[en] Zinc finger homeodomain (ZF-HD) transcription factors play significant roles in plant growth and responses to environmental stresses. In this study, 32 ZF-HD genes identified in the tobacco (Nicotiana tabacum L.) genome were divided into six groups according to phylogenetic analysis with Arabidopsis and tomato ZF-HD members. An examination of gene structures and conserved motifs revealed the relatively conserved exon/intron structures and motif organization within each subgroup. In addition, various stress-related elements are found in the promoter region of these genes. The expression profiling analysis revealed that NtZF-HD genes expressed in different tissues and could be induced by several abiotic stresses. Notably, NtZF-HD21 was highly expressed in response to the drought treatments. Subcellular localization analysis and a virus-induced gene silencing (VIGS) experiment were performed to investigate the potential functions of NtZF-HD21. The subcellular localization indicated that NtZF-HD21 is a nuclear protein. Furthermore, gene silencing of the NtZF-HD21 gene reduced the drought resistance of tobacco. These findings provide insights for further biological functional analyses of the NtZF-HD genes in tobacco.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Sun, Jinhao ; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, China ; Graduate School of Chinese Academy of Agricultural Science, Beijing, China
Xie, Minmin ; Université de Liège - ULiège > TERRA Research Centre ; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, China ; Graduate School of Chinese Academy of Agricultural Science, Beijing, China
Li, Xiaoxu ; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, China ; Technology Center, China Tobacco Hunan Industrial Co., Ltd, Changsha, China
Li, Zhiyuan; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, China ; Graduate School of Chinese Academy of Agricultural Science, Beijing, China
Wang, Qi; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, China ; Graduate School of Chinese Academy of Agricultural Science, Beijing, China
Ding, Anming ; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, China ; Graduate School of Chinese Academy of Agricultural Science, Beijing, China
Wang, Weifeng; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, China ; Graduate School of Chinese Academy of Agricultural Science, Beijing, China
Sun, Yuhe; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, China ; Graduate School of Chinese Academy of Agricultural Science, Beijing, China
Language :
English
Title :
Systematic investigations of the ZF-HD gene family in Tobacco reveal their multiple roles in abiotic stresses
Funding: This work was supported by the Mining and Application of Tobacco Gene Based on EMS Mutant Database (16102320200002) and the Science Foundation for Young Scholars of the Tobacco Research Institute of the Chinese Academy of Agricultural Sciences (2018B02).
Glazebrook, J. Genes controlling expression of defense responses in Arabidopsis—2001 status. Curr. Opin. Plant Biol. 2001, 4, 301–308. [CrossRef]
Singh, K.; Foley, R.C.; Onate-Sanchez, L. Transcription factors in plant defense and stress responses. Curr. Opin. Plant Biol. 2002, 5, 430–436. [CrossRef]
Wang, W.; Wu, P.; Li, Y.; Hou, X. Genome-wide analysis and expression patterns of ZF-HD transcription factors under different developmental tissues and abiotic stresses in Chinese cabbage. Mol. Genet. Genom. 2016, 291, 1451–1464. [CrossRef]
Ciftci-Yilmaz, S.; Mittler, R. The Zinc finger network of plants. Cell. Mol. Life Sci. 2008, 65, 1150–1160. [CrossRef]
Xie, M.M.; Sun, J.H.; Gong, D.P.; Kong, Y.Z. The roles of Arabidopsis C1-2i subclass of C2H2-type Zinc-finger transcription factors. Genes 2019, 10, 653. [CrossRef]
Hu, W.; dePamphilis, C.W.; Ma, H. Phylogenetic analysis of the plant-specific Zinc finger-homeobox and mini Zinc finger gene families. J. Integr. Plant Biol. 2008, 50, 1031–1045. [CrossRef] [PubMed]
Mukherjee, K.; Brocchieri, L.; Burglin, T.R. A comprehensive classification and evolutionary analysis of plant homeobox genes. Mol. Biol. Evol. 2009, 26, 2775–2794. [CrossRef]
Gehring, W.J.; Affolter, M.; Burglin, T. Homeodomain proteins. Annu. Rev. Biochem. 1994, 63, 487–526. [CrossRef] [PubMed]
Ariel, F.D.; Manavella, P.A.; Dezar, C.A.; Chan, R.L. The true story of the HD-ZIP family. Trends Plant Sci. 2007, 12, 419–426. [CrossRef]
Kawagashira, N.; Ohtomo, Y.; Murakami, K.; Matsubara, K.; Kawai, J.; Carninci, P.; Hayashizaki, Y.; Kikuchi, S.; Higo, K. Multiple Zinc finger motifs with comparison of plant and insect. Genom. Inform. 2001, 12, 368–369.
