Abstract
The current decade has witnessed notable advancement towards the utilization of non-thermal (cold) plasma in multidisciplinary fields such as plant sciences. This study intends to validate whether cold plasma contributes to improving callogenesis performance and eliciting the production of cannabinoids in cannabis. The cannabis-derived calli were treated with plasma at different exposure times, including 0, 60, 120, and 180 s. The plasma priming improved the callogenesis performance and callus biomass by an average of 46.6%. The molecular assessment (MSAP method) validated how the plasma priming is epigenetically associated with variation in DNA methylome in the cannabis calli. The cold plasma treatments transcriptionally upregulated the expression of WRKY1 and ERF1B transcription factors by averages of 3.5- and 3.8-fold. The plasma treatment also stimulated the transcription of OLS, OAC, CBGAS, CBDAS, and THCAS genes involved in the biosynthesis of cannabinoids. The HPLC assessment proved the high potency of cold plasma to enhance the synthesis of cannabinoids, including Cannabigerol (CBG), Cannabidiol (CBD), and cannabinol (CBN). The plasma-primed calli contained higher concentrations of proteins (56%), proline (38%), and soluble phenols (40%). The activities of peroxidase and catalase enzymes showed a similar upward trend in response to the plasma. The profound increase in the concentrations of soluble sugars resulted from the plasma treatments. The plasma priming of calli contributed to the significant upregulation in the activity of the phenylalanine ammonia-lyase enzyme. This biological assessment study validates the high potency of plasma priming to elicit the biosynthesis of cannabinoids in cannabis calli.
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Abedi S, Iranbakhsh A, Oraghi Ardebili Z, Ebadi M (2021) Nitric oxide and selenium nanoparticles confer changes in growth, metabolism, antioxidant machinery, gene expression, and flowering in chicory (Cichorium intybus L.): potential benefits and risk assessment. Environ Sci Pollut Res 28:3136–3148. https://doi.org/10.1007/s11356-020-10706-2
Adhikari B, Adhikari M, Ghimire B, Adhikari BC, Park G, Choi EH (2020) Cold plasma seed priming modulates growth, redox homeostasis and stress response by inducing reactive species in tomato (Solanum lycopersicum). Free Radical Biol Med 156:57–69. https://doi.org/10.1016/j.freeradbiomed.2020.06.003
Adhikary D, Kulkarni M, El-Mezawy A, Mobini S, Elhiti M, Rale G, Ray A, Patricia P, Slaski JJ, Maxwell P. Jones M, Pankaj Bhowmik P (2021) Medical cannabis and industrial hemp tissue culture: present status and future potential, frontiers in plant science, Review,Volume 12, 1–22. https://doi.org/10.3389/fpls.2021.627240
Asgari-Targhi G, Iranbakhsh A, Ardebili ZO, Tooski AH (2021) Synthesis and characterization of chitosan encapsulated zinc oxide (ZnO) nanocomposite and its biological assessment in pepper (Capsicum annuum) as an elicitor for in vitro tissue culture applications. Int J Biol Macromol 189:170–182. https://doi.org/10.1016/j.ijbiomac.2021.08.117
Bassolino L, Buti M, Fulvio F, Pennesi A, Mandolino G, Milc J, Francia E, Paris R (2020) In silico identification of MYB and bHLH families reveals candidate transcription factors for secondary metabolic pathways in Cannabis sativa L. Plants 9:1–19. https://doi.org/10.3390/plants9111540
Dey S, Corina Vlot A (2015) Ethylene responsive factors in the orchestration of stress responses in monocotyledonous plants. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00640
Ebrahimibasabi E, Ebrahimi A, Momeni M, reza Amerian M (2020) Elevated expression of diosgenin-related genes and stimulation of the defense system in Trigonella foenum-graecum (Fenugreek) by cold plasma treatment. Sci Hortic, 271.https://doi.org/10.1016/j.scienta.2020.109494
Gabotti D, Locatelli F, Cusano E, Baldoni E, Genga A, Laura Pucci L, Consonni R, Mattana M (2019) Cell suspensions of Cannabis sativa (var. Futura): effect of elicitation on metabolite content and antioxidant activity. Molecules 24(22). https://doi.org/10.3390/molecules24224056
Ghasempour M, Iranbakhsh A, Ebadi M, OraghiArdebili Z (2020) Seed priming with cold plasma improved seedling performance, secondary metabolism, and expression of deacetylvindoline O-acetyltransferase gene in Catharanthusroseus. Contrib Plasma Phys. https://doi.org/10.1002/ctpp.201900159
Han B, Yu NN, Zheng W, Zhang LN, Liu Y, Yu JB, Zhang YQ, Park G, Sun HN, Kwon T (2021) Effect of non-thermal plasma (NTP) on common sunflower (Helianthus annus L.) seed growth via upregulation of antioxidant activity and energy metabolism-related gene expression. Plant Growth Regul 95(2):271–281
Iranbakhsh A, Ardebili ZO, Molaei H, Ardebili NO, Amini M (2020) Cold plasma up-regulated expressions of WRKY1 transcription factor and genes involved in biosynthesis of cannabinoids in hemp (Cannabis sativa L.). Plasma Chem Plasma Process. https://doi.org/10.1007/s11090-020-10058-2
Iranbakhsh A, Ardebili ZO, Ardebili NO (2021) Gene regulation by H2S in plants. In: Singh S, Singh V, Tripathi D, Prasad S, Chauhan D, Dubey NK (eds) Hydrogen sulfide in plant biology, 1st edn. Academic Press, Elsevier, pp. 171–199. https://doi.org/10.1016/B978-0-323-85862-5.00014-2
Iranbakhsh A, Ardebili ZO, Ardebili NO (2022) Gene regulation by NO in plants. In: Singh VP, Singh S, Tripathi D, Romero-Puertas M, Sandalio L (eds) Nitric Oxide in Plant Biology, 1st edn. Academic Press, Elsevier, Chapter 27. https://doi.org/10.1016/B978-0-12-818797-5.00006-6
Judickaitė A, Lyushkevich V, Filatova I, Mildažienė V, Žūkienė R (2022) The potential of cold plasma and electromagnetic field as stimulators of natural sweeteners biosynthesis in Stevia rebaudiana Bertoni. Plants, 11(5).
