Abstract
The sesquiterpene alpha-bisabolol is the predominant active ingredient in essential oils that are highly valued in the cosmetics industry due to its wound healing, anti-inflammatory, and skin-soothing properties. Alpha-bisabolol was thought to be restricted to Compositae plants. Here we reveal that alpha-bisabolol is also synthesized in rice, a non-Compositae plant, where it acts as a novel sesquiterpene phytoalexin. Overexpressing the gene responsible for the biosynthesis of alpha-bisabolol, OsTPS1, conferred bacterial blight resistance in rice. Phylogenomic analyses revealed that alpha-bisabolol-synthesizing enzymes in rice and Compositae evolved independently. Further experiments demonstrated that the natural variation in the disease resistance level was associated with differential transcription of OsTPS1 due to polymorphisms in its promoter. We demonstrated that OsTPS1 was regulated at the epigenetic level by JMJ705 through the methyl jasmonate pathway. These data reveal the cross-family accumulation and regulatory mechanisms of alpha-bisabolol production.
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Akagi, A., Fukushima, S., Okada, K., Jiang, C.J., Yoshida, R., Nakayama, A., Shimono, M., Sugano, S., Yamane, H., and Takatsuji, H. (2014). Wrky45-dependent priming of diterpenoid phytoalexin biosynthesis in rice and the role of cytokinin in triggering the reaction. Plant Mol Biol 86, 171–183.
Alves Gomes Albertti, L., Delatte, T.L., Souza de Farias, K., Galdi Boaretto, A., Verstappen, F., van Houwelingen, A., Cankar, K., Carollo, C.A., Bouwmeester, H.J., and Beekwilder, J. (2018). Identification of the bisabolol synthase in the endangered candeia tree (eremanthus erythropappus (dc) mcleisch). Front Plant Sci 9, 9–1340.
Bart, R., Chern, M., Park, C.J., Bartley, L., and Ronald, P.C. (2006). A novel system for gene silencing using sirnas in rice leaf and stem-derived protoplasts. Plant Methods 2, 13.
Belcher, M.S., Mahinthakumar, J., and Keasling, J.D. (2020). New frontiers: harnessing pivotal advances in microbial engineering for the biosynthesis of plant-derived terpenoids. Curr Opin Biotechnol 65, 88–93.
Bowler, C., Benvenuto, G., Laflamme, P., Molino, D., Probst, A.V., Tariq, M., and Paszkowski, J. (2004). Chromatin techniques for plant cells. Plant J 39, 776–789.
Chen, F., Tholl, D., Bohlmann, J., and Pichersky, E. (2011). The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J 66, 212–229.
Chen, F., Yan, B., Gong, X., Li, H., and He, Z. (2021). Genome sequencing of the bacterial blight pathogen dy89031 reveals its diverse virulence and origins of Xanthomonas oryzae pv. oryzae strains. Sci China Life Sci 64, 2175–2185.
Chen, W., Gao, Y., Xie, W., Gong, L., Lu, K., Wang, W., Li, Y., Liu, X., Zhang, H., Dong, H., et al. (2014). Genome-wide association analyses provide genetic and biochemical insights into natural variation in rice metabolism. Nat Genet 46, 714–721.
Chen, X., Chen, H., Yuan, J.S., Köllner, T.G., Chen, Y., Guo, Y., Zhuang, X., Chen, X., Zhang, Y., Fu, J., et al. (2018). The rice terpene synthase gene OsTPS19 functions as an (S)-limonene synthase in planta, and its overexpression leads to enhanced resistance to the blast fungus Magnaporthe oryzae. Plant Biotechnol J 16, 1778–1787.
Cheng, A.X., Lou, Y.G., Mao, Y.B., Lu, S., Wang, L.J., and Chen, X.Y. (2007a). Plant terpenoids: biosynthesis and ecological functions. J Integra Plant Biol 49, 179–186.
