Abstract
Main conclusion
Santalum album (E,E)-α-farnesene synthase catalyzes FPP into (E,E)-α-farnesene. Overexpression of the SaAFS gene positively improved cold stress tolerance through JA biosynthesis and signaling pathways in Arabidopsis.
Abstract
Volatile terpenoids are released from plants that suffer negative effects following exposure to various biotic and abiotic stresses. Recent studies revealed that (E,E)-α-farnesene synthase (AFS) plays a significant role in a plant’s defence against biotic attack. However, little is known about whether AFS contributes to plant resistance to cold stress. In this study, a SaAFS gene was isolated from Indian sandalwood (Santalum album L.) and functionally characterized. The SaAFS protein mainly converts farnesyl diphosphate to (E,E)-α-farnesene. SaAFS was clustered into the AFS clade from angiosperms, suggesting a highly conserved enzyme. SaAFS displayed a significant response to cold stress and methyl jasmonate. SaAFS overexpression (OE) in Arabidopsis enhanced cold tolerance by increasing proline content, reducing malondialdehyde content, electrolyte leakage, and accumulating reactive oxygen species. Transcriptomic analysis revealed that upregulated genes related to stress response and JA biosynthesis and signaling were detected in SaAFS-OE lines compared with wild type plants that were exposed to cold stress. Endogenous JA and jasmonoyl-isoleucine content increased significantly in SaAFS-OE lines exposed to cold stress. Collectively considered, these results suggest that the SaAFS gene is a positive regulator during cold stress tolerance via JA biosynthesis and signaling pathways.
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Data availability statement
The raw RNA-seq data were deposited in the Sequence Read Archive database (accession number from SRR23283351 to SRR23283374).
Abbreviations
- AFS:
-
(E,E)-α-Farnesene synthase
- CBF:
-
C-repeat (CRT)-binding factor
- CORs:
-
Cold-responsive genes
- FPP:
-
Farnesyl diphosphate
- GP:
-
Germination percentage
- GPP:
-
Geranyl diphosphate
- JA:
-
Jasmonic acid
- MDA:
-
Malondialdehyde
- ROS:
-
Reactive oxygen species
- TPS:
-
Terpene synthase
References
Abbas F, Ke YG, Zhou YW, Ashraf U, Li XY, Yu YY, Yue YC, Ahmad KW, Yu RC, Fan YP (2020) Molecular cloning, characterization and expression analysis of LoTPS2 and LoTPS4 involved in floral scent formation in oriental hybrid Lilium variety “Siberia.” Phytochemistry 173:112294. https://doi.org/10.1016/j.phytochem.2020.112294
Alcázar R, Cuevas JC, Planas J, Zarza X, Bortolotti C, Carrasco P, Salinas J, Tiburcio AF, Altabella T (2011) Integration of polyamines in the cold acclimation response. Plant Sci 180(1):31–38. https://doi.org/10.1016/j.plantsci.2010.07.022
Baldovini N, Delasalle C, Joulain D (2011) Phytochemistry of the heartwood from fragrant Santalum species: a review. Flavour Frag J 26(1):7–26. https://doi.org/10.1002/ffj.2025
Ballaré CL (2011) Jasmonate-induced defenses: a tale of intelligence, collaborators and rascals. Trends Plant Sci 16(5):249–257. https://doi.org/10.1016/j.tplants.2010.12.001
Boncan DAT, Tsang SSK, Li C, Lee IHT, Lam HM, Chan TF, Hui JHL (2020) Terpenes and terpenoids in plants: interactions with environment and insects. Int J Mol Sci 21(19):7382. https://doi.org/10.3390/ijms21197382
Chen THH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5(3):250–257. https://doi.org/10.1016/s1369-5266(02)00255-8
Chen F, Tholl D, Bohlmann J, 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(1):212–229. https://doi.org/10.1111/j.1365-313X.2011.04520.x
