Research Progress and Prospects of Cyanobacterial Secondary Metabolite Scytonemin

doi:10.13523/j.cb.2304053

China Biotechnology

2023, Vol. 43

Issue (10): 85-95 DOI: 10.13523/j.cb.2304053

Research Progress and Prospects of Cyanobacterial Secondary Metabolite Scytonemin

ZHANG Ai-di^1,²,CUI Jin-yu^2,^3,^4,^**(

),ZHANG Ya-ning^2,^3,⁴,MAO Shao-ming^1,^**(

),LUAN Guo-dong^2,^3,⁴,LV Xue-feng^2,^3,⁴

1 Hunan Provincial Key Laboratory of Forestry Biotechnology, College of Life Science and Technology, Central South University of Forestry and Technology, Changsha 410004, China
2 Key Laboratory of Biofuels, Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao 266101, China
3 Shandong Energy Institute, Qingdao 266101, China
4 Qingdao New Energy Shandong Laboratory, Qingdao 266101, China

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Abstract

Cyanobacteria are an important group of photoautotrophic and prokaryotic microorganisms, which can directly convert carbon dioxide and solar energy into high value-added chemicals. Due to low nutritional requirements, rapid growth and well-established genetic manipulation tools, cyanobacteria are considered to be a model system. Scytonemin is a lipid-soluble indole alkaloid pigment, which is found in some cyanobacteria under UV-A radiation. It can strongly absorb UV-A radiation and has great pharmacological potential with interesting anti-inflammatory and anti-proliferative activities. Thus it has great prospects in cosmetic and biomedical applications. So far, the mechanism and regulation of scytonemin synthesis have been illustrated in Nostoc punctiforme PCC 73102. However, several bottlenecks in genetic engineering have hindered the efficient and sustainable synthesis of scytonemin. By the development of synthetic biology in vivo and ex vivo engineering, the efficient synthesis of scytonemin is expected to be realized. Here, we summarize the scytonemin on its structure, chemical properties, biosynthetic pathways, regulatory mechanisms, stress physiology and applications. Moreover, the future prospects and directions of scytonemin are also discussed.

Key words： Cyanobacteria Scytonemin Synthetic regulatory mechanism Environmental stress

Received: 26 April 2023 Published: 02 November 2023

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	ZHANG Ai-di
	CUI Jin-yu
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	LV Xue-feng

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ZHANG Ai-di, CUI Jin-yu, ZHANG Ya-ning, MAO Shao-ming, LUAN Guo-dong, LV Xue-feng. Research Progress and Prospects of Cyanobacterial Secondary Metabolite Scytonemin. China Biotechnology, 2023, 43(10): 85-95.

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https://manu60.magtech.com.cn/biotech/10.13523/j.cb.2304053 OR https://manu60.magtech.com.cn/biotech/Y2023/V43/I10/85

Fig.1 Structural formula, UV protection and anti-proliferation function of scytonemin (a) Schematic diagram of UV protection function of scytonemin (b) Schematic diagram of the inhibition of Polo-like kinase 1 by scytonemin (c) Structural formula of scytonemin

Fig.2 The gene cluster and synthesis pathway of scytonemin in PCC 73102 (a) The gene cluster of scytonemin synthesis in PCC 73102 (b) The synthesis pathway of scytonemin in PCC 73102

