Abstract
Conyza blinii (C. blinii) is a traditional Chinese medicinal plant mainly grown in Sichuan, China. C. blinii is suitable for studying the mechanism of plant tolerance to UV-B due to its living conditions, characterized by a high altitude and exposure to strong ultraviolet radiation. Our results showed that the growth and photosynthetic activity of C. blinii were improved under a specific intensity of UV-B, rather than being significantly inhibited. Although UV-B increased the content of reactive oxygen species (ROS) in C. blinii, the activities of antioxidative enzymes were elevated, including superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), and ascorbate peroxidase (APX), which contributed to the elimination of ROS. Additionally, the content of blinin, the characteristic diterpene in C. blinii, was markedly increased by UV-B. Furthermore, RNA sequencing analyses were used to explore the molecular mechanism of UV-B tolerance in C. blinii. According to the results, most of the key enzyme genes in the blinin synthesis pathway were upregulated by UV-B. In addition, 23 upregulated terpene transporter genes were identified, and these genes might participate in blinin transport during the response to UV-B. Taken together, these results implied that enhanced antioxidant capacity and upregulated transporter genes contributed to increased synthesis of blinin in response to UV-B in C. blinii.
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References
Agarwal SJBP (2007) Increased antioxidant activity in Cassia seedlings under UV-B radiation. Biol Plant 51:157–160
Bravo S, García-Alonso J, Martín-Pozuelo G, Gómez V, Santaella M, Navarro-González I, Periago MJ (2012) The influence of post-harvest UV-C hormesis on lycopene, β-carotene, and phenolic content and antioxidant activity of breaker tomatoes. Food Res Int 49:296–302
Campbell D, Eriksson MJ, Oquist G, Gustafsson P, Clarke AK, J Proceedings of the National Academy of Sciences of the United States of America (1998) The cyanobacterium Synechococcus resists UV-B by exchanging photosystem II reaction-center D1 proteins. PNAS 95:364–369
Crouzet J, Roland J, Peeters E, Trombik T, Ducos E, Nader J, Boutry M (2013) NtPDR1, a plasma membrane ABC transporter from Nicotiana tabacum, is involved in diterpene transport. Plant Mol Biol 82:181–192
Dean M, Rzhetsky A, Allikmets R (2001) The human ATP-binding cassette (ABC) transporter superfamily. Genome Res 11:1156
Deus-Neumann B, Zenk MH (1986) Accumulation of alkaloids in plant vacuoles does not involve an ion-trap mechanism. Planta 167:44–53
El Morchid EM, Torres Londoño P, Papagiannopoulos M, Gobbo-Neto L, Müller C (2014) Variation in flavonoid pattern in leaves and flowers of Primula veris of different origin and impact of UV-B. Biochem Syst Ecol 53:81–88
Fischbach RJ, Kossmann B, Panten H, Steinbrecher R, Schnitzler JP (2002) Seasonal accumulation of ultraviolet〣 screening pigments in needles of Norway spruce (Picea abies (L.) Karst.). Plant Cell Environ 22:27–37
Goodman CD, Walbot V, Walbot V, Casati P (2004) A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. Plant Cell 16:1812–1826
Grec S, Vanham D, de Ribaucourt JC, Purnelle B, Boutry M (2003) Identification of regulatory sequence elements within the transcription promoter region of NpABC1, a gene encoding a plant ABC transporter induced by diterpenes. Plant J 35:237–250
Ibrahim M, Omar H, Zain N (2017) Salicylic acid enhanced photosynthesis, secondary metabolites, antioxidant and lipoxygenase inhibitory activity (LOX) in Centella asiatica. Ann Res Rev Biol 17:1–14
Jasiński M, Stukkens Y, Degand H, Purnelle B, Marchand-Brynaert J, Boutry M (2001) A plant plasma membrane ATP binding cassette-type transporter is involved in antifungal terpenoid secretion. Plant Cell 13:1095–1107
Jenkins GI, Brown BA (2009) Signal transduction in responses to UV-B radiation. Annu Rev Plant Biol 60:407