Chen XJ, Chen H, Yuan JS, Köllner TG, Chen YY, Guo YF, Zhuang XF, Chen XL, Zhang YJ, Fu JY, Nebenführ A, Guo ZJ, Chen F (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(10):1778–1787. https://doi.org/10.1111/pbi.12914
Chini A, Fonseca S, Fernández G, Adie B, Chico JM, Lorenzo O, García-Casado G, López-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671. https://doi.org/10.1038/nature06006
Chinnusamy V, Zhu JH, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12(10):444–451. https://doi.org/10.1016/j.tplants.2007.07.002
Clough SJ, Bent AF (1998) Floral dip a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. https://doi.org/10.1046/j.1365-313x.1998.00343.x
Copolovici L, Kännaste A, Pazouki L, Niinemets U (2012) Emissions of green leaf volatiles and terpenoids from Solanum lycopersicum are quantitatively related to the severity of cold and heat shock treatments. J Plant Physiol 169(7):664–672. https://doi.org/10.1016/j.jplph.2011.12.019
Cuevas JC, López-Cobollo R, Alcázar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol 148(2):1094–1105. https://doi.org/10.1104/pp.108.122945
Danner H, Boeckler GA, Irmisch S, Yuan JS, Chen F, Gershenzon J, Unsicker SB, Köllner TG (2011) Four terpene synthases produce major compounds of the gypsy moth feeding-induced volatile blend of Populus trichocarpa. Phytochemistry 72(9):897–908. https://doi.org/10.1016/j.phytochem.2011.03.014
Dave A, Hernández ML, He ZS, Andriotis VME, Vaistij FE, Larson TR, Graham IA (2011) 12-Oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis. Plant Cell 23(2):583–599. https://doi.org/10.1105/tpc.110.081489
Du H, Liu HB, Xiong LZ (2013) Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice. Front Plant Sci 4:397. https://doi.org/10.3389/fpls.2013.00397
Fu JH, Chu JF, Sun XH, Wang JD, Yan CY (2012) Simple, rapid, and simultaneous assay of multiple carboxy containing phytohormones in wounded tomatoes by UPLC-MS/MS using single SPE purification and isotope dilution. Anal Sci 28:1081–1087. https://doi.org/10.2116/analsci.28.1081
Gao-Takai M, Katayama-Ikegami A, Matsuda K, Shindo H, Uemae S, Oyaizu M (2019) A low temperature promotes anthocyanin biosynthesis but does not accelerate endogenous abscisic acid accumulation in red-skinned grapes. Plant Sci 283:165–176. https://doi.org/10.1016/j.plantsci.2019.01.015
Gapper NE, Bai J, Whitaker BD (2006) Inhibition of ethylene-induced α-farnesene synthase gene PcAFS1 expression in ‘d’Anjou’ pears with 1-MCP reduces synthesis and oxidation of α-farnesene and delays development of superficial scald. Postharvest Biol Technol 41(3):225–233. https://doi.org/10.1016/j.postharvbio.2006.04.014
Hamachi A, Nisihara M, Saito S, Rim H, Takahashi H, Islam M, Uemura T, Ohnishi T, Ozawa R, Maffei ME, Arimura GI (2019) Overexpression of geraniol synthase induces heat stress susceptibility in Nicotiana tabacum. Planta 249(1):235–249. https://doi.org/10.1007/s00425-018-3054-z
Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15(3):176–184. https://doi.org/10.1016/j.tplants.2010.01.006
Hong GJ, Xue XY, Mao YB, Wang LJ, Chen XY (2012) Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24(6):2635–2648. https://doi.org/10.1105/tpc.112.098749
Hou XL, Zhou JN, Liu C, Liu L, Shen LS, Yu H (2014) Nuclear factor Y-mediated H3K27me3 demethylation of the SOC1 locus orchestrates flowering responses of Arabidopsis. Nat Commun 5:4601. https://doi.org/10.1038/ncomms5601