环境因素	菌株	对伪枝藻素合成的影响	参考文献
光照	Chlorogloeopsis sp.	白光[50 μmol/(m²·s)],0.05 μg/mg;白光[200 μmol/(m²·s)],11.51 μg/mg	[66]
	A. fertilissima NCCU-443	紫外辐射,产量提高约187.5% 黄光,产量提高288.9%	[67]
	Scytonema hoffmani	UV-B,产量提高18.7%	[70]
	Scytonema sp. R77DM	可见光,产量提高约20%;可见光、UV-A,产量提高160%;可见光、UV-A和UV-B,产量提高240%	[12]
盐胁迫	A. fertilissima NCCU-443	0.45 mol/L,产量提高70%	[67]
	L. aestuarii	0.43 mol/L,产量最高,在低于0.1 mol/L、高于3.4 mol/L时伪枝藻素会降解	[15]
	Chroococcidiopsis M88 VD-G	盐浓度的增加抑制伪枝藻素的合成	[25]
氧化胁迫	Chroococcidiopsis M88 VD-G	0.5 μmol/L的亚甲基蓝,产量约25 μg/mg	[25]
温度胁迫	A. fertilissima NCCU-443	35℃,产量提高50%	[67]
	Scytonema sp. R77DM	35℃、可见光、UV-A和UV-B,产量提高128.6%	[12]
	Chroococcidiopsis M88 VD-G	34~35℃,产量约11.83 μg/mg	[25]
氮源	PCC 73102	0.4 mmol/L N $O 3 -$ ,产量提高36.4% 0.1 mmol/L N $H 4 +$ ,产量提高26.7% 1 mmol/L NH₄NO₃,产量降低85.7%	[68]
干旱胁迫	PCC 73102	干旱5 d,产量32.5 μg/mg,比水化提高了30%	[33]
	Chroococcidiopsis CCMEE 5056	干旱5 d,产量70 μg/mg,比水化提高了100%	[33]
	Chroococcidiopsis CCMEE 246	干旱5 d,产量35 μg/mg,是连续水化的65%	[33]

Table 1 Effects of various stress factors on scytonemin synthesis


[1]	Stanier R Y, Cohen-Bazire G. Phototrophic prokaryotes: the cyanobacteria. Annual Review of Microbiology, 1977, 31(1): 225-274. doi: 10.1146/micro.1977.31.issue-1

[2]	Zehr J P. Nitrogen fixation by marine cyanobacteria. Trends in Microbiology, 2011, 19(4): 162-173. doi: 10.1016/j.tim.2010.12.004 pmid: 21227699

[3]	Garlapati D, Chandrasekaran M, Devanesan A, et al. Role of cyanobacteria in agricultural and industrial sectors: an outlook on economically important byproducts. Applied Microbiology and Biotechnology, 2019, 103(12): 4709-4721. doi: 10.1007/s00253-019-09811-1 pmid: 31030286

[4]	Perera I A, Abinandan S, Subashchandrabose S R, et al. Advances in the technologies for studying consortia of bacteria and cyanobacteria/microalgae in wastewaters. Critical Reviews in Biotechnology, 2019, 39(5): 709-731. doi: 10.1080/07388551.2019.1597828 pmid: 30971144

[5]	Gonçalves A L, Pires J C M, Simões M. Biotechnological potential of Synechocystis salina co-cultures with selected microalgae and cyanobacteria: nutrients removal, biomass and lipid production. Bioresource Technology, 2016, 200: 279-286. doi: 10.1016/j.biortech.2015.10.023 pmid: 26496217

[6]	De Philippis R, Colica G, Micheletti E. Exopolysaccharide-producing cyanobacteria in heavy metal removal from water: molecular basis and practical applicability of the biosorption process. Applied Microbiology and Biotechnology, 2011, 92(4): 697-708. doi: 10.1007/s00253-011-3601-z pmid: 21983706

[7]	Wu L, Zhu Q H, Yang L, et al. Nutrient transferring from wastewater to desert through artificial cultivation of desert cyanobacteria. Bioresource Technology, 2018, 247: 947-953. doi: S0960-8524(17)31692-9 pmid: 30060434

[8]	Jensen P E, Leister D. Cyanobacteria as an experimental platform for modifying bacterial and plant photosynthesis. Frontiers in Bioengineering and Biotechnology, 2014, 2: 7. pmid: 25024050

[9]	Jaiswal D, Sahasrabuddhe D, Wangikar P P. Cyanobacteria as cell factories: the roles of host and pathway engineering and translational research. Current Opinion in Biotechnology, 2022, 73: 314-322. doi: 10.1016/j.copbio.2021.09.010

[10]	Khatoon H, Kok Leong L, Abdu Rahman N, et al. Effects of different light source and media on growth and production of phycobiliprotein from freshwater cyanobacteria. Bioresource Technology, 2018, 249: 652-658. doi: S0960-8524(17)31881-3 pmid: 29091850

[11]	Xiong W, Cano M, Wang B, et al. The plasticity of cyanobacterial carbon metabolism. Current Opinion in Chemical Biology, 2017, 41: 12-19. doi: S1367-5931(17)30058-3 pmid: 28968542

[12]	Rastogi R P, Sonani R R, Madamwar D. The high-energy radiation protectant extracellular sheath pigment scytonemin and its reduced counterpart in the cyanobacterium Scytonema sp. R77DM. Bioresource Technology, 2014, 171: 396-400. doi: 10.1016/j.biortech.2014.08.106 pmid: 25226055

[13]	Rastogi R P, Madamvar D, Incharoensakdi A. Multiple defense systems in cyanobacteria in response to solar UV radiation. Cyanobacteria:Ecological Importance, Biotechnological Uses and Risk Management. New York: Nova Science Publishers, 2015: 125-158.