Englbrecht, C.C.; Schoof, H.; Bohm, S. Conservation, diversification and expansion of C2 H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genom. 2004, 5, 39. [CrossRef]
Windhovel, A.; Hein, I.; Dabrowa, R.; Stockhaus, J. Characterization of a novel class of plant homeodomain proteins that bind to the C4 phosphoenolpyruvate carboxylase gene of Flaveria trinervia. Plant Mol. Biol. 2001, 45, 201–214. [CrossRef]
Galvao, V.C.; Horrer, D.; Kuttner, F.; Schmid, M. Spatial control of flowering by della proteins in Arabidopsis thaliana. Development 2012, 139, 4072–4082. [CrossRef]
Porri, A.; Torti, S.; Romera-Branchat, M.; Coupland, G. Spatially distinct regulatory roles for gibberellins in the promotion of flowering of Arabidopsis under long photoperiods. Development 2012, 139, 2198–2209. [CrossRef] [PubMed]
Shalmani, A.; Muhammad, I.; Sharif, R.; Zhao, C.; Ullah, U.; Zhang, D.; Jing, X.Q.; Amin, B.; Jia, P.; Tahir, M.M.; et al. Zinc finger-homeodomain genes: Evolution, functional differentiation, and expression profiling under flowering-related treatments and abiotic stresses in plants. Evol. Bioinform. 2019, 15, 1–16. [CrossRef]
Hong, S.Y.; Kim, O.K.; Kim, S.G.; Yang, M.S.; Park, C.M. Nuclear import and DNA binding of the ZHD5 transcription factor is modulated by a competitive peptide inhibitor in Arabidopsis. J. Biol. Chem. 2011, 286, 1659–1668. [CrossRef] [PubMed]
Perrella, G.; Davidson, M.L.H.; O’Donnell, L.; Nastase, A.M.; Herzyk, P.; Breton, G.; Pruneda-Paz, J.L.; Kay, S.A.; Chory, J.; Kaiserli, E. Zinc-finger interactions mediate transcriptional regulation of hypocotyl growth in Arabidopsis. Proc. Natl. Acad. Sci. USA 2018, 115, E4503–E4511. [CrossRef]
Khatun, K.; Nath, U.K.; Robin, A.H.K.; Park, J.I.; Lee, D.J.; Kim, M.B.; Kim, C.K.; Lim, K.B.; Nou, I.S.; Chung, M.Y. Genome-wide analysis and expression profiling of Zinc finger homeodomain (ZHD) family genes reveal likely roles in organ development and stress responses in tomato. BMC Genom. 2017, 18, 695. [CrossRef] [PubMed]
Liu, M.; Wang, X.; Sun, W.; Ma, Z.; Zheng, T.; Huang, L.; Wu, Q.; Tang, Z.; Bu, T.; Li, C.; et al. Genome-wide investigation of the ZF-HD gene family in tartary buckwheat (Fagopyrum tataricum). BMC Plant Biol. 2019, 19, 248. [CrossRef]
Tran, L.S.P.; Nakashima, K.; Sakuma, Y.; Osakabe, Y.; Qin, F.; Simpson, S.D.; Maruyama, K.; Fujita, Y.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Co-expression of the stress-inducible Zinc finger homeodomain ZFHD1 and NAC transcription factors enhances expression of the ERD1 gene in Arabidopsis. Plant. J. 2007, 49, 46–63. [CrossRef] [PubMed]
Wang, H.; Yin, X.; Li, X.; Wang, L.; Zheng, Y.; Xu, X.; Zhang, Y.; Wang, X. Genome-wide identification, evolution and expression analysis of the grape (Vitis vinifera L.) Zinc finger-homeodomain gene family. Int. J. Mol. Sci. 2014, 15, 5730–5748. [CrossRef] [PubMed]
Bhattacharjee, A.; Jain, M. Homeobox genes as potential candidates for crop improvement under abiotic stress. Plant. Acclim. Environ. Stress 2013, 163–176. [CrossRef]
Barth, O.; Vogt, S.; Uhlemann, R.; Zschiesche, W.; Humbeck, K. Stress induced and nuclear localized hipp26 from Arabidopsis thaliana interacts via its heavy metal associated domain with the drought stress related Zinc finger transcription factor ATHB29. Plant Mol. Biol. 2009, 69, 213–226. [CrossRef] [PubMed]
Park, H.C.; Kim, M.L.; Lee, S.M.; Bahk, J.D.; Yun, D.J.; Lim, C.O.; Hong, J.C.; Lee, S.Y.; Cho, M.J.; Chung, W.S. Pathogen-induced binding of the soybean zinc finger homeodomain proteins GmZF-HD1 and GmZF-HD2 to two repeats of atta homeodomain binding site in the Calmodulin Isoform 4 (GmCaM4) promoter. Nucleic Acids Res. 2007, 35, 3612–3623. [CrossRef] [PubMed]
Jain, M.; Tyagi, A.K.; Khurana, J.P. Genome-wide identification, classification, evolutionary expansion and expression analyses of homeobox genes in rice. FEBS J. 2008, 275, 2845–2861. [CrossRef]
