMYB142, a poplar R2R3-MYB transcription factor, contributes to drought tolerance by regulating wax biosynthesis. Tree Physiol. 2022, 42, 2133–2147. [Google Scholar] [CrossRef]
- Stracke, R.; Werber, M.; Weisshaar, B. The R2R3-MYB gene family in Arabidopsis thaliana. Curr. Opin. Plant Biol. 2001, 4, 447–456. [Google Scholar] [CrossRef]
- Matus, J.T.; Aquea, F.; Arce-Johnson, P. Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biol. 2008, 8, 83. [Google Scholar] [CrossRef] [Green Version]
- Soler, M.; Camargo, E.L.; Carocha, V.; Cassan-Wang, H.; San Clemente, H.; Savelli, B.; Hefer, C.A.; Paiva, J.A.; Myburg, A.A.; Grima-Pettenati, J. The Eucalyptus grandis R2R3-MYB transcription factor family: Evidence for woody growth-related evolution and function. New Phytol. 2015, 206, 1364–1377. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.; Liu, Y.; Tang, B.; Dai, X.; Xie, L.; Liu, F.; Zou, X. Genome-Wide Identification and Capsaicinoid Biosynthesis-Related Expression Analysis of the R2R3-MYB Gene Family in Capsicum annuum L. Front. Genet. 2020, 11, 598183. [Google Scholar] [CrossRef] [PubMed]
- Lou, X.; Yao, S.; Chen, P.; Wang, D.; Agassin, R.H.; Hou, Y.; Zhang, C.; Ji, K. Transcriptome Identification of R2R3-MYB Gene Family Members in Pinus massoniana and PmMYB4 Response to Drought Stress. Forests 2023, 14, 410. [Google Scholar] [CrossRef]
- Yin, Y.; Guo, C.; Shi, H.; Zhao, J.; Ma, F.; An, W.; He, X.; Luo, Q.; Cao, Y.; Zhan, X. Genome-Wide Comparative Analysis of the R2R3-MYB Gene Family in Five Solanaceae Species and Identification of Members Regulating Carotenoid Biosynthesis in Wolfberry. Int. J. Mol. Sci. 2022, 23, 2259. [Google Scholar] [CrossRef] [PubMed]
- Chai, G.; Wang, Z.; Tang, X.; Yu, L.; Qi, G.; Wang, D.; Yan, X.; Kong, Y.; Zhou, G. R2R3-MYB gene pairs in Populus: Evolution and contribution to secondary wall formation and flowering time. J. Exp. Bot. 2014, 65, 4255–4269. [Google Scholar] [CrossRef] [Green Version]
- Zhao, K.; Cheng, Z.; Guo, Q.; Yao, W.; Liu, H.; Zhou, B.; Jiang, T. Characterization of the Poplar R2R3-MYB Gene Family and Over-Expression of PsnMYB108 Confers Salt Tolerance in Transgenic Tobacco. Front. Plant Sci. 2020, 11, 571881. [Google Scholar] [CrossRef]
- Yang, X.; Li, J.; Guo, T.; Guo, B.; Chen, Z.; An, X. Comprehensive analysis of the R2R3-MYB transcription factor gene family in Populus trichocarpa. Ind. Crops Prod. 2021, 168, 7. [Google Scholar] [CrossRef]
- Zhou, F.; Chen, Y.; Wu, H.; Yin, T. Genome-Wide Comparative Analysis of R2R3 MYB Gene Family in Populus and Salix and Identification of Male Flower Bud Development-Related Genes. Front. Plant Sci. 2021, 12, 721558. [Google Scholar] [CrossRef]
- Singh, P.; Mukhopadhyay, K. Comprehensive molecular dissection of TIFY Transcription factors reveal their dynamic responses to biotic and abiotic stress in wheat (Triticum aestivum L.). Sci. Rep. 2021, 11, 9739. [Google Scholar] [CrossRef]
- Zeng, D.; Dai, L.J.; Li, X.; Li, W.; Qu, G.Z.; Li, S. Genome-Wide Identification of the ERF Transcription Factor Family for Structure Analysis, Expression Pattern, and Response to Drought Stress in Populus alba × Populus glandulosa. Int. J. Mol. Sci. 2023, 24, 3697. [Google Scholar] [CrossRef]