[14]	Rastogi R P, Sinha R P. Biotechnological and industrial significance of cyanobacterial secondary metabolites. Biotechnology Advances, 2009, 27(4): 521-539. doi: 10.1016/j.biotechadv.2009.04.009 pmid: 19393308

[15]	Rath J, Mandal S, Adhikary S P. Salinity induced synthesis of UV-screening compound scytonemin in the cyanobacterium Lyngbya aestuarii. Journal of Photochemistry and Photobiology B: Biology, 2012, 115: 5-8. doi: 10.1016/j.jphotobiol.2012.06.002

[16]	Gao X, Jing X, Liu X F, et al. Biotechnological production of the sunscreen pigment scytonemin in cyanobacteria: progress and strategy. Marine Drugs, 2021, 19(3): 129. doi: 10.3390/md19030129

[17]	Gröniger A, Sinha R P, Klisch M, et al. Photoprotective compounds in cyanobacteria, phytoplankton and macroalgae: a database. Journal of Photochemistry and Photobiology B: Biology, 2000, 58(2-3): 115-122. doi: 10.1016/S1011-1344(00)00112-3

[18]	Büdel B, Becker U, Follmann G, et al. Algae, fungi, and lichens on inselbergs. Inselbergs:Biotic Diversity of Isolated Rock Outcrops in Tropical and Temperate Regions. Berlin: Springer Berlin Heidelberg, 2000: 69-90.

[19]	Proteau P J, Gerwick W H, Garcia-Pichel F, et al. The structure of scytonemin, an ultraviolet sunscreen pigment from the sheaths of cyanobacteria. Experientia, 1993, 49(9): 825-829. pmid: 8405307

[20]	Rastogi R P, Kumari S, Richa, et al. Molecular characterization of hot spring cyanobacteria and evaluation of their photoprotective compounds. Canadian Journal of Microbiology, 2012, 58(6): 719-727. doi: 10.1139/w2012-044 pmid: 22582897

[21]	Matsui K, Nazifi E, Hirai Y, et al. The cyanobacterial UV-absorbing pigment scytonemin displays radical-scavenging activity. The Journal of General and Applied Microbiology, 2012, 58(2): 137-144. doi: 10.2323/jgam.58.137

[22]	Stevenson C S, Capper E A, Roshak A K, et al. Scytonemin: a marine natural product inhibitor of kinases key in hyperproliferative inflammatory diseases. Inflammation Research, 2002, 51(2): 112-114. doi: 10.1007/BF02684014 pmid: 11926312

[23]	Pathak J, Mondal S, Ahmed H, et al. In silico study on interaction between human polo-like kinase 1 and cyanobacterial sheath pigment scytonemin by molecular docking approach. Biointerface Research in Applied Chemistry, 2019, 9(5): 4374-4378. doi: 10.33263/BRIAC

[24]	Soule T Y, Garcia-Pichel F, Stout V. Gene expression patterns associated with the biosynthesis of the sunscreen scytonemin in Nostoc punctiforme ATCC 29133 in response to UVA radiation. Journal of Bacteriology, 2009, 191(14): 4639-4646. doi: 10.1128/JB.00134-09

[25]	Dillon J G, Tatsumi C M, Tandingan P G, et al. Effect of environmental factors on the synthesis of scytonemin, a UV-screening pigment, in a cyanobacterium (Chroococcidiopsis sp.). Archives of Microbiology, 2002, 177(4): 322-331. pmid: 11889486

[26]	Němečková K, Culka A, Němec I, et al. Raman spectroscopic search for scytonemin and gloeocapsin in endolithic colonizations in large gypsum crystals. Journal of Raman Spectroscopy, 2021, 52(12): 2633-2647. doi: 10.1002/jrs.v52.12

