Biologia plantarum 64: 378-384, 2020 | DOI: 10.32615/bp.2020.012

An HD-Zip IV transcription factor protein NbGL3 regulates glandular trichome initiation in tobacco

Y.S. TIAN1,2, T.W. DAI2, C.X. FAN2, J. ZHOU1, X.L. REN1,*, Y. XU2,*
1 Molecular Genetics Key Laboratory of China Tobacco, Guizhou Academy of Tobacco Science, Guiyang 550081, P.R. China
2 College of Life Sciences, Sichuan University, Chengdu 610065, P.R. China

Glandular trichomes, a specialized multicellular structure, are considered as biofactories due to their capability to synthesize and secrete a large amount of secondary metabolites. Tobacco leaves have a high density of glandular trichomes that produce huge amounts of secondary metabolites, which can be used as important industrial raw materials. However, molecular mechanism controling glandular trichome development in tobacco still remains largely unknown. In the present study, we found that NbGL3, an HD-Zip IV family gene from Nicotiana benthamiana, was highly expressed in mature leaves, and ethylene or auxin application could increase the expression of NbGL3. Virus induced gene silencing NbGL3 resulted in a decreased glandular trichome density on leaves. Putative downstream genes, such as micro trichome, cyclin B2, and wax inducer 1 like were down regulated in NbGL3 silenced plants. Our results demonstrate that NbGL3 could positively regulate initiation of glandular trichomes in tobacco.

Keywords: auxin, ethylene, Nicotiana benthamiana, secondary metabolites, virus induced gene silencing.

Received: October 17, 2019; Revised: January 2, 2020; Accepted: January 20, 2020; Prepublished online: May 25, 2020; Published online: May 26, 2020Show citation

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TIAN, Y.S., DAI, T.W., FAN, C.X., ZHOU, J., REN, X.L., & XU, Y. (2020). An HD-Zip IV transcription factor protein NbGL3 regulates glandular trichome initiation in tobacco. Biologia plantarum, 64, 378-384. doi: 10.32615/bp.2020.012.
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    References