Ma, J.J.; Zheng, L.W.; Zhao, C.D.; Li, G.F.; Shen, Y.W.; An, N.; Zhang, D.; Han, M.Y. Genome-wide identification and expression analysis of half-size ABCG genes in Malus × domestica. Hortic Plant. J. 2018, 4, 45–54. [CrossRef]
Sierro, N.; Battey, J.N.; Ouadi, S.; Bakaher, N.; Bovet, L.; Willig, A.; Goepfert, S.; Peitsch, M.C.; Ivanov, N.V. The tobacco genome sequence and its comparison with those of tomato and potato. Nat. Commun. 2014, 5, 3833. [CrossRef] [PubMed]
Edwards, K.D.; Fernandez-Pozo, N.; Drake-Stowe, K.; Humphry, M.; Evans, A.D.; Bombarely, A.; Allen, F.; Hurst, R.; White, B.; Kernodle, S.P.; et al. A reference genome for Nicotiana tabacum enables map-based cloning of homeologous loci implicated in nitrogen utilization efficiency. BMC Genom. 2017, 18, 448. [CrossRef] [PubMed]
Fernandez-Pozo, N.; Menda, N.; Edwards, J.D.; Saha, S.; Tecle, I.Y.; Strickler, S.R.; Bombarely, A.; Fisher-York, T.; Pujar, A.; Foerster, H.; et al. The Sol Genomics Network (SGN)–from genotype to phenotype to breeding. Nucleic Acids Res. 2015, 43, D1036–D1041. [CrossRef]
Poole, R.L. The TAIR database. Methods Mol. Biol. 2007, 406, 179–212. [PubMed]
Finn, R.D.; Coggill, P.; Eberhardt, R.Y.; Eddy, S.R.; Mistry, J.; Mitchell, A.L.; Potter, S.C.; Punta, M.; Qureshi, M.; Sangrador-Vegas, A.; et al. The Pfam protein families database: Towards a more sustainable future. Nucleic Acids Res. 2016, 44, D279–D285. [CrossRef] [PubMed]
Letunic, I.; Doerks, T.; Bork, P. SMART: Recent updates, new developments and status in 2015. Nucleic Acids Res. 2015, 43, D257–D260. [CrossRef]
Garg, V.K.; Avashthi, H.; Tiwari, A. MFPPI—Multi FASTA protparam interface. Bioinformation 2016, 12, 74–77. [CrossRef]
Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [CrossRef] [PubMed]
Lescot, M.; Dehais, P.; Thijs, G.; Marchal, K.; Moreau, Y.; Van de Peer, Y.; Rouze, P.; Rombauts, S. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002, 30, 325–327. [CrossRef]
Chen, C.J.; Chen, H.; Zhang, Y.; Thomas, H.R.; Frank, M.H.; He, Y.H.; Xia, R. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Mol. Plant 2020, 13, 1194–1202. [CrossRef]
Khatun, K.; Robin, A.H.K.; Park, J.I.; Ahmed, N.U.; Kim, C.K.; Lim, K.B.; Kim, M.B.; Lee, D.J.; Nou, I.S.; Chung, M.Y. Genome-wide identification, characterization and expression profiling of LIM family genes in Solanum lycopersicum L. Plant Physiol Biochem. 2016, 108, 177–190. [CrossRef] [PubMed]
Ren, A.; Ahmed, R.I.; Chen, H.; Han, L.; Sun, J.; Ding, A.; Guo, Y.; Kong, Y. Genome-wide identification, characterization and expression patterns of the pectin methylesterase inhibitor genes in sorghum bicolor. Genes 2019, 10, 755. [CrossRef] [PubMed]
Untergasser, A.; Cutcutache, I.; Koressaar, T.; Ye, J.; Faircloth, B.C.; Remm, M.; Rozen, S.G. Primer3–new capabilities and interfaces. Nucleic Acids Res. 2012, 40, e115. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
Chou, K.C.; Shen, H.B. Plant-mPLoc: A top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS ONE 2010, 5, e11335. [CrossRef] [PubMed]
Li, X.; Guo, C.; Ahmad, S.; Wang, Q.; Yu, J.; Liu, C.; Guo, Y. Systematic analysis of MYB family genes in potato and their multiple roles in development and stress responses. Biomolecules 2019, 9, 317. [CrossRef]
Gao, X.; Shan, L. Functional Genomic Analysis of Cotton Genes with Agrobacterium-Mediated Virus-Induced Gene Silencing. Methods Mol. Biol. 2013, 975, 157–165. [CrossRef] [PubMed]
Burch-Smith, T.M.; Anderson, J.C.; Martin, G.B.; Dinesh-Kumar, S.P. Applications and advantages of virus-induced gene silencing for gene function studies in plants. Plant J. 2010, 39, 734–746. [CrossRef] [PubMed]
Li, Y.; Bai, B.; Wen, F.; Zhao, M.; Xia, Q.; Yang, D.H.; Wang, G. Genome-wide identification and expression analysis of HD-ZIP|gene subfamily in Nicotiana tabacum. Genes 2019, 10, 575. [CrossRef]