- Zhang, H.; Jiang, W.; Xia, P.; Yin, J.; Chen, H.; Li, W.; Ma, D. Genome-Wide Identification Transcriptional Expression Analysis of E2F-DP Transcription Factor Family in Wheat. Plant Mol. Biol. Report. 2022, 40, 339–358. [Google Scholar] [CrossRef]
- Kim, J.S.; Mizoi, J.; Yoshida, T.; Fujita, Y.; Nakajima, J.; Ohori, T.; Todaka, D.; Nakashima, K.; Hirayama, T.; Shinozaki, K.; et al. An ABRE promoter sequence is involved in osmotic stress-responsive expression of the DREB2A gene, which encodes a transcription factor regulating drought-inducible genes in Arabidopsis. Plant Cell Physiol. 2011, 52, 2136–2146. [Google Scholar] [CrossRef] [Green Version]
- Seidl, V.; Seiboth, B.; Karaffa, L.; Kubicek, C.P. The fungal STRE-element-binding protein Seb1 is involved but not essential for glycerol dehydrogenase (gld1) gene expression and glycerol accumulation in Trichoderma atroviride during osmotic stress. Fungal Genet. Biol. 2004, 41, 1132–1140. [Google Scholar] [CrossRef]
- Liang, J.; Zhang, H.; Yi, L.; Tang, Y.; Long, H.; Yu, M.; Deng, G. Identification of HvLRX, a new dehydration and light responsive gene in Tibetan hulless barley (Hordeum vulgare var. nudum). Genes Genom. 2021, 43, 1445–1461. [Google Scholar] [CrossRef] [PubMed]
- Yousefi, M. Survey of Promoters Cis-elements and Genes Co- expression of Oxidative Defense Pathway in Arabidopsis thaliana L. Plant. Int. J. Agric. Crop Sci. 2012, 4, 1021–1025. [Google Scholar]
- Goldsbrough, A.P.; Albrecht, H.; Stratford, R. Salicylic acid-inducible binding of a tobacco nuclear protein to a 10 bp sequence which is highly conserved amongst stress-inducible genes. Plant J. 1993, 3, 563–571. [Google Scholar] [CrossRef] [PubMed]
- Jiang, C.K.; Rao, G.Y. Insights into the Diversification and Evolution of R2R3-MYB Transcription Factors in Plants. Plant Physiol. 2020, 183, 637–655. [Google Scholar] [CrossRef] [PubMed]
- Millard, P.S.; Kragelund, B.B.; Burow, M. R2R3 MYB Transcription Factors—Functions outside the DNA-Binding Domain. Trends Plant Sci. 2019, 24, 934–946. [Google Scholar] [CrossRef] [PubMed]
- Cui, L.; Wall, P.K.; Leebens-Mack, J.H.; Lindsay, B.G.; Soltis, D.E.; Doyle, J.J.; Soltis, P.S.; Carlson, J.E.; Arumuganathan, K.; Barakat, A.; et al. Widespread genome duplications throughout the history of flowering plants. Genome Res. 2006, 16, 738–749. [Google Scholar] [CrossRef] [Green Version]
- Berlin, S.; Lagercrantz, U.; von Arnold, S.; Ost, T.; Rönnberg-Wästljung, A.C. High-density linkage mapping and evolution of paralogs and orthologs in Salix and Populus. BMC Genom. 2010, 11, 129. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fang, Y.; Xiong, L. General mechanisms of drought response and their application in drought resistance improvement in plants. Cell Mol. Life Sci. 2015, 72, 673–689. [Google Scholar] [CrossRef]
- Chen, Y.; Yang, X.; He, K.; Liu, M.; Li, J.; Gao, Z.; Lin, Z.; Zhang, Y.; Wang, X.; Qiu, X.; et al. The MYB transcription factor superfamily of Arabidopsis: Expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol. Biol. 2006, 60, 107–124. [Google Scholar] [CrossRef] [PubMed]