Cheng, A.X., Xiang, C.Y., Li, J.X., Yang, C.Q., Hu, W.L., Wang, L.J., Lou, Y.G., and Chen, X.Y. (2007b). The rice (E)-β-caryophyllene synthase (OsTPS3) accounts for the major inducible volatile sesquiterpenes. Phytochemistry 68, 1632–1641.
Dokku, P., Das, K.M., and Rao, G.J.N. (2013). Genetic enhancement of host plant-resistance of the lalat cultivar of rice against bacterial blight employing marker-assisted selection. Biotechnol Lett 35, 1339–1348.
Fejér, J., and Salamon, I. (2016). Breeding of German chamomile, Matricaria recutita L., with a high content of α-bisabolol. Acta Hortic 1125, 287–292.
Fernandes, M.Y.D., Carmo, M.R.S., Fonteles, A.A., Neves, J.C.S., Silva, A. T.A., Pereira, J.F., Ferreira, E.O., Lima, N.M.R., Neves, K.R.T., and Andrade, G.M. (2019). (-)-α-bisabolol prevents neuronal damage and memory deficits through reduction of proinflammatory markers induced by permanent focal cerebral ischemia in mice. Eur J Pharmacol 842, 270–280.
Gershenzon, J., and Dudareva, N. (2007). The function of terpene natural products in the natural world. Nat Chem Biol 3, 408–414.
Gong, L., Chen, W., Gao, Y., Liu, X., Zhang, H., Xu, C., Yu, S., Zhang, Q., and Luo, J. (2013). Genetic analysis of the metabolome exemplified using a rice population. Proc Natl Acad Sci USA 110, 20320–20325.
Gong, Z., Xiong, L., Shi, H., Yang, S., Herrera-Estrella, L.R., Xu, G., Chao, D.Y., Li, J., Wang, P.Y., Qin, F., et al. (2020). Plant abiotic stress response and nutrient use efficiency. Sci China Life Sci 63, 635–674.
Groussin, A.L., and Antoniotti, S. (2012). Valuable chemicals by the enzymatic modification of molecules of natural origin: terpenoids, steroids, phenolics and related compounds. Bioresource Tech 115, 237–243.
He, K., Mei, H., Zhu, J., Qiu, Q., Cao, X., and Deng, X. (2021). The histone H3K27 demethylase REF6/JMJ12 promotes thermomorphogenesis in Arabidopsis. Natl Sci Rev 9, nwab213.
Jin, C., Fang, C., Yuan, H., Wang, S., Wu, Y., Liu, X., Zhang, Y., and Luo, J. (2015). Interaction between carbon metabolism and phosphate accumulation is revealed by a mutation of a cellulose synthase-like protein, CSLF6. J Exp Bot 66, 2557–2567.
Kadir, R., and Barry, B.W. (1991). A-bisabolol, a possible safe penetration enhancer for dermal and transdermal therapeutics. Int J Pharm 70, 87–94.
Kamatou, G.P.P., and Viljoen, A.M. (2010). A review of the application and pharmacological properties of α-bisabolol and α-bisabolol-rich oils. J Americ Oil Chem Soc 87, 1–7.
Kant, M.R., Ament, K., Sabelis, M.W., Haring, M.A., and Schuurink, R.C. (2004). Differential timing of spider mite-induced direct and indirect defenses in tomato plants. Plant Physiol 135, 483–495.
Kappers, I.F., Aharoni, A., van Herpen, T.W.J.M., Luckerhoff, L.L.P., Dicke, M., and Bouwmeester, H.J. (2005). Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309, 2070–2072.
Kariya, K., Ube, N., Ueno, M., Teraishi, M., Okumoto, Y., Mori, N., Ueno, K., and Ishihara, A. (2020). Natural variation of diterpenoid phytoalexins in cultivated and wild rice species. Phytochemistry 180, 112518.
Kauffman, H.E., Reddy A.P.K., Hsieh S.P.Y., and Merca S.D. (1973). An improved technique for evaluating resistance of rice varieties to Xanthomonas oryzae. Plant Dis Rep 57, 537–541.