Jha NK, Kar R, Niranjan R (2019) ABC Transporters in neurological disorders: an important gateway for botanical compounds mediated neuro-therapeutics. Curr Top Med Chem 19:795–811
Jin H et al (2007) Molecular cloning and characterization of Crmdr1, a novel MDR-type ABC transporter gene from Catharanthus roseus. Dna Seq J Dna Seq Map 18:316–325
Kim DY, Jin JY, Alejandro S, Martinoia E, Lee Y (2010) Overexpression of AtABCG36 improves drought and salt stress resistance in Arabidopsis. Physiol Plant 139:170–180
Kim HY, Lee JM, Yokozawa T, Sakata K, Lee S (2011) Protective activity of flavonoid and flavonoid glycosides against glucose-mediated protein damage. Food Chem 126:892–895
Kolaczkowski M, VDR M, Cybularz-Kolaczkowska A, Soumillion J-P, Konings WN, Andre G (1996) Anticancer drugs, ionophoric peptides, and steroids as substrates of the yeast multidrug transporter Pdr5p. J Biol Chem 271:31543–31548
Kotilainen T, Tegelberg R, Julkunen Tilltto R, Lindfors A, PJJGCB A (2010) Metabolite specific effects of solar UV-A and UV-B on alder and birch leaf phenolics. Glob Chang Biol 14:1294–1304
Kramer GF, Norman HA, Krizek DT, Mirecki RMJP (1991) influence of UV-B radiation on polyamines, lipid peroxidation and membrane lipids in cucumber. Phytochemistry 30:2101–2108
Liu H, Cao X, Liu X, Xin R, Chen K (2017a) UV- B irradiation differentially regulates terpene synthases and terpene content of peach: UV-B regulates peach volatile production. Plant Cell Environ 40(10):2261–2275
Liu H et al (2017b) A triterpenoidal saponin fraction of Conyza blinii H.Lév. is a dual-targeting autophagy inhibitor for HeLa cells. RSC Adv 7:24291–24297
Ma L, Liu H, Meng L, Qin P, Zhang B, Li Y, Man S, Liu Z, Liu Z, Diao A (2017a) Evaluation of the anti-cancer activity of the triterpenoidal saponin fraction isolated from the traditional Chinese medicine Conyza blinii H. Lév RSC Advances 7:3408–3412
Ma L et al (2017b) 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
Markham KR, Ryan KG, Bloor SJ, Mitchell KA (1998) An increase in the luteolin: apigenin ratio in Marchantia polymorpha on UV-B enhancement. Phytochemistry 48:791–794
Marrs KA, Alfenito MR, Lloyd AM, Walbot V (1995) A glutathione-S-transferase involved in vacuolar transfer encoded by the maize gene bronze-2. Nature 375:397–400
Mccaskill DG, Martin DL, Scott AI (1988) Characterization of alkaloid uptake by Catharanthus roseus (L.) G. Don Protoplasts Plant Physiol 87:402–408
Novak AB, Short FT (2011) UV-B induces leaf reddening and supports photosynthesis in the seagrass Thalassia testudinum. J Exp Mar Biol Ecol 409:136–142
Prado FE, Rosa M, Prado C, Podazza G, Interdonato R, González JA, Hilal M (2012) UV-B radiation, its effects and defense mechanisms in terrestrial plants. In: Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change. pp 57-83
Qiao X et al (2010) Rapid characterization of triterpene saponins from <em>Conyza blinii</em> by liquid chromatography coupled with mass spectrometry. Rapid Commun Mass Spectrom 24:3340–3350
Quan J, Song S, Abdulrashid K, Chai Y, Yue M, Liu X (2018) Separate and combined response to UV-B radiation and jasmonic acid on photosynthesis and growth characteristics of Scutellaria baicalensis. Int J Mol Sci 19(4):1194
Righini S, Rodriguez EJ, Berosich C, Grotewold E, Casati P, Falcone Ferreyra ML (2019) Apigenin produced by maize flavone synthase I and II protects plants against UV-B-induced damage. Plant Cell Environ 42:495–508
Von Roepenack-Lahaye E (2004) Profiling of Arabidopsis secondary metabolites by capillary liquid chromatography coupled to electrospray ionization quadrupole time-of-flight mass spectrometry. Plant Physiol 134:548–559
Rozema J, Van De Staaij J, Björn LO, Caldwell M, J Trends in Ecology, Evolution (1997) UV-B as an environmental factor in plant life: stress and regulation. Trends Ecol Evol 12:22–28