Hu YR, Jiang LQ, Wang F, Yu DQ (2013) Jasmonate regulates the inducer of CBF expression-C-repeat binding factor/DRE binding factor1 cascade and freezing tolerance in Arabidopsis. Plant Cell 25(8):2907–2924. https://doi.org/10.1105/tpc.113.112631
Huelin FE, Murray KE (1966) Alpha-farnesene in the natural coating of apples. Nature 210:1260–1261. https://doi.org/10.1038/2101260a0
Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 20(4):219–229. https://doi.org/10.1016/j.tplants.2015.02.001
Kim YS, Lee M, Lee JH, Lee HJ, Park CM (2015) The unified ICE-CBF pathway provides a transcriptional feedback control of freezing tolerance during cold acclimation in Arabidopsis. Plant Mol Biol 89(1–2):187–201. https://doi.org/10.1007/s11103-015-0365-3
Kim TH, Hatano T, Okamoto K, Yoshida T, Kanzaki H, Arita M, Ito H (2017) Antifungal and ichthyotoxic sesquiterpenoids from Santalum album heartwood. Molecules 22(7):1139. https://doi.org/10.3390/molecules22071139
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054
Li R, Wang M, Wang Y, Schuman MC, Weinhold A, Schäfer M, Jiménez-Alemán GH, Barthel A, Baldwin IT (2017) Flower-specific jasmonate signaling regulates constitutive floral defenses in wild tobacco. Proc Natl Acad Sci USA 114(34):E7205–E7214. https://doi.org/10.1073/pnas.1703463114
Lin JY, Wang D, Chen XL, Köllner TG, Mazarei M, Guo H, Pantalone VR, Arelli P, Stewart CN Jr, Wang NN, Chen F (2017) An (E, E)-alpha-farnesene synthase gene of soybean has a role in defence against nematodes and is involved in synthesizing insect-induced volatiles. Plant Biotechnol J 15(4):510–519. https://doi.org/10.1111/pbi.12649
Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBPAP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406. https://doi.org/10.1105/tpc.10.8.1391
Liu HR, Cao XM, Liu XH, Xin R, Wang JJ, Gao J, Wu BP, Gao LX, Xu CJ, Zhang B, Grierson D, Chen KS (2017) UV-B irradiation differentially regulates terpene synthases and terpene content of peach. Plant Cell Environ 40(10):2261–2275. https://doi.org/10.1111/pce.13029
Martin DM, Fäldt J, Bohlmann J (2004) Functional characterization of nine Norway Spruce TPS genes and evolution of gymnosperm terpene synthases of the TPS-d subfamily. Plant Physiol 135(4):1908–1927. https://doi.org/10.1104/pp.104.042028
Martin DM, Aubourg S, Schouwey MB, Daviet L, Schalk M, Toub O, Lund ST, Bohlmann J (2010) Functional annotation, genome organization and phylogeny of the grapevine (Vitis vinifera) terpene synthase gene family based on genome assembly. BMC Plant Biol 10:226. https://doi.org/10.1186/1471-2229-10-226
Mercke P, Kappers IF, Verstappen FWA, Vorst O, Dicke M, Bouwmeester HJ (2004) Combined transcript and metabolite analysis reveals genes involved in spider mite induced volatile formation in cucumber plants. Plant Physiol 135(4):2012–2024. https://doi.org/10.1104/pp.104.048116
Ming RH, Zhang Y, Wang Y, Khan M, Dahro B, Liu JH (2021) The JA-responsive MYC2-BADH-like transcriptional regulatory module in Poncirus trifoliata contributes to cold tolerance by modulation of glycine betaine biosynthesis. New Phytol 229(5):2730–2750. https://doi.org/10.1111/nph.17063
Murashige T, Skoog F (1962) A revised medium for growth and bioassays with tobacco tissue culture. Physiol Plant 15(3):473–497
Nieuwenhuizen NJ, Wang MY, Matich AJ, Green SA, Chen X, Yauk YK, Beuning LL, Nagegowda DA, Dudareva N, Atkinson RG (2009) Two terpene synthases are responsible for the major sesquiterpenes emitted from the flowers of kiwifruit (Actinidia deliciosa). J Exp Bot 60(11):3203–3219. https://doi.org/10.1093/jxb/erp162