Kiryu, M., Hamanaka, M., Yoshitomi, K., Mochizuki, S., Akimitsu, K., and Gomi, K. (2018). Rice terpene synthase 18 (OsTPS18) encodes a sesquiterpene synthase that produces an antibacterial (E)-nerolidol against a bacterial pathogen of rice. J Gen Plant Pathol 84, 221–229.
Kitaoka, N., Zhang, J., Oyagbenro, R.K., Brown, B., Wu, Y., Yang, B., Li, Z., and Peters, R.J. (2020). Interdependent evolution of biosynthetic gene clusters for momilactone production in rice. Plant Cell 33, 290–305.
Köllner, T.G., Held, M., Lenk, C., Hiltpold, I., Turlings, T.C.J., Gershenzon, J., and Degenhardt, J. (2008a). A maize (E)-β-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most american maize varieties. Plant Cell 20, 482–494.
Köllner, T.G., Schnee, C., Li, S., Svatoš, A., Schneider, B., Gershenzon, J., and Degenhardt, J. (2008b). Protonation of a neutral (S)-β-bisabolene intermediate is involved in (S)-β-macrocarpene formation by the maize sesquiterpene synthases TPS6 and TPS11. J Biol Chem 283, 20779–20788.
Lafos, M., Kroll, P., Hohenstatt, M.L., Thorpe, F.L., Clarenz, O., and Schubert, D. (2011). Dynamic regulation of h3k27 trimethylation during Arabidopsis differentiation. PLoS Genet 7, e1002040.
Lee, G.W., Chung, M.S., Kang, M., Chung, B.Y., and Lee, S. (2016). Direct suppression of a rice bacterial blight (Xanthomonas oryzae pv. oryzae) by monoterpene (S)-limonene. Protoplasma 253, 683–690.
Li, J.X., Fang, X., Zhao, Q., Ruan, J.X., Yang, C.Q., Wang, L.J., Miller, D. J., Faraldos, J.A., Allemann, R.K., Chen, X.Y., et al. (2013a). Rational engineering of plasticity residues of sesquiterpene synthases from Artemisia annua: product specificity and catalytic efficiency. Biochem J 451, 417–426.
Li, T., Chen, X., Zhong, X., Zhao, Y., Liu, X., Zhou, S., Cheng, S., and Zhou, D.X. (2013b). Jumonji C domain protein JMJ705-mediated removal of histone H3 lysine 27 trimethylation is involved in defense-related gene activation in rice. Plant Cell 25, 4725–4736.
Li, W., Chern, M., Yin, J., Wang, J., and Chen, X. (2019). Recent advances in broad-spectrum resistance to the rice blast disease. Curr Opin Plant Biol 50, 114–120.
Li, W., Zhu, Z., Chern, M., Yin, J., Yang, C., Ran, L., Cheng, M., He, M., Wang, K., Wang, J., et al. (2017). A natural allele of a transcription factor in rice confers broad-spectrum blast resistance. Cell 170, 114–126.e15.
Liang, J., Liu, J., Brown, R., Jia, M., Zhou, K., Peters, R.J., and Wang, Q. (2018). Direct production of dihydroxylated sesquiterpenoids by a maize terpene synthase. Plant J 94, 847–856.
Liang, J., Shen, Q., Wang, L., Liu, J., Fu, J., Zhao, L., Xu, M., Peters, R.J., and Wang, Q. (2021). Rice contains a biosynthetic gene cluster associated with production of the casbane-type diterpenoid phytoalexin ent-10-oxodepressin. New Phytol 231, 85–93.
Lim, H.S., Kim, S.K., Woo, S.G., Kim, T.H., Yeom, S.J., Yong, W., Ko, Y. J., Kim, S.J., Lee, S.G., and Lee, D.H. (2021). (−)-α-bisabolol production in engineered Escherichia coli expressing a novel (−)-α-bisabolol synthase from the globe artichoke Cynara cardunculus var. scolymus. J Agric Food Chem 69, 8492–8503.