Sasabe M, Toyoda K, Shiraishi T, Inagaki Y, Ichinose Y (2002) cDNA cloning and characterization of tobacco ABC transporter: NtPDR1 is a novel elicitor-responsive gene. FEBS Lett 518:164–168
Shan L, Rong S, Tang Z, Gao J, Hu H, Hui C (2013) Genetic diversity of wild populations of Conyza blinii Lévl. and extraction of total flavonoids. Biotechnol Bull
Shi SB, Zhu W-Y, Li H-M, Zhou D-W, Han F, Zhao X-Q, Tang Y-H (2004) Photosynthesis of Saussurea superba and Gentiana straminea is not reduced after long-term enhancement of UV-B radiation. Environ Exp Bot 51:75–83
Stavisky J, Funderburk J, Brodbeck BV, Olson SM, Andersen PC (2002) Population dynamics of Frankliniella spp. and tomato spotted wilt incidence as influenced by cultural management tactics in tomato 95:1216-1221
Stukkens Y, Bultreys A, Grec S, Trombik T, Vanham D, Boutry M (2005) NpPDR1, a pleiotropic drug resistance-type ATP-binding cassette transporter from Nicotiana plumbaginifolia, plays a major role in plant pathogen defense. Plant Physiol 139:341–352
Su N, Lu Y, Wu Q, Liu Y, Xia Y, Xia K, Cui J (2016) UV-B-induced anthocyanin accumulation in hypocotyls of radish sprouts continues in the dark after irradiation. J Sci Food Agric 96:886–892
Suzuki N, Koussevitzky S, Mittler R, Miller G (2011) ROS and redox signaling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270
Takeuchi Y, Murakami M, Nakajima N, Kondo N, Nikaido OJP, Physiology C (1996) Induction and repair of damage to DNA in cucumber cotyledons irradiated with UV-B. Plant Cell Physiol 37:181–187
Teramura AH, Ziska LH, Ester Sztein A (2010) Changes in growth and photosynthetic capacity of rice with increased UV-B radiation. Biology 83:373–380
Van den Brule S (2002) The ABC transporter SpTUR2 confers resistance to the antifungal diterpene sclareol. Plant J 30(6):649–662
Yadav A et al (2019) The B-Box-containing microprotein miP1a/BBX31 regulates photomorphogenesis and UV-B protection. Plant Physiol 179:1876–1892
Yang C, He Z, Li X, Zheng Q, He C, Yang J, MORITA T (1989) Blinin, a neoclerodane diterpene from conyza blinii. Phyrochmistry 28:3131–3134
Zavala JA, Ravetta DA (2002) The effect of solar UV-B radiation on terpenes and biomass production inGrindelia chiloensis(Asteraceae), a woody perennial of Patagonia. Argentina Plant Ecol 161:185–191
Zhang R, Huang G, Wang L, Zhou Q, Huang X (2019) Effects of elevated ultraviolet-B radiation on root growth and chemical signaling molecules in plants. Ecotoxicol Environ Saf 171:683–690
Zhang X et al (2018) Transcriptome analysis of radish sprouts hypocotyls reveals the regulatory role of hydrogen-rich water in anthocyanin biosynthesis under UV-A. BMC Plant Biol 18:227
Zhao J, Dixon R (2010) The ‘ins’ and ‘outs’ of flavonoid transport. Trends Plant Sci 15:72–80
Acknowledgments
We 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 a study on improving the content of blinin in Conyza blinii H. Lév. by metabolic engineering (2018HH0074), a study on DNA Damage by Body Fluid Chloride and its Mechanism supported by Sichuan Science and Technology Program (2020YFH0136), and entrepreneurship training program for college students (201810626106). 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.-Y.Z and Q.Y designed the research; J.-Y.Z, Q.Y, T.-R.Z, Z.-Y.L, W.-J.S, M.-J.W, and T.W performed the research; J.-Y.Z, T.-L.B, and Z.-Z.T analyzed the data; J.-Y.Z, Q.Y, and Z.-Y.L wrote the paper. All authors read and approved the final manuscript.
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Zhan, J., Yang, Q., Lin, Z. et al. Enhanced antioxidant capacity and upregulated transporter genes contribute to the UV-B-induced increase in blinin in Conyza blinii. Environ Sci Pollut Res 28, 13275–13287 (2021). https://doi.org/10.1007/s11356-020-11502-8
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DOI: https://doi.org/10.1007/s11356-020-11502-8