- González, M.; Carrasco, B.; Salazar, E. Genome-wide identification and characterization of R2R3MYB family in Rosaceae. Genom. Data 2016, 9, 50–57. [Google Scholar] [CrossRef] [Green Version]
- Luan, X.; Xu, W.; Zhang, J.; Shen, T.; Chen, C.; Xi, M.; Zhong, Y.; Xu, M. Genome-Scale Identification, Classification, and Expression Profiling of MYB Transcription Factor Genes in Cinnamomum camphora. Int. J. Mol. Sci. 2022, 23, 14279. [Google Scholar] [CrossRef]
- Chen, X.; Wang, P.; Gu, M.; Lin, X.; Hou, B.; Zheng, Y.; Sun, Y.; Jin, S.; Ye, N. R2R3-MYB transcription factor family in tea plant (Camellia sinensis): Genome-wide characterization, phylogeny, chromosome location, structure and expression patterns. Genomics 2021, 113, 1565–1578. [Google Scholar] [CrossRef]
- Peng, X.; Liu, H.; Wang, D.; Shen, S. Genome-wide identification of the Jatropha curcas MYB family and functional analysis of the abiotic stress responsive gene JcMYB2. BMC Genom. 2016, 17, 251. [Google Scholar] [CrossRef] [Green Version]
- Yang, X.; Guo, T.; Li, J.; Chen, Z.; Guo, B.; An, X. Genome-wide analysis of the MYB-related transcription factor family and associated responses to abiotic stressors in Populus. Int. J. Biol. Macromol. 2021, 191, 359–376. [Google Scholar] [CrossRef] [PubMed]
- Wu, W.; Zhu, S.; Zhu, L.; Wang, D.; Liu, Y.; Liu, S.; Zhang, J.; Hao, Z.; Lu, Y.; Cheng, T.; et al. Characterization of the Liriodendron Chinense MYB Gene Family and Its Role in Abiotic Stress Response. Front. Plant Sci. 2021, 12, 641280. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Lin-Wang, K.; Liu, Z.; Allan, A.C.; Qin, S.; Zhang, J.; Liu, Y. Genome-wide analysis and expression profiles of the StR2R3-MYB transcription factor superfamily in potato (Solanum tuberosum L.). Int. J. Biol. Macromol. 2020, 148, 817–832. [Google Scholar] [CrossRef]
- Wei, Q.; Chen, R.; Wei, X.; Liu, Y.; Zhao, S.; Yin, X.; Xie, T. Genome-wide identification of R2R3-MYB family in wheat and functional characteristics of the abiotic stress responsive gene TaMYB344. BMC Genom. 2020, 21, 792. [Google Scholar] [CrossRef]
- Oh, I.H.; Reddy, E.P. The myb gene family in cell growth, differentiation and apoptosis. Oncogene 1999, 18, 3017–3033. [Google Scholar] [CrossRef] [Green Version]
- 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] [PubMed]
- Smita, S.; Katiyar, A.; Chinnusamy, V.; Pandey, D.M.; Bansal, K.C. Transcriptional Regulatory Network Analysis of MYB Transcription Factor Family Genes in Rice. Front. Plant Sci. 2015, 6, 1157. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ramalingam, A.; Kudapa, H.; Pazhamala, L.T.; Garg, V.; Varshney, R.K. Gene Expression and Yeast Two-Hybrid Studies of 1R-MYB Transcription Factor Mediating Drought Stress Response in Chickpea (Cicer arietinum L.). Front. Plant Sci. 2015, 6, 1117. [Google Scholar] [CrossRef] [Green Version]
- Zhang, X.L.; Chen, Y.; Huang, M.R.; Zhu, S. Research progress on drought-responsive transcription factors of Populus. J. Northwest A & F Univ. (Nat. Sci. Ed. ) 2023, 51, 2–14. [Google Scholar]