Lu, X., Zhang, J., Brown, B., Li, R., Rodríguez-Romero, J., Berasategui, A., Liu, B., Xu, M., Luo, D., Pan, Z., et al. (2018). Inferring roles in defense from metabolic allocation of rice diterpenoids. Plant Cell 30, 1119–1131.
Ma, Y., Li, W., Mai, J., Wang, J., Wei, Y., Ledesma-Amaro, R., and Ji, X.J. (2021). Engineering Yarrowia lipolytica for sustainable production of the chamomile sesquiterpene (−)-α-bisabolol. Green Chem 23, 780–787.
Mercke, P., Kappers, I.F., Verstappen, F.W.A., Vorst, O., Dicke, M., and Bouwmeester, H.J. (2004). Combined transcript and metabolite analysis reveals genes involved in spider mite induced volatile formation in cucumber plants. Plant Physiol 135, 2012–2024.
Miao, J., Guo, D., Zhang, J., Huang, Q., Qin, G., Zhang, X., Wan, J., Gu, H., and Qu, L.J. (2013). Targeted mutagenesis in rice using crispr-cas system. Cell Res 23, 1233–1236.
Muangphrom, P., Misaki, M., Suzuki, M., Shimomura, M., Suzuki, H., Seki, H., and Muranaka, T. (2019). Identification and characterization of (+)-α-bisabolol and 7-epi-silphiperfol-5-ene synthases from artemisia abrotanum. Phytochemistry 164, 144–153.
Peng, M., Gao, Y., Chen, W., Wang, W., Shen, S., Shi, J., Wang, C., Zhang, Y., Zou, L., Wang, S., et al. (2016). Evolutionarily distinct bahd n-acyltransferases are responsible for natural variation of aromatic amine conjugates in rice. Plant Cell 28, 1533–1550.
Peng, M., Shahzad, R., Gul, A., Subthain, H., Shen, S., Lei, L., Zheng, Z., Zhou, J., Lu, D., Wang, S., et al. (2017). Differentially evolved glucosyltransferases determine natural variation of rice flavone accumulation and uv-tolerance. Nat Commun 8, 1975.
Piasecka, A., Jedrzejczak-Rey, N., and Bednarek, P. (2015). Secondary metabolites in plant innate immunity: conserved function of divergent chemicals. New Phytol 206, 948–964.
Polturak, G., and Osbourn, A. (2021). The emerging role of biosynthetic gene clusters in plant defense and plant interactions. PLoS Pathog 17, e1009698.
Pu, Q., Liang, J., Shen, Q., Fu, J., Pu, Z., Liu, J., Wang, X., and Wang, Q. (2019). A wheat β-patchoulene synthase confers resistance against herbivory in transgenic Arabidopsis. Genes 10, 441.
Quadrana, L., Almeida, J., Asís, R., Duffy, T., Dominguez, P.G., Bermúdez, L., Conti, G., Corrêa da Silva, J.V., Peralta, I.E., Colot, V., et al. (2014). Natural occurring epialleles determine vitamin e accumulation in tomato fruits. Nat Commun 5, 4027.
Roudier, F., Ahmed, I., Bérard, C., Sarazin, A., Mary-Huard, T., Cortijo, S., Bouyer, D., Caillieux, E., Duvernois-Berthet, E., Al-Shikhley, L., et al. (2011). Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J 30, 1928–1938.
Schnee, C., Kollner, T.G., Gershenzon, J., and Degenhardt, J.. (2002). The maize gene terpene synthase 1 encodes a sesquiterpene synthase catalyzing the formation of (E)-β-farnesene, (E)-nerolidol, and (E,E)-farnesol after herbivore damage. Plant Physiol 130, 2049–2060.
