biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 65:60-67, 2021 | DOI: 10.32615/bp.2020.141

Cloning and functional analysis of the promoter of the sesquiterpene synthase gene ASS1 in Aquilaria sinensis

Y.H. XU1, F.F. LV2, P.W. SUN1, M.H. TIAN1, J.H. WEI1, 2, *
1 Key Laboratory of Bioactive Substances and Resources Utilization of Chinese Herbal Medicine, Ministry of Education; Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100193, P.R. China
2 Hainan Branch of the Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences and Peking Union Medical College, Haikou 570311, P.R. China

Agarwood, the resin part of Aquilaria spp., is valued in medicine, perfumes, and incense. The most important components of agarwood are sesquiterpenes, which are produced only when a healthy tree is wounded. Agarwood sesquiterpene synthase 1 (ASS1) is one of key enzymes responsible for the biosynthesis of sesquiterpenes in Aquilaria sinensis (Lour.) Gilg, and it is a typical wound-inducible synthase. To elucidate its regulatory mechanism at the transcriptional level, a 978-bp sequence upstream of the translation initiation codon ATG of the promoter for ASS1 was cloned. Computational analysis revealed that this promoter contained many known cis-elements including several defense related transcriptional factor-binding boxes. To functionally validate the promoter, a 5' truncated fragment fused with the β-glucuronidase (GUS) reporter gene was used for generating stable transgenic Arabidopsis plants. The spatial and temporal expression patterns of GUS in transgenic Arabidopsis showed that the promoter of ASS1 was induced by mechanical wound and mainly expressed in vascular bundles. Subcellular localization showed that ASS1 localized in the nucleus and plasma membrane. Here, identification of the ASS1 promoter not only lays a foundation for studying its transcriptional regulation, but also provides clues for studying the synthesis mechanism of agarwood sesquiterpenes.

Keywords: agarwood, β-glucuronidase, onion epidermis, transgenic Arabidopsis plants.

Received: April 27, 2020; Revised: September 25, 2020; Accepted: September 29, 2020; Published online: March 29, 2021  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
XU, Y.H., LV, F.F., SUN, P.W., TIAN, M.H., & WEI, J.H. (2021). Cloning and functional analysis of the promoter of the sesquiterpene synthase gene ASS1 in Aquilaria sinensis . Biologia plantarum, 65, Article 60-67. https://doi.org/10.32615/bp.2020.141
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Agrawal, A.A.: Induced responses to herbivory and increased plant performance. - Science 279: 1201-1202, 1998. Go to original source...
    2. Aharoni, A., Giri, A.P., Verstappen, F.W.: Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. - Plant Cell 16: 3110-3131, 2004. Go to original source...
    3. Arimura, G., Ozawa, R., Shimoda, T., Nishioka, T., Boland, W., Takabayashi, J.: Herbivory-induced volatiles elicit defence genes in lima bean leaves. - Nature 406: 512-515, 2000. Go to original source...
    4. Bang, S.W., Park, S.H., Jeong, J.S., Kim, Y.S., Jung, H., Ha, S.H., Kim, J.K.: Characterization of the stress-inducible OsNCED3 promoter in different transgenic rice organs and over three homozygous generations. - Planta 237: 211-224, 2013. Go to original source...
    5. Chen, F., Tholl, D., D'Auria, J.C., Farooq, A., Pichersky, E., Gershenzon, J.: Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. - Plant Cell 15: 481-494, 2003. Go to original source...
    6. Chen, H.Q., Yang, Y., Xue, J., Wei, J.H., Zhang, Z., Chen, H.J.: Comparison of compositions and antimicrobial activities of essential oils from chemically stimulated agarwood, wild agarwood and healthy Aquilaria sinensis (Lour.) Gilg trees. - Molecules 16: 4884-4896, 2011. Go to original source...
    7. Chen, H.Q., Wei, J.H., Yang, J.S., Zhang, Z., Yang, Y.: Chemical constituents of agarwood originating from the endemic genus Aquilaria plants. - Chem. Biodiv. 9: 236-250, 2012. Go to original source...