- Qu, X.; Zou, J.; Wang, J.; Yang, K.; Wang, X.; Le, J. A Rice R2R3-Type MYB Transcription Factor OsFLP Positively Regulates Drought Stress Response via OsNAC. Int. J. Mol. Sci. 2022, 23, 5873. [Google Scholar] [CrossRef]
- Davidson, E.H.; Rast, J.P.; Oliveri, P.; Ransick, A.; Calestani, C.; Yuh, C.H.; Minokawa, T.; Amore, G.; Hinman, V.; Arenas-Mena, C.; et al. A provisional regulatory gene network for specification of endomesoderm in the sea urchin embryo. Dev. Biol. 2002, 246, 162–190. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Otim, O. An empirical model of Onecut binding activity at the sea urchin SM50 C-element gene regulatory region. Int. J. Dev. Biol. 2017, 61, 537–543. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dubos, C.; Stracke, R.; Grotewold, E.; Weisshaar, B.; Martin, C.; Lepiniec, L. MYB transcription factors in Arabidopsis. Trends Plant Sci. 2010, 15, 573–581. [Google Scholar] [CrossRef]
- Katiyar, A.; Smita, S.; Lenka, S.K.; Rajwanshi, R.; Chinnusamy, V.; Bansal, K.C. Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC Genom. 2012, 13, 544. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liang, Y.K.; Dubos, C.; Dodd, I.C.; Holroyd, G.H.; Hetherington, A.M.; Campbell, M.M. AtMYB61, an R2R3-MYB transcription factor controlling stomatal aperture in Arabidopsis thaliana. Curr. Biol. 2005, 15, 1201–1206. [Google Scholar] [CrossRef] [Green Version]
- Kim, J.H.; Nguyen, N.H.; Jeong, C.Y.; Nguyen, N.T.; Hong, S.W.; Lee, H. Loss of the R2R3 MYB, AtMyb73, causes hyper-induction of the SOS1 and SOS3 genes in response to high salinity in Arabidopsis. J Plant Physiol 2013, 170, 1461–1465. [Google Scholar] [CrossRef]
- Liu, Y.; Man, J.; Wang, Y.; Yuan, C.; Shi, Y.; Liu, B.; Hu, X.; Wu, S.; Zhang, T.; Lian, C. Overexpression of PtrMYB121 Positively Regulates the Formation of Secondary Cell Wall in Arabidopsis thaliana. Int. J. Mol. Sci. 2020, 21, 7734. [Google Scholar] [CrossRef]
- Kalyaanamoorthy, S.; Minh, B.Q.; Wong, T.K.F.; von Haeseler, A.; Jermiin, L.S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods 2017, 14, 587–589. [Google Scholar] [CrossRef] [Green Version]
- Nguyen, L.T.; Schmidt, H.A.; von Haeseler, A.; Minh, B.Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 2015, 32, 268–274. [Google Scholar] [CrossRef] [PubMed]
- Yu, G. Using ggtree to Visualize Data on Tree-Like Structures. Curr. Protoc. Bioinformatics 2020, 69, e96. [Google Scholar] [CrossRef] [PubMed]
- Filichkin, S.A.; Hamilton, M.; Dharmawardhana, P.D.; Singh, S.K.; Sullivan, C.; Ben-Hur, A.; Reddy, A.S.N.; Jaiswal, P. Abiotic Stresses Modulate Landscape of Poplar Transcriptome via Alternative Splicing, Differential Intron Retention, and Isoform Ratio Switching. Front. Plant Sci. 2018, 9, 5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bolger, A.M.; Lohse, M.; Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 2014, 30, 2114–2120. [Google Scholar] [CrossRef] [Green Version]
- Dobin, A.; Davis, C.A.; Schlesinger, F.; Drenkow, J.; Zaleski, C.; Jha, S.; Batut, P.; Chaisson, M.; Gingeras, T.R. STAR: Ultrafast universal RNA-seq aligner. Bioinformatics 2013, 29, 15–21. [Google Scholar] [CrossRef]