[27]	Bultel-Poncé V, Felix-Theodose F, Sarthou C, et al. New pigments from the terrestrial cyanobacterium Scytonema sp. collected on the mitaraka inselberg, French Guyana. Journal of Natural Products, 2004, 67(4): 678-681. pmid: 15104503

[28]	Grant C S, Louda J W. Scytonemin-imine, a mahogany-colored UV/Vis sunscreen of cyanobacteria exposed to intense solar radiation. Organic Geochemistry, 2013, 65: 29-36. doi: 10.1016/j.orggeochem.2013.09.014

[29]	Cui L J, Xu H Y, Zhu Z X, et al. The effects of the exopolysaccharide and growth rate on the morphogenesis of the terrestrial filamentous cyanobacterium Nostoc flagelliforme. Biology Open, 2017, 6(9): 1329-1335. doi: 10.1242/bio.026955

[30]	Shailendra P S, Sunita K, Rajesh P R, et al. Photoprotective and biotechnological potentials of cyanobacterial sheath pigment, scytonemin. African Journal of Biotechnology, 2010, 9(5): 581-588. doi: 10.5897/AJB

[31]	Ferroni L, Klisch M, Pancaldi S, et al. Complementary UV-absorption of mycosporine-like amino acids and scytonemin is responsible for the UV-insensitivity of photosynthesis in Nostoc flagelliforme. Marine Drugs, 2010, 8(1): 106-121. doi: 10.3390/md8010106

[32]	Rastogi R P, Incharoensakdi A. Characterization of UV-screening compounds, mycosporine-like amino acids, and scytonemin in the cyanobacterium Lyngbya sp. CU2555. FEMS Microbiology Ecology, 2014, 87(1): 244-256. doi: 10.1111/1574-6941.12220 pmid: 24111939

[33]	Fleming E D, Castenholz R W. Effects of periodic desiccation on the synthesis of the UV-screening compound, scytonemin, in cyanobacteria. Environmental Microbiology, 2007, 9(6): 1448-1455. pmid: 17504482

[34]	Squier A H, Hodgson D A, Keely B J. A critical assessment of the analysis and distributions of scytonemin and related UV screening pigments in sediments. Organic Geochemistry, 2004, 35(11-12): 1221-1228. doi: 10.1016/j.orggeochem.2004.07.005

[35]	Lali D, Meriluoto J, Zori M, et al. Potential of cyanobacterial secondary metabolites as biomarkers for paleoclimate reconstruction. CATENA, 2020, 185: 104283. doi: 10.1016/j.catena.2019.104283

[36]	Rastogi R P, Sonani R R, Madamwar D. Cyanobacterial sunscreen scytonemin: role in photoprotection and biomedical research. Applied Biochemistry and Biotechnology, 2015, 176(6): 1551-1563. doi: 10.1007/s12010-015-1676-1 pmid: 26013282

[37]	Rastogi R P, Sinha R P, Incharoensakdi A. Partial characterization, UV-induction and photoprotective function of sunscreen pigment, scytonemin from Rivularia sp. HKAR-4. Chemosphere, 2013, 93(9): 1874-1878. doi: 10.1016/j.chemosphere.2013.06.057 pmid: 23859424

[38]	Yasuhiro I, Hiroshi Y, Fumio M, et al. Polo-like kinase 1 (PLK1) expression is associated with cell proliferative activity and cdc2 expression in malignant lymphoma of the thyroid. Anticancer Research, 2004, 24(1): 259-63. pmid: 15015605

[39]	Strebhardt K, Ullrich A. Targeting polo-like kinase 1 for cancer therapy. Nature Reviews Cancer, 2006, 6(4): 321-330. doi: 10.1038/nrc1841 pmid: 16557283

[40]	Zhang G J, Zhang Z, Liu Z G. Polo-like kinase 1 is overexpressed in renal cancer and participates in the proliferation and invasion of renal cancer cells. Tumor Biology, 2013, 34(3): 1887-1894. doi: 10.1007/s13277-013-0732-0

[41]	Zhang G J, Zhang Z, Liu Z G. Scytonemin inhibits cell proliferation and arrests cell cycle through downregulating Plk1 activity in multiple myeloma cells. Tumor Biology, 2013, 34(4): 2241-2247. doi: 10.1007/s13277-013-0764-5

