Abstract
Background and aims
Conyza blinii is a unique traditional Chinese medicine growing in Sichuan, China, which has soils with an abundant iron content. This Fe-enriched environment contributes to a variety of terpenoids in C. blinii, such as blinin and saponin, which play an important role in the process of resisting abiotic stress. The relationship between Fe and terpenoid metabolism was studied to explore the Fe tolerance mechanism of C. blinii.
Methods
In this study, C. blinii was treated with ferrous iron solutions, and the effect of ferrous iron on the synthesis of blinin and saponins was further studied by spectrophotometry and liquid chromatography. Additionally, gene expression was detected by qRT-PCR.
Results
Under ferrous treatment, the blinin content of C. blinii increased, while the total saponin content decreased. When the ferrous concentration reached 200 μM, the difference in metabolite production was the largest. Furthermore, it was found that blinin and saponins have synchronous and opposite accumulation trends, characterized by time dependence. The gene expression results of key enzymes in the MVA and MEP pathways showed the same trends. In this process, the expression of CbNudixs played a key role in switching the material flux between MVA and MEP by catalyzing the dephosphorylation of isoprenoid diphosphate.
Conclusions
In this study, it was found that under ferrous iron stimulation, the terpenoid content in C. blinii was different, and the metabolic pathways of MVA and MEP were periodically regulated.
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References
Aharoni A, Giri AP, Deuerlein S et al (2003) Terpenoid metabolism in wild-type and transgenic arabidopsis plants. Plant Cell 15:2866–2884. https://doi.org/10.1105/tpc.016253
Arimura GI, Ozawa R, Kugimiya S et al (2004) Herbivore-induced defense response in a model legume. Two-spotted spider mites induce emission of (E)-β-ocimene and transcript accumulation of (E)-β-ocimene synthase in Lotus japonicus. Plant Physiol 135:1976–1983. https://doi.org/10.1104/pp.104.042929
Audebert A, Fofana M (2009) Rice yield gap due to iron toxicity in West Africa. J Agron Crop Sci 195:66–76. https://doi.org/10.1111/j.1439-037X.2008.00339.x
Bartram S, Jux A, Gleixner G, Boland W (2006) Dynamic pathway allocation in early terpenoid biosynthesis of stress-induced lima bean leaves. Phytochemistry 67:1661–1672. https://doi.org/10.1016/j.phytochem.2006.02.004
Bashir K, Ishimaru Y, Shimo H et al (2011) The rice mitochondrial iron transporter is essential for plant growth. Nat Commun. https://doi.org/10.1038/ncomms1326
Becker M, Asch F (2005) Iron toxicity in rice-conditions and management concepts. J Plant Nutr Soil Sci 168:558–573
Becker R, Manteuffel R, Neumann D, Scholz G (1998) Excessive iron accumulation in the pea mutants dgl and brz: subcellular localization of iron and ferritin. Planta 207:217–223. https://doi.org/10.1007/s004250050475
Bick JA, Lange BM (2003) Metabolic cross talk between cytosolic and plastidial pathways of isoprenoid biosynthesis: unidirectional transport of intermediates across the chloroplast envelope membrane. Arch Biochem Biophys 415:146–154. https://doi.org/10.1016/S0003-9861(03)00233-9
Chen F, Tholl D, D’Auria JC et al (2003) Biosynthesis and emission of terpenoid volatiles from arabidopsis flowers. Plant Cell 15:481–494. https://doi.org/10.1105/tpc.007989
Chen C, Chen H, He Y, Xia R (2018) TBtools, a Toolkit for Biologists integrating various biological data handling tools with a user-friendly interface. bioRxiv