Scossa, F., Brotman, Y., de Abreu e Lima, F., Willmitzer, L., Nikoloski, Z., Tohge, T., and Fernie, A.R. (2016). Genomics-based strategies for the use of natural variation in the improvement of crop metabolism. Plant Sci 242, 47–64.
Shimizu, T., Lin, F., Hasegawa, M., Okada, K., Nojiri, H., and Yamane, H. (2012). Purification and identification of naringenin 7-O-methyltransferase, a key enzyme in biosynthesis of flavonoid phytoalexin sakuranetin in rice. J Biol Chem 287, 19315–19325.
Swaminathan, S., Morrone, D., Wang, Q., Fulton, D.B., and Peters, R.J. (2009). CYP76M7 is an ent-cassadiene C11α-hydroxylase defining a second multifunctional diterpenoid biosynthetic gene cluster in rice. Plant Cell 21, 3315–3325.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). Mega6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30, 2725–2729.
Tan, F., Lu, Y., Jiang, W., Wu, T., Zhang, R., Zhao, Y., and Zhou, D.X. (2018). Ddm1 represses noncoding RNA expression and RNA-directed DNA methylation in heterochromatin. Plant Physiol 177, 1187–1197.
Tian, X., Ruan, J.X., Huang, J.Q., Yang, C.Q., Fang, X., Chen, Z.W., Hong, H., Wang, L.J., Mao, Y.B., Lu, S., et al. (2018). Characterization of gossypol biosynthetic pathway. Proc Natl Acad Sci USA 115, E5410–E5418.
Uji, Y., Taniguchi, S., Tamaoki, D., Shishido, H., Akimitsu, K., and Gomi, K. (2016). Overexpression of OsMYC2 results in the up-regulation of early JA-rresponsive genes and bacterial blight resistance in rice. Plant Cell Physiol 57, 1814–1827.
Wang, J., Long, X., Chern, M., and Chen, X. (2021). Understanding the molecular mechanisms of trade-offs between plant growth and immunity. Sci China Life Sci 64, 234–241.
Wang, Q., Hillwig, M.L., Okada, K., Yamazaki, K., Wu, Y., Swaminathan, S., Yamane, H., and Peters, R.J. (2012). Characterization of CYP76M58 indicates metabolic plasticity within a plant biosynthetic gene cluster. J Biol Chem 287, 6159–6168.
Wen, W., Li, D., Li, X., Gao, Y., Li, W., Li, H., Liu, J., Liu, H., Chen, W., Luo, J., et al. (2014). Metabolome-based genome-wide association study of maize kernel leads to novel biochemical insights. Nat Commun 5, 3438.
Wu, Y., Hillwig, M.L., Wang, Q., and Peters, R.J. (2011). Parsing a multifunctional biosynthetic gene cluster from rice: biochemical characterization of CYP71Z6 & 7. FEBS Lett 585, 3446–3451.
Wu, Y., Wang, Q., Hillwig, M.L., and Peters, R.J. (2013). Picking sides: distinct roles for CYP76M6 and CYP76M8 in rice oryzalexin biosynthesis. Biochem J 454, 209–216.
Xue, J., Lu, Z., Liu, W., Wang, S., Lu, D., Wang, X., and He, X. (2021). The genetic arms race between plant and xanthomonas: lessons learned from tale biology. Sci China Life Sci 64, 51–65.
Yang, C.Q., Wu, X.M., Ruan, J.X., Hu, W.L., Mao, Y.B., Chen, X.Y., and Wang, L.J. (2013). Isolation and characterization of terpene synthases in cotton (Gossypium hirsutum). Phytochemistry 96, 46–56.
Yokotani, N., Sato, Y., Tanabe, S., Chujo, T., Shimizu, T., Okada, K., Yamane, H., Shimono, M., Sugano, S., Takatsuji, H., et al. (2013). Wrky76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance. J Exp Bot 64, 5085–5097.