- Liao, Y.; Smyth, G.K.; Shi, W. featureCounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 2014, 30, 923–930. [Google Scholar] [CrossRef] [Green Version]
- Love, M.I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 2014, 15, 550. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gu, Z.; Gu, L.; Eils, R.; Schlesner, M.; Brors, B. circlize Implements and enhances circular visualization in R. Bioinformatics 2014, 30, 2811–2812. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.; Tang, H.; Debarry, J.D.; Tan, X.; Li, J.; Wang, X.; Lee, T.H.; Jin, H.; Marler, B.; Guo, H.; et al. MCScanX: A toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 2012, 40, e49. [Google Scholar] [CrossRef] [Green Version]
- Tang, H.; Wang, X.; Bowers, J.E.; Ming, R.; Alam, M.; Paterson, A.H. Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Res. 2008, 18, 1944–1954. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Z.; Xiao, J.; Wu, J.; Zhang, H.; Liu, G.; Wang, X.; Dai, L. ParaAT: A parallel tool for constructing multiple protein-coding DNA alignments. Biochem. Biophys. Res. Commun. 2012, 419, 779–781. [Google Scholar] [CrossRef] [PubMed]
- Lei, L.; Zhou, S.L.; Ma, H.; Zhang, L.S. Expansion and diversification of the SET domain gene family following whole-genome duplications in Populus trichocarpa. BMC Evol. Biol. 2012, 12, 51. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, J.; Li, Y.; Liu, B.; Wang, L.; Zhang, L.; Hu, J.; Chen, J.; Zheng, H.; Lu, M. Characterization of the Populus Rab family genes and the function of PtRabE1b in salt tolerance. BMC Plant Biol. 2018, 18, 124. [Google Scholar] [CrossRef] [Green Version]
- Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef] [PubMed]
- Tan, B.Y.; Xu, M.; Chen, Y.; Huang, M.R. Transient expression for functional gene analysis using Populus protoplasts. Plant Cell Tissue Organ Cult. 2013, 114, 11–18. [Google Scholar] [CrossRef]
- Fang, Z.; Ji, Y.; Hu, J.; Guo, R.; Sun, S.; Wang, X. Strigolactones and Brassinosteroids Antagonistically Regulate the Stability of the D53-OsBZR1 Complex to Determine FC1 Expression in Rice Tillering. Mol. Plant 2020, 13, 586–597. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zhang, X.; Wang, H.; Chen, Y.; Huang, M.; Zhu, S. Comprehensive Genome-Wide Analyses of Poplar R2R3-MYB Transcription Factors and Tissue-Specific Expression Patterns under Drought Stress. Int. J. Mol. Sci. 2023, 24, 5389. https://doi.org/10.3390/ijms24065389
Zhang X, Wang H, Chen Y, Huang M, Zhu S. Comprehensive Genome-Wide Analyses of Poplar R2R3-MYB Transcription Factors and Tissue-Specific Expression Patterns under Drought Stress. International Journal of Molecular Sciences. 2023; 24(6):5389. https://doi.org/10.3390/ijms24065389
Chicago/Turabian StyleZhang, Xueli, Haoran Wang, Ying Chen, Minren Huang, and Sheng Zhu. 2023. "Comprehensive Genome-Wide Analyses of Poplar R2R3-MYB Transcription Factors and Tissue-Specific Expression Patterns under Drought Stress" International Journal of Molecular Sciences 24, no. 6: 5389. https://doi.org/10.3390/ijms24065389