O’Brien JA, Daudi A, Butt VS, Bolwell GP (2012) Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 236(3):765–779. https://doi.org/10.1007/s00425-012-1696-9
Pazouki L, Kanagendran A, Li S, Kannaste A, Memari HR, Bichele R, Niinemets U (2016) Mono- and sesquiterpene release from tomato (Solanum lycopersicum) leaves upon mild and severe heat stress and through recovery: from gene expression to emission responses. Environ Exp Bot 132:1–15. https://doi.org/10.1016/j.envexpbot.2016.08.003
Pechous SW, Whitaker BD (2004) Cloning and functional expression of an (E, E)-alpha-farnesene synthase cDNA from peel tissue of apple fruit. Planta 219(1):84–94. https://doi.org/10.1007/s00425-003-1191-4
Pichersky E, Raguso RA (2018) Why do plants produce so many terpenoid compounds? New Phytol 220(3):692–702. https://doi.org/10.1111/nph.14178
Shan XY, Zhang YS, Peng W, Wang ZL, Xie DX (2009) Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis. J Exp Bot 60(13):3849–3860. https://doi.org/10.1093/jxb/erp223
Shan XY, Wang JX, Chua LL, Jiang D, Peng W, Xie DX (2011) The role of Arabidopsis Rubisco activase in jasmonate-induced leaf senescence. Plant Physiol 155(2):751–764. https://doi.org/10.1104/pp.110.166595
Shen Q, Lu X, Yan TX, Fu XQ, Lv ZY, Zhang FY, Pan QF, Wang GF, Sun XF, Tang KX (2016) The jasmonate-responsive AaMYC2 transcription factor positively regulates artemisinin biosynthesis in Artemisia annua. New Phytol 210(4):1269–1281. https://doi.org/10.1111/nph.13874
Souleyre EJF, Bowen JK, Matich AJ, Tomes S, Chen XY, Hunt MB, Wang MY, Ileperuma NR, Richards K, Rowan DD, Chagne D, Atkinson RG (2019) Genetic control of alpha-farnesene production in apple fruit and its role in fungal pathogenesis. Plant J 100(6):1148–1162. https://doi.org/10.1111/tpj.14504
Thines B, Katsir L, Melotto M, Niu YJ, Mandaokar A, Liu GH, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448(7154):661–665. https://doi.org/10.1038/nature05960
Tholl D, Sohrabi R, Huh JH, Lee S (2011) The biochemistry of homoterpenes-common constituents of floral and herbivore-induced plant volatile bouquets. Phytochemistry 72(13):1635–1646. https://doi.org/10.1016/j.phytochem.2011.01.019
Vranová E, Coman D, Gruissem W (2013) Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annu Rev Plant Biol 64:665–700. https://doi.org/10.1146/annurev-arplant-050312-120116
Wang F, Guo Z, Li H, Wang M, Onac E, Zhou J, Xia X, Shi K, Yu J, Zhou Y (2016) Phytochrome A and B function antagonistically to regulate cold tolerance via abscisic acid-dependent jasmonate signaling. Plant Physiol 170:459–471. https://doi.org/10.1104/pp.15.01171
Wang XW, Zeng LT, Liao YY, Li JL, Tang JC, Yang ZY (2019) Formation of alpha-farnesene in tea (Camellia sinensis) leaves induced by herbivore-derived wounding and its effect on neighboring tea plants. Int J Mol Sci 20:4151. https://doi.org/10.3390/ijms20174151
Xie XK, Kirby J, Keasling JD (2012a) Functional characterization of four sesquiterpene synthases from Ricinus communis (castor bean). Phytochemistry 78:20–28. https://doi.org/10.1016/j.phytochem.2012.02.022
Xie XB, Li S, Zhang RF, Zhao J, Chen YC, Zhao Q, Yao YX, You CX, Zhang XS, Hao YJ (2012b) The bHLH transcription factor MdbHLH3 promotes anthocyanin accumulation and fruit colouration in response to low temperature in apples. Plant Cell Environ 35(11):1884–1897. https://doi.org/10.1111/j.1365-3040.2012.02523.x