[42]	Itoh T, Tsuzuki R, Tanaka T, et al. Reduced scytonemin isolated from Nostoc commune induces autophagic cell death in human T-lymphoid cell line Jurkat cells. Food and Chemical Toxicology, 2013, 60: 76-82. doi: 10.1016/j.fct.2013.07.016

[43]	Kang M R, Jo S A, Lee H, et al. Inhibition of skin inflammation by scytonemin, an ultraviolet sunscreen pigment. Marine Drugs, 2020, 18(6): 300. doi: 10.3390/md18060300

[44]	Helms G L, Moore R E, Niemczura W P, et al. Scytonemin A, a novel calcium antagonist from a blue-green alga. The Journal of Organic Chemistry, 1988, 53(6): 1298-1307. doi: 10.1021/jo00241a033

[45]	He Y F, Suyama T L, Kim H, et al. Discovery of novel tyrosinase inhibitors from marine cyanobacteria. Frontiers in Microbiology, 2022, 13: 912621. doi: 10.3389/fmicb.2022.912621

[46]	Brenner M, Hearing V J. The protective role of melanin against UV damage in human skin. Photochemistry and Photobiology, 2008, 84(3): 539-549. doi: 10.1111/j.1751-1097.2007.00226.x pmid: 18435612

[47]	Pillaiyar T, Manickam M, Namasivayam V. Skin whitening agents: medicinal chemistry perspective of tyrosinase inhibitors. Journal of Enzyme Inhibition and Medicinal Chemistry, 2017, 32(1): 403-425. doi: 10.1080/14756366.2016.1256882 pmid: 28097901

[48]	Ekebergh A, Karlsson I, Mete R D, et al. Oxidative coupling as a biomimetic approach to the synthesis of scytonemin. Organic Letters, 2011, 13(16): 4458-4461. doi: 10.1021/ol201812n pmid: 21786790

[49]	Soule T Y, Palmer K, Gao Q J, et al. A comparative genomics approach to understanding the biosynthesis of the sunscreen scytonemin in cyanobacteria. BMC Genomics, 2009, 10: 336. doi: 10.1186/1471-2164-10-336 pmid: 19630972

[50]	Ferreira D, Garcia-Pichel F. Mutational studies of putative biosynthetic genes for the cyanobacterial sunscreen scytonemin in Nostoc punctiforme ATCC 29133. Frontiers in Microbiology, 2016, 7: 735. doi: 10.3389/fmicb.2016.00735 pmid: 27242750

[51]	Klicki K, Ferreira D, Hamill D, et al. The widely conserved ebo cluster is involved in precursor transport to the periplasm during scytonemin synthesis in Nostoc punctiforme. mBio, 2018, 9(6): e02266-18.

[52]	Balskus E P, Walsh C T. Investigating the initial steps in the biosynthesis of cyanobacterial sunscreen scytonemin. Journal of the American Chemical Society, 2008, 130(46): 15260-15261. doi: 10.1021/ja807192u pmid: 18954141

[53]	Balskus E P, Walsh C T. An enzymatic cyclopentyl[b]indole formation involved in scytonemin biosynthesis. Journal of the American Chemical Society, 2009, 131(41): 14648-14649. doi: 10.1021/ja906752u pmid: 19780555

[54]	Sorrels C M, Proteau P J, Gerwick W H. Organization, evolution, and expression analysis of the biosynthetic gene cluster for scytonemin, a cyanobacterial UV-absorbing pigment. Applied and Environmental Microbiology, 2009, 75(14): 4861-4869. doi: 10.1128/AEM.02508-08 pmid: 19482954

[55]	Naurin S, Bennett J, Videau P, et al. The response regulator Npun_F1278 is essential for scytonemin biosynthesis in the cyanobacterium Nostoc punctiforme ATCC 29133. Journal of Phycology, 2016, 52(4): 564-571. doi: 10.1111/jpy.2016.52.issue-4

[56]	Malla S, Sommer M O A. A sustainable route to produce the scytonemin precursor using Escherichia coli. Green Chemistry, 2014, 16(6): 3255-3265. doi: 10.1039/C4GC00118D