    1. Abe, M., Katsumata, H., Komeda, Y., Takahashi, T.: Regulation of shoot epidermal cell differentiation by a pair of homeodomain proteins in Arabidopsis. - Development 130: 635, 2003. Go to original source...
    2. Ariel, F.D., Manavella, P.A., Dezar, C.A., Chan, R.L.: The true story of the HD-Zip family. - Trends Plant Sci. 12: 419-426, 2007. Go to original source...
    3. Brandt, R., Cabedo, M., Xie, Y., Wenkel, S.: Homeodomain leucine-zipper proteins and their role in synchronizing growth and development with the environment. - J. integr. Plant Biol. 56: 518-526, 2014. Go to original source...
    4. Chen, C., Liu, M., Jiang, L., Liu, X., Zhao, J., Yan, S., Zhang, X.: Transcriptome profiling reveals roles of meristem regulators and polarity genes during fruit trichome development in cucumber (Cucumis sativus L.). - J. exp. Bot. 65: 4943-4958, 2014. Go to original source...
    5. Cui, J.Y., Miao, H., Ding, L.H., Wehner, T.C., Liu, P.N., Wang, Y., Gu, X.F.: A New glabrous gene (csgl3) identified in trichome development in cucumber (Cucumis sativus L.). - PLoS ONE 11: e0148422, 2016. Go to original source...
    6. Di Cristina, M., Sessa, G., Dolan, L., Linstead, P., Baima, S., Ruberti, I., Morelli, G..: The Arabidopsis Athb-10 (GLABRA2) is an HD-Zip protein required for regulation of root hair development. - Plant J. 10: 393-402, 1996. Go to original source...
    7. Glover, B.J., Perez-Rodriguez, M., Martin, C.: Development of several epidermal cell types can be specified by the same MYB-related plant transcription factor. - Development 125: 3497, 1998.
    8. Henriksson, E., Olsson, A.S., Johannesson, H., Johansson, H., Hanson, J., Engström, P., Söderman, E.: Homeodomain leucine zipper class I genes in Arabidopsis. Expression patterns and phylogenetic relationships. - Plant Physiol. 139: 509-518, 2005. Go to original source...
    9. Huchelmann, A., Boutry, M., Hachez, C.: Plant glandular trichomes: natural cell factories of high biotechnological interest. - Plant Physiol. 175: 6-22, 2017. Go to original source...
    10. Hur, Y.S., Um, J.H., Kim, S., Kim, K., Park, H.J., Lim, J.S., Lim, J.: Arabidopsis thaliana homeobox 12 (ATHB12), a homeodomain-leucine zipper protein, regulates leaf growth by promoting cell expansion and endoreduplication. - New Phytol. 205: 316-328, 2015. Go to original source...
    11. Kang, J.H., Campos, M.L., Zemelisdurfee, S., Alhaddad, J.M., Jones, A.D., Telewski, F.W., Howe, G.A.: Molecular cloning of the tomato Hairless gene implicates actin dynamics in trichome-mediated defense and mechanical properties of stem tissue. - J. exp. Bot. 67: 5313-5324, 2016. Go to original source...
    12. Kang, J.H., Mcroberts, J., Shi, F., Moreno, J.E., Jones, A.D., Howe, G.A.: The flavonoid biosynthetic enzyme chalcone isomerase modulates terpenoid production in glandular trichomes of tomato. - Plant Physiol. 164: 1161, 2014. Go to original source...
    13. Khosla, A., Paper, J.M., Boehler, A.P., Bradley, A.M., Neumann, T.R., Schrick, K.: HD-Zip proteins GL2 and HDG11 have redundant functions in Arabidopsis trichomes, and GL2 activates a positive feedback loop via MYB23. - Plant Cell 26: 2184-2200, 2014. Go to original source...
    14. Liu, Y., Liu, D., Hu, R., Hua, C., Ali, I., Zhang, A., Gan, Y.: AtGIS, a C2H2 zinc-finger transcription factor from Arabidopsis regulates glandular trichome development through GA signaling in tobacco. - Biochem. biophys. Res. Commun. 483: 209-215, 2017. Go to original source...
    15. Liu, Y., Liu, D., Khan, A. R., Liu, B., Wu, M., Huang, L., Gan, Y.: NbGIS regulates glandular trichome initiation through GA signaling in tobacco. - Plant mol. Biol. 98: 153-167, 2018. Go to original source...
    16. Marks, M.D., Feldmann, K.A.: Trichome Ddvelopment in Arabidopsis thaliana. I. T-DNA tagging of the GLABROUS1 gene. - Plant Cell 1: 1043-1050, 1989.
    17. Nielsen, M.T., Akers, C.P., Järlfors, U.E., Wagner, G.J., Berger, S.: comparative ultrastructural features of secreting and nonsecreting glandular trichomes of two genotypes of Nicotiana tabacum L. - Bot. Gaz. 152: 13-22, 1991. Go to original source...
    18. Otsuga, D., Deguzman, B., Prigge, M.J., Drews, G.N., Clark, S.E.: REVOLUTA regulates meristem initiation at lateral positions. - Plant J. 25: 223-236, 2010.
    19. Pan, Y., Bo, K., Cheng, Z., Weng, Y.: The loss-of-function GLABROUS 3 mutation in cucumber is due to LTR-retrotransposon insertion in a class IV HD-ZIP transcription factor gene CsGL3 that is epistatic over CsGL1. - BMC Plant Biol. 15: 302, 2015. Go to original source...