Cheng AX, Lou YG, Mao YB et al (2007) Plant terpenoids: biosynthesis and ecological functions. J Integr Plant Biol 49:179–186. https://doi.org/10.1111/j.1744-7909.2007.00395.x
Connolly EL, Lou GM (2002) Iron stress in plants. Genome Biol 3:1–4. https://doi.org/10.1186/gb-2002-3-8-reviews1024
Crichton RR, Ward RJ (1992) Iron metabolism-new perspectives in view. Biochemistry 31:11255–11264. https://doi.org/10.1021/bi00161a001
Dellas N, Thomas ST, Manning G, Noel JP (2013) Discovery of a metabolic alternative to the classical mevalonate pathway. Elife 2:1–18. https://doi.org/10.7554/elife.00672
Fuglsang AT, Paez-Valencia J, Gaxiola RA (2011) Plant proton pumps: regulatory circuits involving H+-ATPase and H+-PPase BT—transporters and pumps in plant signaling, Geisler M, Venema K (eds). Springer, Berlin, pp 39–64
Gong X, Guo C, Terachi T et al (2015) Tobacco PIC1 mediates iron transport and regulates chloroplast development. Plant Mol Biol Rep 33:401–413. https://doi.org/10.1007/s11105-014-0758-5
Henry LK, Gutensohn M, Thomas ST et al (2015) Orthologs of the archaeal isopentenyl phosphate kinase regulate terpenoid production in plants. Proc Natl Acad Sci USA 112:10050–10055. https://doi.org/10.1073/pnas.1504798112
Henry LK, Thomas ST, Widhalm JR et al (2018) Contribution of isopentenyl phosphate to plant terpenoid metabolism. Nat Plants 4:721–729. https://doi.org/10.1038/s41477-018-0220-z
Imsande J (2010) Iron, sulfur, and chlorophyll deficiencies: a need for an integrative approach in plant physiology. Physiol Plant 103:139–144
Iranshahi M, Kalategi F, Rezaee R et al (2008) Cancer chemopreventive activity of terpenoid coumarins from Ferula species. Planta Med 74:147–150. https://doi.org/10.1055/s-2008-1034293
Kannan S (1981) Regulation of Fe-stress response in some crop varieties: anomaly of a mechanism for recovery through non-redumptive PH reduction. J Plant Nutr 4:1–19. https://doi.org/10.1080/01904168109362896
Keeling CI, Bohlmann J (2012) Natural products in chemical biology 5. Plant terpenoids. In: Natural products in chemical biology, pp 127–142
Kleine S, Müller C (2014) Drought stress and leaf herbivory affect root terpenoid concentrations and growth of Tanacetum vulgare. J Chem Ecol 40:1115–1125. https://doi.org/10.1007/s10886-014-0505-2
Kraszewska E (2008) The plant Nudix hydrolase family. Acta Biochim Pol 55:663–671. https://doi.org/10.18388/abp.2008_3025
Laule O, Fürholz A, Chang HS et al (2003) Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 100:6866–6871. https://doi.org/10.1073/pnas.1031755100
Li G, Xu W, Kronzucker HJ, Shi W (2015) Ethylene is critical to the maintenance of primary root growth and Fe homeostasis under Fe stress in Arabidopsis. J Exp Bot 66:2041–2054. https://doi.org/10.1093/jxb/erv005
Liu R, Yi H, Li W et al (2019) Characteristics and evaluation of heavy metal pollution in soil and near-surface atmospheric dust of typical mining cities in Southwest China—a case study from Panzhihua city. Mineral Petrol 39:111–119
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Ma L, Liu H, Qin P et al (2017) Saponin fraction isolated from Conyza blinii H.Lev. demonstrates strong anti-cancer activity that is due to its NF-kappaB inhibition. Biochem Biophys Res Commun 483:779–785. https://doi.org/10.1016/j.bbrc.2016.12.066
McCandliss RJ, Herrmann KM (1978) Iron, an essential element for biosynthesis of aromatic compounds. Proc Natl Acad Sci USA 75:4810–4813. https://doi.org/10.1073/pnas.75.10.4810
McGarvey DJ, Croteau R (1995) Terpenoid metabolism. Am Soc Plant Biol 7:1015–1026
