Heteromerization of short-chain trans-prenyltransferase controls precursor allocation within a plastidial terpenoid network.

Arabidopsis geranylfarnesyl diphosphate synthase geranylgeranyl pyrophosphate synthase plastid sesterterpene terpene network

Journal

Journal of integrative plant biology
ISSN: 1744-7909
Titre abrégé: J Integr Plant Biol
Pays: China (Republic : 1949- )
ID NLM: 101250502

Informations de publication

Date de publication:
May 2023
Historique:
received: 19 09 2022
accepted: 16 01 2023
medline: 15 5 2023
pubmed: 18 1 2023
entrez: 17 1 2023
Statut: ppublish

Résumé

Terpenes are the largest and most diverse class of plant specialized metabolites. Sesterterpenes (C25), which are derived from the plastid methylerythritol phosphate pathway, were recently characterized in plants. In Arabidopsis thaliana, four genes encoding geranylfarnesyl diphosphate synthase (GFPPS) (AtGFPPS1 to 4) are responsible for the production of GFPP, which is the common precursor for sesterterpene biosynthesis. However, the interplay between sesterterpenes and other known terpenes remain elusive. Here, we first provide genetic evidence to demonstrate that GFPPSs are responsible for sesterterpene production in Arabidopsis. Blockage of the sesterterpene pathway at the GFPPS step increased the production of geranylgeranyl diphosphate (GGPP)-derived terpenes. Interestingly, co-expression of sesterTPSs in GFPPS-OE (overexpression) plants rescued the phenotypic changes of GFPPS-OE plants by restoring the endogenous GGPP. We further demonstrated that, in addition to precursor (DMAPP/IPP) competition by GFPPS and GGPP synthase (GGPPS) in plastids, GFPPS directly decreased the activity of GGPPS through protein-protein interaction, ultimately leading to GGPP deficiency in planta. Our study provides a new regulatory mechanism of the plastidial terpenoid network in plant cells.

Identifiants

pubmed: 36647626
doi: 10.1111/jipb.13454
doi:

Substances chimiques

Terpenes 0
Dimethylallyltranstransferase EC 2.5.1.1
Sesterterpenes 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1170-1182

Informations de copyright

© 2023 Institute of Botany, Chinese Academy of Sciences.