    20. Pattanaik, S., Patra, B., Singh, S.K., Yuan, L.: An overview of the gene regulatory network controlling trichome development in the model plant Arabidopsis. - Front. Plant Sci. 5: 259, 2014. Go to original source...
    21. Payne, T., Clement, J., Arnold, D., Lloyd, A.: Heterologous myb genes distinct from GL1 enhance trichome production when overexpressed in Nicotiana tabacum. - Development 126: 671-682, 1999.
    22. Pesch, M., Hülskamp, M.: One, two, three models for trichome patterning in Arabidopsis. - Curr. Opin. Plant Biol. 12: 587-592, 2009. Go to original source...
    23. Qing, L., Aoyama, T.: Pathways for epidermal cell differentiation via the homeobox gene GLABRA2: update on the roles of the classic regulator F. - J. integr. Plant Biol. 54: 729-737, 2012. Go to original source...
    24. Roda, A.L., Oldham, N.J., Svatos, A., Baldwin, I.T.: Allometric analysis of the induced flavonols on the leaf surface of wild tobacco (Nicotiana attenuata). - Phytochemistry 62: 527-536, 2003. Go to original source...
    25. Sallets, A., Beyaert, M., Boutry, M., Champagne, A.: Comparative proteomics of short and tall glandular trichomes of Nicotiana tabacum reveals differential metabolic activities. - J. Proteome Res. 13: 3386-3396, 2014. Go to original source...
    26. Schena, M., Davis, R.W.: HD-Zip proteins: members of an Arabidopsis homeodomain protein superfamily. - Proc. nat. Acad. Sci. USA 89: 3894-3898, 1992. Go to original source...
    27. Schilmiller, A.L., Last, R.L., Pichersky, E.: Harnessing plant trichome biochemistry for the production of useful compounds. - Plant J. 54: 702-711, 2010.
    28. Senthilkumar, M., Mysore, K.S.: Tobacco rattle virus-based virus-induced gene silencing in Nicotiana benthamiana. - Natur. Protocols 9: 1549-1562, 2014. Go to original source...
    29. Serna, L., Cathie, M. : Trichomes: different regulatory networks lead to convergent structures. - Trends Plant Sci. 11: 274-280, 2006. Go to original source...
    30. Shi, X., Gu, Y., Dai, T., Wu, Y., Wu, P., Xu, Y., Chen, F. : Regulation of trichome development in tobacco by JcZFP8, a C2H2 zinc finger protein gene from Jatropha curcas L. - Gene 658: 47-53, 2018. Go to original source...
    31. Vernoud, V., Laigle, G., Rozier, F., Meeley, R. B., Perez, P., Rogowsky, P. M. : The HD-ZIP IV transcription factor OCL4 is necessary for trichome patterning and anther development in maize. - Plant J. Cell mol. Biol. 59: 883-894, 2010.
    32. Wagner, G.J., Wang, E., Shepherd, R.W. : New approaches for studying and exploiting an old protuberance, the plant trichome. - Ann. Bot. 93: 3-11, 2004. Go to original source...
    33. Walford, S.A., Wu, Y., Llewellyn, D.J., Dennis, E.S.: Epidermal cell differentiation in cotton mediated by the homeodomain leucine zipper gene, GhHD-1. - Plant J. 71: 464-478, 2012. Go to original source...
    34. Wang, Y.L., Nie, J.T., Chen, H.M., Guo, C.L., Pan, J., He, H.L., Cai, R.: Identification and mapping of Tril, a homeodomain-leucine zipper gene involved in multicellular trichome initiation in Cucumis sativus. - Theor. appl. Genet. 129: 305-316, 2016. Go to original source...
    35. Werker, E. : Trichome diversity and development. - Adv. bot. Res. 31: 1-35, 2000. Go to original source...
    36. Williams, L., Grigg, S.P., Xie, M., Christensen, S., Fletcher, J.C. : Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. - Development 132: 3657-3668, 2005. Go to original source...
    37. Yan, A., Wu, M., Zhao, Y., Zhang, A., Gan, Y.: Involvement of C2H2 zinc finger proteins in the regulation of epidermal cell fate determination in Arabidopsis. - J. integr. Plant Biol. 56: 1112-1117, 2014. Go to original source...
    38. Yang, C., Gao, Y., Gao, S., Yu, G., Xiong, C., Chang, J., Ye, Z.: Transcriptome profile analysis of cell proliferation molecular processes during multicellular trichome formation induced by tomato Wov gene in tobacco. - BMC Genomics 16: 868, 2015. Go to original source...
    39. Yang, C., Li, H., Zhang, J., Luo, Z., Gong, P., Zhang, C., Ye, Z.: A regulatory gene induces trichome formation and embryo lethality in tomato. - Proc. nat. Acad. Sci. USA 108: 11836-11841, 2011. Go to original source...
    40. Zhang, F., Zuo, K., Zhang, J., Liu, X., Zhang, L., Sun, X., Tang, K.: An L1 box binding protein, GbML1, interacts with GbMYB25 to control cotton fibre development. - J. exp. Bot. 61: 3599-3613, 2010. Go to original source...
    41. Zhao, J.L., Wang, Y.L., Yao, D.Q., Zhu, W.Y., Chen, L., He, H.L., Cai, R.: Transcriptome profiling of trichome-less reveals genes associated with multicellular trichome development in Cucumis sativus. - Mol. Genet. Genomics 290: 2007-2018, 2015.

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