McLennan AG (2006) The Nudix hydrolase superfamily. Cell Mol Life Sci 63:123–143. https://doi.org/10.1007/s00018-005-5386-7
Mithöfer A, Wanner G, Boland W (2005) Effects of feeding Spodoptera littoralis on Lima Bean Leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol 137:1160–1168. https://doi.org/10.1104/pp.104.054460
Ruiz C, Aguirre L, Corvalan J et al (1961) Distribution of the elements in some major units of the Earth’s Crust. Geological Society of America Bulletin Distribution 175–192
Samaranayake P, Peiris BD, Dssanayake S (2012) Effect of excessive ferrous (Fe 2+) on growth and iron content in rice (Oryza sativa). Int J Agric Biol 14:296–298
Sanglard L, Barbosa M, Namorato F et al (2019) Silicon nutrition mitigates the negative impacts of iron toxicity on rice photosynthesis and grain yield. Ecotoxicol Environ Saf 189:110008. https://doi.org/10.1016/j.ecoenv.2019.110008
Sun W-J, Zhan J-Y, Zheng T-R et al (2018) The jasmonate-responsive transcription factor CbWRKY24 regulates terpenoid biosynthetic genes to promote saponin biosynthesis in Conyza blinii H. Lév. J Genet 97:1379–1388. https://doi.org/10.1007/s12041-018-1026-5
Takabayashi J, Dicke M, Posthumus MA (1994) Volatile herbivore-induced terpenoids in plant-mite interactions: variation caused by biotic and abiotic factors. J Chem Ecol 20:1329–1354. https://doi.org/10.1007/BF02059811
Tholl D (2015) Biosynthesis and biological functions of terpenoids in plants. In: Advances in biochemical engineering/biotechnology, pp 63–106
Thomine S, Lanquar V (2011) Iron transport and signaling in plants BT—transporters and pumps in plant signaling, Geisler M, Venema K (eds). Springer, Berlin, pp 99–131
Tu Y (2016) ChemInform abstract: artemisinin—a gift from traditional chinese medicine to the world (nobel lecture). ChemInform 47:10210–10226. https://doi.org/10.1002/chin.201641275
Tuo X-G, Xu Z-Q, Teng Y, Mu K-L (2007) The geochemical characteristics of heavy metals in soils in the Panzhihua V-Ti magnetite mine and the pollution evaluation. Bull Mineral Petrol Geochem 26:127–131
Zheng T, Wang M, Zhan J et al (2020) Ferrous iron-induced increases in capitate glandular trichome density and upregulation of CbHO-1 contributes to increases in blinin content in Conyza blinii. Planta 252:1–16. https://doi.org/10.1007/s00425-020-03492-1
Acknowledgements
We would like to thank all the colleagues in our laboratory for providing useful discussions and technical assistance. We are very grateful to the editor and reviewers for critically evaluating the manuscript and providing constructive comments for its improvement.
Funding
This research was supported by the Study of DNA Damage by Body Fluid Chloride and its Mechanism supported by the Sichuan Science and Technology Program (2020YFH0136). Funds were used for the design of the study and collection, analysis, and interpretation of data and in writing the manuscript, as well as in the open access payment.
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J-YZ and T-RZ designed research; J-YZ, T-RZ, W-JS and M-JW performed research; J-YZ and T-RZ analyzed data; J-YZ and T-RZ wrote the paper. All authors read and approved the final manuscript.
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Zheng, T., Zhan, J., Wang, M. et al. Fe induces a dynamic and biased allocation of material flux within terpenoid metabolism controlled by CbNudix in Conyza blinii. Plant Soil 467, 421–436 (2021). https://doi.org/10.1007/s11104-021-05110-9
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DOI: https://doi.org/10.1007/s11104-021-05110-9