Références

Barja, M.V., Ezquerro, M., Beretta, S., Diretto, G., Florez-Sarasa, I., Feixes, E., Fiore, A., Karlova, R., Fernie, A.R., Beekwilder, J., and Rodriguez-Concepcion, M. (2021). Several geranylgeranyl diphosphate synthase isoforms supply metabolic substrates for carotenoid biosynthesis in tomato. New Phytol. 231: 255-272.
Beck, G., Coman, D., Herren, E., Ruiz-Sola, M., Rodriguez-Concepcion, M., Gruissem, W., and Vranova, E. (2013). Characterization of the GGPP synthase gene family in Arabidopsis thaliana. Plant Mol. Biol. 82: 393-416.
Burke, C.C., Wildung, M.R., and Croteau, R. (1999). Geranyl diphosphate synthase: Cloning, expression, and characterization of this prenyltransferase as a heterodimer. Proc. Natl. Acad. Sci. U.S.A. 96: 13062-13067.
Chen, H.M., Zou, Y., Shang, Y.L., Lin, H.Q., Wang, Y.J., Cai, R., Tang, X.Y., and Zhou, J.M. (2008). Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol. 146: 368-376.
Chen, Q., Fan, D., and Wang, G. (2015). Heteromeric geranyl(geranyl). diphosphate synthase is involved in monoterpene biosynthesis in Arabidopsis flowers. Mol. Plant 8: 1434-1437.
Chen, Q., Jiang, T., Liu, Y.X., Liu, H., Zhao, T., Liu, Z., Gan, X., Hallab, A., Wang, X., He, J., Ma, Y., Zhang, F., Jin, T., Schranz, M.E., Wang, Y., Bai, Y., and Wang, G. (2019). Recently duplicated sesterterpene (C25). gene clusters in Arabidopsis thaliana modulate root microbiota. Sci. China: Life Sci. 62: 947-958.
Chen, Q., Li, J., Liu, Z., Mitsuhashi, T., Zhang, Y., Liu, H., Ma, Y., He, J., Shinada, T., Sato, T., Wang, Y., Liu, H., Abe, I., Zhang, P., and Wang, G. (2020). Molecular basis for sesterterpene diversity produced by plant terpene synthases. Plant Commun. 1: 100051.
Chen, Q., Li, J., Ma, Y., Yuan, W., Zhang, P., and Wang, G. (2021a). Occurrence and biosynthesis of plant sesterterpenes (C25), a new addition to terpene diversity. Plant Commun. 2: 100184.
Chen, Y.G., Li, D.S., Ling, Y., Liu, Y.C., Zuo, Z.L., Gan, L.S., Luo, S.H., Hua, J., Chen, D.Y., Xu, F., Li, M., Guo, K., Liu, Y., Gershenzon, J., and Li, S.H. (2021a). A cryptic plant terpene cyclase producing unconventional 18- and 14-membered macrocyclic C25 and C20 terpenoids with immunosuppressive activity. Angew. Chem. Int. Ed. Engl. 60: 25468-25476.
Christianson, D.W. (2017). Structural and chemical biology of terpenoid cyclases. Chem. Rev. 117: 11570-11648.
Closa, M., Vranova, E., Bortolotti, C., Bigler, L., Arro, M., Ferrer, A., and Gruissem, W. (2010). The Arabidopsis thaliana FPP synthase isozymes have overlapping and specific functions in isoprenoid biosynthesis, and complete loss of FPP synthase activity causes early developmental arrest. Plant J. 63: 512-525.
Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
Coman, D., Altenhoff, A., Zoller, S., Gruissem, W., and Vranova, E. (2014). Distinct evolutionary strategies in the GGPPS family from plants. Front. Plant Sci. 5: 230.
Guo, K., Liu, Y., and Li, S.H. (2021). The untapped potential of plant sesterterpenoids: Chemistry, biological activities and biosynthesis. Nat. Prod. Rep. 38: 2293-2314.
Herde, M., Gartner, K., Kollner, T.G., Fode, B., Boland, W., Gershenzon, J., Gatz, C., and Tholl, D. (2008). Identification and regulation of TPS04/GES, an Arabidopsis geranyllinalool synthase catalyzing the first step in the formation of the insect-induced volatile C-16-homoterpene TMTT. Plant Cell 20: 1152-1168.
Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K., and Pease, L.R. (1989). Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51-59.
Hsieh, F.L., Chang, T.H., Ko, T.P., and Wang, A.H.J. (2011). Structure and mechanism of an Arabidopsis medium/long-chain-length prenyl pyrophosphate synthase. Plant Physiol. 155: 1079-1090.
Huang, A.C., Kautsar, S.A., Hong, Y.J., Medema, M.H., Bond, A.D., Tantillo, D.J., and Osbourn, A. (2017). Unearthing a sesterterpene biosynthetic repertoire in the Brassicaceae through genome mining reveals convergent evolution. Proc. Natl. Acad. Sci. U.S.A. 114: E6005-E6014.
Kainou, T., Okada, K., Suzuki, K., Nakagawa, T., Matsuda, H., and Kawamukai, M. (2001). Dimer formation of octaprenyl-diphosphate synthase (IspB). is essential for chain length determination of ubiquinone. J. Biol. Chem. 276: 7876-7883.
Liu, Y., Luo, S.H., Schmidt, A., Wang, G.D., Sun, G.L., Grant, M., Kuang, C., Yang, M.J., Jing, S.X., Li, C.H., Schneider, B., Gershenzon, J., and Li, S.H. (2016). A geranylfarnesyl diphosphate synthase provides the precursor for sesterterpenoid (C-25). formation in the glandular trichomes of the mint species Leucosceptrum canum. Plant Cell 28: 804-822.
Nagel, R., Berasategui, A., Paetz, C., Gershenzon, J., and Schmidt, A. (2014). Overexpression of an isoprenyl diphosphate synthase in spruce leads to unexpected terpene diversion products that function in plant defense. Plant Physiol. 164: 555-569.
Nagel, R., Bernholz, C., Vranova, E., Kosuth, J., Bergau, N., Ludwig, S., Wessjohann, L., Gershenzon, J., Tissier, A., and Schmidt, A. (2015). Arabidopsis thaliana isoprenyl diphosphate synthases produce the C25 intermediate geranylfarnesyl diphosphate. Plant J. 84: 847-859.