[57]	Zhang J J, Tang X Y, Moore B S. Genetic platforms for heterologous expression of microbial natural products. Natural Product Reports, 2019, 36(9): 1313-1332. doi: 10.1039/c9np00025a pmid: 31197291

[58]	Brey L F, Włodarczyk A J, Bang Thøfner J F, et al. Metabolic engineering of Synechocystis sp. PCC 6803 for the production of aromatic amino acids and derived phenylpropanoids. Metabolic Engineering, 2020, 57: 129-139. doi: 10.1016/j.ymben.2019.11.002

[59]	Videau P, Wells K N, Singh A J, et al. Expanding the natural products heterologous expression repertoire in the model cyanobacterium Anabaena sp. strain PCC 7120: production of pendolmycin and teleocidin B-4. ACS Synthetic Biology, 2020, 9(1): 63-75. doi: 10.1021/acssynbio.9b00334

[60]	Taton A, Ecker A, Diaz B, et al. Heterologous expression of cryptomaldamide in a cyanobacterial host. ACS Synthetic Biology, 2020, 9(12): 3364-3376. doi: 10.1021/acssynbio.0c00431 pmid: 33180461

[61]	Yang G, Cozad M A, Holland D A, et al. Photosynthetic production of sunscreen shinorine using an engineered cyanobacterium. ACS Synthetic Biology, 2018, 7(2): 664-671. doi: 10.1021/acssynbio.7b00397 pmid: 29304277

[62]	Knoot C J, Khatri Y, Hohlman R M, et al. Engineered production of hapalindole alkaloids in the cyanobacterium Synechococcus sp. UTEX 2973. ACS Synthetic Biology, 2019, 8(8): 1941-1951. doi: 10.1021/acssynbio.9b00229 pmid: 31284716

[63]	Shang J L, Chen M, Hou S W, et al. Genomic and transcriptomic insights into the survival of the subaerial cyanobacterium Nostoc flagelliforme in arid and exposed habitats. Environmental Microbiology, 2019, 21(2): 845-863. doi: 10.1111/emi.2019.21.issue-2

[64]	Liang F Y, Lindblad P. Effects of overexpressing photosynthetic carbon flux control enzymes in the cyanobacterium Synechocystis PCC 6803. Metabolic Engineering, 2016, 38: 56-64. doi: 10.1016/j.ymben.2016.06.005

[65]	De Porcellinis A J, Nørgaard H, Brey L M F, et al. Overexpression of bifunctional fructose-1, 6-bisphosphatase/sedoheptulose-1, 7-bisphosphatase leads to enhanced photosynthesis and global reprogramming of carbon metabolism in Synechococcus sp. PCC 7002. Metabolic Engineering, 2018, 47: 170-183. doi: S1096-7176(17)30384-1 pmid: 29510212

[66]	Garcia-Pichel F, Sherry N D, Castenholz R W. Evidence for an ultraviolet sunscreen role of the extracellular pigment scytonemin in the terrestrial cyanobacterium Chiorogloeopsis sp. Photochemistry and Photobiology, 1992, 56(1): 17-23. pmid: 1508978

[67]	Mushir S, Fatma T. Monitoring stress responses in cyanobacterial scytonemin-screening and characterization. Environmental Technology, 2012, 33(2): 153-157. doi: 10.1080/09593330.2011.553842

[68]	Fleming E D, Castenholz R W. Effects of nitrogen source on the synthesis of the UV-screening compound, scytonemin, in the cyanobacterium Nostoc punctiforme PCC 73102. FEMS Microbiology Ecology, 2008, 63(3): 301-308. doi: 10.1111/j.1574-6941.2007.00432.x pmid: 18218026

[69]	Meixner K, Daffert C, Dalnodar D, et al. Glycogen, poly(3-hydroxybutyrate) and pigment accumulation in three Synechocystis strains when exposed to a stepwise increasing salt stress. Journal of Applied Phycology, 2022, 34(3): 1227-1241. doi: 10.1007/s10811-022-02693-3 pmid: 35673609

[70]	Azarafshan M, Peyvandi M, Abbaspour H, et al. The effects of UV-B radiation on genetic and biochemical changes of Pelargonium graveolens L’Her. Physiology and Molecular Biology of Plants, 2020, 26(3): 605-616. doi: 10.1007/s12298-020-00758-6 pmid: 32205934

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