    8. De Moraes, C.M., Lewis, W.J., Pare, P.W., Alborn, H.T., Tumlinson, J.H.: Herbivore-infested plants selectively attract parasitoids. - Nature 393: 570-573, 1998. Go to original source...
    9. Duan, L.X., Chen, T.L., Li, M., Chen, M., Zhou, Y.Q., Cui, G.H., Zhao, A.H., Jia, W., Huang, L.Q., Qi, X.: Use of the metabolomics approach to characterize Chinese medicinal material Huangqi. - Mol. Plants 5: 376-386, 2012. Go to original source...
    10. Dubos, C., Stracke, R., Grotewold, E., Weisshaar, B., Martin, C., Lepiniec, L.: MYB transcription factors in Arabidopsis. - Trends Plant Sci. 15: 573-581, 2010. Go to original source...
    11. Farmer, E.E., Ryan, C.A.: Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. - Plant Cell 4: 129-134, 1992 Go to original source...
    12. Gomi, K., Yamasaki, Y., Yamamoto, H., Akimitsu, K.: Characterization of a hydroperoxide lyase gene and effect of C6-volatiles on expression of genes of the oxylipin metabolism in Citrus. - J. Plant Physiol. 160: 1219-1231, 2003. Go to original source...
    13. Hashimoto, K., Nakahara, S., Inoue, T., Sumida, Y., Takahashi, M.: A new chromone from agarwood and pyrolysis products of chromone derivatives. - Chem. Pharm. Bull. 33: 5088-5091, 1985. Go to original source...
    14. He, J., Giusti, M.M.: Anthocyanins: natural colorants with health-promoting properties. - Annu. Rev. Food Sci. 1: 163-187, 2010. Go to original source...
    15. Hernandez-Garcia, C.M., Finer, J.J.: Identification and validation of promoters and cis-acting regulatory elements. - Plant Sci. 217-218: 109-119, 2014. Go to original source...
    16. Himmelbach, A., Liu, L., Zierold, U., Altschmied, L., Maucher, H., Beier, F., Müller, D., Hensel, G., Heise, A., Schützendübel, A., Kumlehn, J., Schweizer, P.: Promoters of the barley germin-like GER4 gene cluster enable strong transgene expression in response to pathogen attack. - Plant Cell 22: 937-952, 2010. Go to original source...
    17. Hwang, S.H., Lee, I.A., Yie, S.W., Hwang, D.J.: Identification of an OsPR10a promoter region responsive to salicylic acid. - Planta 227: 1141-1150, 2008. Go to original source...
    18. Ito, M., Okimoto, K., Yagura, T., Honda, G.: Induction of sesquiterpenoid production by methyl jasmonate in Aquilaria sinensis cell suspension culture. - J. essential Oil Res. 17: 175-180, 2005. Go to original source...
    19. Itoh, T., Tabata, Y., Widjaja, E., Mulyaningsih T., Parman, H.W.: Structure and artificial induction of aloe wood. - IAWA J. 23: 466-467, 2002.
    20. Kazan, K., Manners, J.M.: MYC2: the master in action. - Mol. Plants 6: 686-703, 2013. Go to original source...
    21. Kessler, A., Baldwin, I.T.: Plant responses to insect herbivory: the emerging molecular analysis. - Annu. Rev. Plant Biol. 53: 299-328, 2002. Go to original source...
    22. Kroymann, J.: Natural diversity and adaptation in plant secondary metabolism. - Curr. Opin. Plant Biol. 1: 246-251, 2011. Go to original source...
    23. Kumeta, Y., Ito, M.: Characterization of δ-guaiene synthases from cultured cells of Aquilaria, responsible for the formation of the sesquiterpenes in agarwood. - Plant Physiol. 154: 1998-2007, 2010. Go to original source...