Ruiz-Sola, M.A., Coman, D., Beck, G., Barja, M.V., Colinas, M., Graf, A., Welsch, R., Rutimann, P., Buhlmann, P., Bigler, L., Gruissem, W., Rodríguez-Concepción, M., and Vranova, E. (2015). Arabidopsis GERANYLGERANYL DIPHOSPHATE SYNTHASE 11 is a hub isozyme required for the production of most photosynthesis-related isoprenoids. New Phytol. 209: 252-264.
Ruppel, N.J., Kropp, K.N., Davis, P.A., Martin, A.E., Luesse, D.R., and Hangarter, R.P. (2013). Mutations in geranylgeranyl diphosphate synthase 1 affect chloroplast development in Arabidopsis thaliana (Brassicaceae). Am. J. Bot. 100: 2074-2084.
Sato, T., Yamaga, H., Kashima, S., Murata, Y., Shinada, T., Nakano, C., and Hoshino, T. (2013). Identification of novel sesterterpene/triterpene synthase from Bacillus clausii. Chembiochem 14: 822-825.
Shao, J., Chen, Q.W., Lv, H.J., He, J., Liu, Z.F., Lu, Y.N., Liu, H.L., Wang, G.D., and Wang, Y. (2017). (+)-Thalianatriene and (-)-retigeranin B catalyzed by sesterterpene synthases from Arabidopsis thaliana. Org. Lett. 19: 1816-1819.
Tholl, D., Kish, C.M., Orlova, I., Sherman, D., Gershenzon, J., Pichersky, E., and Dudareva, N. (2004). Formation of monoterpenes in Antirrhinum majus and Clarkia breweri flowers involves heterodimeric geranyl diphosphate synthases. Plant Cell 16: 977-992.
Tholl, D., and Lee, S. (2011). Elucidating the metabolism of plant terpene volatiles: Alternative tools for engineering plant defenses? Recent Adv. Phytochem. 41: 159-178.
Wallrapp, F.H., Pan, J.J., Ramamoorthy, G., Almonacid, D.E., Hillerich, B.S., Seidel, R., Patskovsky, Y., Babbitt, P.C., Almo, S.C., Jacobson, M.P., Poulter, C.D. (2013). Prediction of function for the polyprenyl transferase subgroup in the isoprenoid synthase superfamily. Proc. Natl. Acad. Sci. U.S.A. 110: E1196-E1202.
Wang, C., Chen, Q., Fan, D., Li, J., Wang, G., and Zhang, P. (2016). Structural analyses of short-chain prenyltransferases identify an evolutionarily conserved GFPPS clade in Brassicaceae plants. Mol. Plant 9: 195-204.
Wang, G., and Dixon, R.A. (2009). Heterodimeric geranyl(geranyl).diphosphate synthase from hop (Humulus lupulus). and the evolution of monoterpene biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 106: 9914-9919.
Wei, G., Tian, P., Zhang, F., Qin, H., Miao, H., Chen, Q., Hu, Z., Cao, L., Wang, M., Gu, X., Huang, S., Chen, M., and Wang, G. (2016). Integrative analyses of nontargeted volatile profiling and transcriptome data provide molecular insight into VOC diversity in cucumber plants (Cucumis sativus). Plant Physiol. 172: 603-618.
Yan, L.H., Wei, S.W., Wu, Y.R., Hu, R.L., Li, H.J., Yang, W.C., and Xie, Q. (2015). High-efficiency genome editing in Arabidopsis using YAO promoter-driven CRISPR/Cas9 system. Mol. Plant 8: 1820-1823.
Zhang, J., Ma, Y., Chen, Q., Yang, M., Feng, D., Zhou, F., Wang, G., and Wang, C. (2022). Functional prediction of trans-prenyltransferases reveals the distribution of GFPPSs in species beyond the Brassicaceae clade. Int. J. Mol. Sci. 23: 9471.
Zeng, T., Chen, Y.X.X., Jian, Y.X., Zhang, F., and Wu, R.B. (2022). Chemotaxonomic investigation of plant terpenoids with an established database (TeroMOL). New Phytol. 235: 662-673.
Zhou, F., and Pichersky, E. (2020). The complete functional characterisation of the terpene synthase family in tomato. New Phytol. 226: 1341-1360.
Zhou, F., Wang, C.Y., Gutensohn, M., Jiang, L., Zhang, P., Zhang, D., Dudareva, N., and Lu, S. (2017). A recruiting protein of geranylgeranyl diphosphate synthase controls metabolic flux toward chlorophyll biosynthesis in rice. Proc. Natl. Acad. Sci. U.S.A. 114: 6866-6871.

Auteurs

Yihua Ma (Y)

State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing, 100101, China.
University of Chinese Academy of Sciences, Beijing, 100039, China.

Qingwen Chen (Q)

State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing, 100101, China.

Yaoyao Wang (Y)

State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing, 100101, China.
University of Chinese Academy of Sciences, Beijing, 100039, China.

Fengxia Zhang (F)

State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing, 100101, China.

Chengyuan Wang (C)

Center for Microbes, Development and Health, Institut Pasteur of Shanghai, Chinese Academy of Sciences, Shanghai, 200031, China.

Guodong Wang (G)

State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing, 100101, China.
University of Chinese Academy of Sciences, Beijing, 100039, China.
Center for Microbes, Development and Health, Institut Pasteur of Shanghai, Chinese Academy of Sciences, Shanghai, 200031, China.

Articles similaires

Arabidopsis Arabidopsis Proteins Osmotic Pressure Cytoplasm RNA, Messenger
Genome Size Genome, Plant Magnoliopsida Evolution, Molecular Arabidopsis
Glycine max Photoperiod Ubiquitin-Protein Ligases Flowers Gene Expression Regulation, Plant

Classifications MeSH