Yu, N., Nützmann, H.W., MacDonald, J.T., Moore, B., Field, B., Berriri, S., Trick, M., Rosser, S.J., Kumar, S.V., Freemont, P.S., et al. (2016). Delineation of metabolic gene clusters in plant genomes by chromatin signatures. Nucleic Acids Res 44, 2255–2265.
Zhan, C., Lei, L., Liu, Z., Zhou, S., Yang, C., Zhu, X., Guo, H., Zhang, F., Peng, M., Zhang, M., et al. (2020). Selection of a subspecies-specific diterpene gene cluster implicated in rice disease resistance. Nat Plants 6, 1447–1454.
Zhang, B., Zhang, H., Li, F., Ouyang, Y., Yuan, M., Li, X., Xiao, J., and Wang, S. (2020). Multiple alleles encoding atypical NLRs with unique central tandem repeats in rice confer resistance to Xanthomonas oryzae pv. oryzae. Plant Commun 1, 100088.
Zhang, H., Tao, Z., Hong, H., Chen, Z., Wu, C., Li, X., Xiao, J., and Wang, S. (2016). Transposon-derived small RNA is responsible for modified function of WRKY45 locus. Nat Plants 2, 16016.
Zhang, H., Wang, Y., Deng, C., Zhao, S., Zhang, P., Feng, J., Huang, W., Kang, S., Qian, Q., Xiong, G., et al. (2022). High-quality genome assembly of Huazhan and Tianfeng, the parents of an elite rice hybrid Tian-you-hua-zhan. Sci China Life Sci 65, 398–411.
Zhang, X., Clarenz, O., Cokus, S., Bernatavichute, Y.V., Pellegrini, M., Goodrich, J., and Jacobsen, S.E. (2007). Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol 5, e129.
Zhang, Y., Chen, K., Zhao, F.J., Sun, C., Jin, C., Shi, Y., Sun, Y., Li, Y., Yang, M., Jing, X., et al. (2018). OsATX1 interacts with heavy metal P1B-type ATPases and affects copper transport and distribution. Plant Physiol 178, 329–344.
Zhao, L., Xie, L., Zhang, Q., Ouyang, W., Deng, L., Guan, P., Ma, M., Li, Y., Zhang, Y., Xiao, Q., et al. (2020). Integrative analysis of reference epigenomes in 20 rice varieties. Nat Commun 11, 2658.
Zhou, S., Liu, X., Zhou, C., Zhou, Q., Zhao, Y., Li, G., and Zhou, D.X. (2016). Cooperation between the H3K27me3 chromatin marker and non-CG methylation in epigenetic regulation. Plant Physiol 172, 1131–1141.
Zhuang, X., Köllner, T.G., Zhao, N., Li, G., Jiang, Y., Zhu, L., Ma, J., Degenhardt, J., and Chen, F. (2012). Dynamic evolution of herbivore-induced sesquiterpene biosynthesis in sorghum and related grass crops. Plant J 69, 70–80.
Zi, J., Mafu, S., and Peters, R.J. (2014). To gibberellins and beyond! Surveying the evolution of (di)terpenoid metabolism. Annu Rev Plant Biol 65, 259–286.
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This work was supported by the Hainan Major Science and Technology Project (ZDKJ202002), the National Natural Science Foundation of China (32100318), China Postdoctoral Science Foundation (2021TQ0093), Hainan Yazhou Bay Seed Laboratory (B21Y10904), the Hainan Academician Innovation Platform (HD-YSZX-202003, HD-YSZX-202004), the Hainan University Startup Fund (KYQD(ZR)1866), Hainan Provincial Natural Science Foundation of China (322RC573), and Hainan Provincial Natural Science Foundation of China (321QN184).
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Zhan, C., Lei, L., Guo, H. et al. Disease resistance conferred by components of essential chrysanthemum oil and the epigenetic regulation of OsTPS1. Sci. China Life Sci. 66, 1108–1118 (2023). https://doi.org/10.1007/s11427-022-2241-0
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DOI: https://doi.org/10.1007/s11427-022-2241-0