    24. Lange, B.M., Ahkami, A.: Metabolic engineering of plant monoterpenes, sesquiterpenes and diterpenes-current status and future opportunities. - Plant Biotechnol. J. 11: 169-196, 2013. Go to original source...
    25. Li, R.H., Fan, Y.P.: Molecular cloning and expression analysis of a terpene synthase gene, HcTPS2, in Hedychium coronarium. - Plant mol. Biol. Rep. 29: 35-42, 2011. Go to original source...
    26. Liu, P.W., Zhang, X.L., Yang, Y., Sui, C., Xu, Y.H., Wei, J.H.: Interxylary phloem and xylem rays are the structural foundation of agarwood resin formation in the stems of Aquilaria sinensis. - Trees 33: 533-542, 2019. Go to original source...
    27. Liu, Y.Y., Chen, H.Q., Yang, Y., Zhang, Z., Wei, J.H., Meng, H.: Whole-tree agarwood-inducing technique: an efficient novel technique for producing high-quality agarwood in cultivated Aquilaria sinensis trees. - Molecules 18: 3086-3106, 2013. Go to original source...
    28. Lou, Y.G., Ma, B., Cheng, J.A.: Attraction of the parasitoid Anagrus nilaparvatae to rice volatiles induced by the rice brown planthopper Nilaparvata lugens. - J. chem. Ecol. 31: 2357-2372, 2007. Go to original source...
    29. Nagegowda, D.A., Gutensohn, M., Wilkerson, C.G., Dudareva, N.: Two nearly identical terpene synthases catalyze the formation of nerolidol and linalool in snapdragon flowers. - Plant J. 55: 224-239, 2008. Go to original source...
    30. Nieuwenhuizen, N.J., Wang, M.Y., Matich, A.J., Green, S.A., Chen, X.Y., Yauk, Y.K., Beuning, L.L., Nagegowda, D.A., Dudareva, N., Atkinson, R.G.: Two terpene synthases are responsible for the major sesquiterpenes emitted from the flowers of kiwifruit (Actinidia deliciosa). - J. exp. Bot. 60: 3203-3219, 2009. Go to original source...
    31. Noguero, M., Atif, R.M., Ochatt, S., Thompson, R.D.: The role of the DNA-binding One Zinc Finger (DOF) transcription factor family in plants. - Plant Sci. 209: 32-45, 2013. Go to original source...
    32. Okudera, Y., Ito, M.: Production of agarwood fragrant constituents in Aquilaria calli and cell suspension cultures. - Plant Biotechnol. 26: 307-315, 2009. Go to original source...
    33. Pandey, S.P., Somssich, I.E.: The role of WRKY transcription factors in plant immunity. - Plant Physiol. 150: 1648-1655, 2009. Go to original source...
    34. Pellegrineschi, A., Reynolds, M., Pacheco, M., Brito, R.M., Almeraya, R., Yamaguchi- Shinozaki, K., Hoisington, D.: Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. - Genome 47: 493-500, 2004. Go to original source...
    35. Penninckx, I.A., Thomma, B.P., Buchala, A., Métraux, J.P., Broekaert, W.F.: Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. - Plant Cell 10: 2103-2113, 1998. Go to original source...
    36. Peremarti, A., Twyman, R.M., Gomez-Galera, S., Naqvi, S., Farre, G., Sabalza, M., Miralpeix, B., Dashevskaya, S., Yuan, D., Ramessar, K., Christou, P., Zhu, C., Bassie, L., Capell, T.: Promoter diversity in multigene transformation. - Plant mol. Biol. 73: 363-378, 2010. Go to original source...
    37. Persoon, G.A., van Beek, H.H.: Growing 'the wood of the gods': agarwood production in southeast Asia. Smallholder tree growing for rural development and environmental service. - Adv. Agroforest. 5: 245-262, 2008. Go to original source...
    38. Pichersky, E., Gershenzon, J.: The formation and function of plant volatiles: perfumes for pollinator attraction and defense. - Curr. Opin. Plant Biol. 5: 237-243, 2002. Go to original source...