Xu YH, Zhang Z, Wang MX, Wei JH, Chen HJ, Gao ZH, Sui C, Luo HM, Zhang XL, Yang Y, Meng H, Li WL (2013) Identification of genes related to agarwood formation transcriptome analysis of healthy and wounded tissues of Aquilaria sinensis. BMC Genom 14:227. https://doi.org/10.1186/1471-2164-14-227
Yan JB, Zhang C, Gu M, Bai ZY, Zhang WG, Qi TC, Cheng ZW, Peng W, Luo HB, Nan FJ, Wang Z, Xie DX (2009) The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21(8):2220–2236. https://doi.org/10.1105/tpc.109.065730
Yao MM, Ge WY, Zhou Q, Zhou X, Luo ML, Zhao YB, Wei BD, Ji SJ (2021) Exogenous glutathione alleviates chilling injury in postharvest bell pepper by modulating the ascorbate-glutathione (AsA-GSH) cycle. Food Chem 352:129458. https://doi.org/10.1016/j.foodchem.2021.129458
Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2(7):1565–1572. https://doi.org/10.1038/nprot.2007.199
Zhang XH, Teixeira da Silva JA, Niu MY, Li MZ, He CM, Zhao JH, Zeng SJ, Duan J, Ma GH (2017) Physiological and transcriptomic analyses reveal a response mechanism to cold stress in Santalum album L. leaves. Sci Rep 7:42165. https://doi.org/10.1038/srep42165
Zhang XH, Niu MY, Teixeira da Silva JA, Zhang YY, Yuan YF, Jia YX, Xiao YY, Li Y, Fang L, Zeng SJ, Ma GH (2019) Identification and functional characterization of three new terpene synthase genes involved in chemical defense and abiotic stresses in Santalum album. BMC Plant Biol 19(1):115. https://doi.org/10.1186/s12870-019-1720-3
Zhang XH, Teixeira da Silva JA, Niu MY, Zhang T, Liu HF, Zheng F, Yuan YF, Li Y, Fang L, Zeng SJ, Ma GH (2021) Functional characterization of an Indian sandalwood (Santalum album L.) dual-localized bifunctional nerolidol/linalool synthase gene involved in stress response. Phytochemistry 183:112610. https://doi.org/10.1016/j.phytochem.2020.112610
Zhao ML, Wang JN, Shan W, Fan JG, Kuang JF, Wu KQ, Li XP, Chen WX, He FY, Chen JY, Lu WJ (2013) Induction of jasmonate signalling regulators MaMYC2s and their physical interactions with MaICE1 in methyl jasmonate-induced chilling tolerance in banana fruit. Plant Cell Environ 36(1):30–51. https://doi.org/10.1111/j.1365-3040.2012.02551.x
Zhao CZ, Lang ZB, Zhu JK (2015) Cold responsive gene transcription becomes more complex. Trends Plant Sci 20(8):466–468. https://doi.org/10.1016/j.tplants.2015.06.001
Zhao CZ, Zhang ZJ, Xie SJ, Si T, Li YY, Zhu JK (2016) Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis. Plant Physiol 171(4):2744–2759. https://doi.org/10.1104/pp.16.00533
Zhou Y, Zeng LT, Liu XY, Gui JD, Mei X, Fu XM, Dong F, Tang JC, Zhang LY, Yang ZY (2017) Formation of (E)-nerolidol in tea (Camellia sinensis) leaves exposed to multiple stresses during tea manufacturing. Food Chem 231:78–86. https://doi.org/10.1016/j.foodchem.2017.03.122
Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167(2):313–324. https://doi.org/10.1016/j.cell.2016.08.029
Acknowledgements
This study was financially supported by the National Natural Science Foundation of China (32171841, 31870666), Guangdong Basic and Applied Basic Research Foundation (2019A1515011590 and 2021A1515012068) and Guangdong Special Support Program (2017TQ04N303).
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Zhang, X., Chen, X., Teixeira da Silva, J.A. et al. Characterization of sandalwood (E,E)-α-farnesene synthase whose overexpression enhances cold tolerance through jasmonic acid biosynthesis and signaling in Arabidopsis. Planta 258, 54 (2023). https://doi.org/10.1007/s00425-023-04212-1
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DOI: https://doi.org/10.1007/s00425-023-04212-1