    39. Pojanagaroon, S., Kaewrak, C.: Mechanical methods to stimulate aloes wood formation in Aquilaria crassna Pierre Ex H. LEC. (Kritsana) trees. - ISHS Acta Hort. 676: 161-166, 2005. Go to original source...
    40. Sallaud, C., Rontein, D., Onillon, S., Jabes, F., Duffe, P., Giacalone, C., Thoraval, S., Escoffier, C., Herbette, G., Leonhardt, N., Causse, M., Tissier, A.: A novel pathway for sesquiterpene biosynthesis from Z,Z-farnesyl pyrophosphate in the wild tomato Solanum habrochaltes. - Plant Cell 21: 310-307, 2009. Go to original source...
    41. Shen, B.Z., Zheng, Z.W., Dooner, H.K.: A maize sesquiterpene cyclase gene induced by insect herbivory and volicitin: characterization of wild-type and mutant alleles. - Proc. nat. Acad. Sci. USA 97: 14807-14812, 2000. Go to original source...
    42. Turlings, T.C., Tumlinson, J.H., Lewis, W.J.: Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. - Science 250: 1251-1253, 1990. Go to original source...
    43. Xu, Y.H., Zhang, Z., Wang, M.X., Wei, J.H., Chen, H.J., Gao, Z.H., Sui, C., Luo, H.M., Zhang, X.L., Yang, Y., Meng, H., Li, W.L.: Identification of genes related to agarwood formation: transcriptome analysis of healthy and wounded tissues of Aquilaria sinensis. - BMC Genomics 14: 227, 2013. Go to original source...
    44. Xu, Y.H., Liao, Y.C., Zhang, Z., Liu, J., Sun, P.W., Gao, Z.H., Sui, C., Wei, J.H.: Jasmonic acid is a crucial signal transducer in heat shock induced sesquiterpene formation in Aquilaria sinensis. - Sci. Rep. 6: 21843, 2016. Go to original source...
    45. Yamasaki, Y., Kunoh, H., Yamamoto, H., Akimitsu, K.: Biological roles of monoterpene volatiles derived from rough lemon (Citrus jambhiri Lush) in citrus defense. - J. gen. Plant Pathol. 3: 168-179, 2007. Go to original source...
    46. Yi, N., Oh S.J., Kim, Y.S., Jang, H.J., Park, S.H., Jeong, J.S., Song, S.I., Choi, Y.D., Kim, J.K.: Analysis of the Wsi18, a stress-inducible promoter that is active in the whole grain of transgenic rice. - Transgenic Res. 20: 153-163, 2011. Go to original source...
    47. Yu, F.N., Okamto, S., Nakasone, K., Adachi, K., Matsuda, S., Harada, H., Misawa, N., Utsumi, R.: Molecular cloning and functional characterization of alpha humulene synthase, a possible key enzyme of zerumbone biosynthesis in shampoo ginger (Zingiber zerumbet Smith). - Planta 227: 1291-1299, 2008a. Go to original source...
    48. Yu, F., Harada, H., Yamasaki, K., Okamoto, S., Hirase, S., Tanaka, Y., Misawa, N., Utsumi, R.: Isolation and functional characterization of a beta-eudesmol synthase, a new sesquiterpene synthase from Zingiber zerumbet Smith. - FEBS Lett. 582: 565-572, 2008b. Go to original source...
    49. Zhou, M.L., Zhu, X.M., Shao, J.R., Tang, Y.X., Wu, Y.M.: Production and metabolic engineering of bioactive substances in plant hairy root culture. - Appl. Microbiol. Biotechnol. 90: 1229-1239, 2011. Go to original source...
    50. Zou, C., Sun, K., Mackaluso, J.D., Seddon, A.E., Jin, R., Michael, F., Thomashow, M.F., Shiu, S.H.: Cis-regulatory code of stress-responsive transcription in Arabidopsis thaliana. - Proc. nat. Acad. Sci. USA 108: 14992-14997, 2011. Go to original source...

    Return to the content