Kyzek S, Holubová Ľ, Medvecká V, Tomeková J, Gálová E, Zahoranová A (2019) Cold atmospheric pressure plasma can induce adaptive response in pea seeds. Plasma Chem Plasma Process 39(2):475–486. https://doi.org/10.3390/ijms22062833
Li K, Zhong C, Shi Q, Bi H, Gong B (2021) Cold plasma seed treatment improves chilling resistance of tomato plants through hydrogen peroxide and abscisic acid signaling pathway. Free Radical Biol Med 172:286–297. https://doi.org/10.1016/j.freeradbiomed.2021.06.011
Liu Y, Zhu P, Cai S, Haughn G, Page JE (2021) Three novel transcription factors involved in cannabinoid biosynthesis in Cannabis sativa L. Plant Mol Biol 106:49–65. https://doi.org/10.1007/s11103-021-01129-9
Mildažienė V, Aleknavičiūtė V, Žūkienė R, Paužaitė G, Naučienė Z, Filatova I, Lyushkevich V, Haimi P, Tamošiūnė I, Baniulis D (2019) Treatment of common sunflower (Helianthus annus L.) seeds with radio-frequency electromagnetic field and cold plasma induces changes in seed phytohormone balance, seedling development and leaf protein expression. Sci rep 9(1):1–12. https://doi.org/10.1038/s41598-019-42893-5
Mirakhorli T, Ardebili ZO, Ladan-Moghadam A, Danaee E (2021) Nitric oxide improved growth and yield in soybean (Glycine max) by mediating physiological, anatomical, and transcriptional modifications. J Plant Growth Regul. https://doi.org/10.1007/s00344-021-10389-0
Mirakhorli T, Ardebili ZO, Ladan-Moghadam A, Danaee E (2021b) Bulk and nanoparticles of zinc oxide exerted their beneficial effects by conferring modifications in transcription factors, histone deacetylase, carbon and nitrogen assimilation, antioxidant biomarkers, and secondary metabolism in soybean . plos one pp.1–16. https://doi.org/10.1371/journal.pone.0256905
Moghadam AV, Iranbakhsh A, Saadatmand S, Ebadi M, Ardebili ZO (2021) New insights into the transcriptional, epigenetic, and physiological responses to zinc oxide nanoparticles in Datura stramonium; potential species for phytoremediation. J Plant Growth Regul. https://doi.org/10.1007/s00344-021-10305-6
Nakano R, Tashiro K, Aijima R, Hayashi N (2016) Effect of oxygen plasma irradiation on gene expression in plant seeds induced by active oxygen species. Plasma Med 6.https://doi.org/10.1615/plasmaMed.2016019093
Negi N, Khurana P (2021) A salicylic acid inducible mulberry WRKY transcription factor, Mi WRKY53 is involved in plant defence response. Plant Cell Rep, pp.1–21. https://doi.org/10.1007/s00299-021-02710-8
Neysanian M, Iranbakhsh A, Ahmadvand R, Oraghi Ardebili Z, Ebadi M (2020) Comparative efficacy of selenate and selenium nanoparticles for improving growth, productivity, fruit quality, and postharvest longevity through modifying nutrition, metabolism, and gene expression in tomato; potential benefits and risk assessment. PLoS ONE 15(12):e0244207. https://doi.org/10.1371/journal.pone.0244207
Pavasupree S, Chanchula N, Bootchanont A, Wattanawikkam C, Jitjing P, Boonyawan D, Porjai P (2021) Enhancement propagation of protocorms in orchid (Cymbidium tracyanum L. Castle) by cold atmospheric pressure air plasma Jet. Plasma Chem Plasma Process 41(2):573–589. https://doi.org/10.1007/s11090-020-10148-1
Pejam F, Ardebili ZO, Ladan-Moghadam A, Danaee E (2021) Zinc oxide nanoparticles mediated substantial physiological and molecular changes in tomato. Plos one, 16(3). https://doi.org/10.1371/journal.pone.0248778
Pérez-Pizá MC, Ibañez VN, Varela A, Cejas E, Ferreyra M, Chamorro-Garces JC, Zilli C, Vallecorsa P, Fina B, Prevosto L, Marfil CF (2021) Non-thermal plasmas affect plant growth and DNA methylation patterns in glycine max. J Plant Growth Regul, pp.1–11.
Rajaee Behbahani S, Iranbakhsh A, Ebadi M, Majd A, Ardebili ZO (2020) Red elemental selenium nanoparticles mediated substantial variations in growth, tissue differentiation, metabolism, gene transcription, epigenetic cytosine DNA methylation, and callogenesis in bittermelon (Momordica charantia); an in vitro experiment. Plos one, 15(7). https://doi.org/10.1371/journal.pone.0235556
Sheteiwy MS, An J, Mengqi Y, Xiaowen J, Yajing G, Fei H, Jin H (2019) Cold plasma treatment and exogenous salicylic acid priming enhances salinity tolerance of Oryza sativa seedlings. Protoplasma 256:79–99. https://doi.org/10.1007/s00709-018-1279-0
Siddique SS, Hardy GSJ, Bayliss KL (2018) Cold plasma: a potential new method to manage postharvest diseases caused by fungal plant pathogens. Plant Pathol 67(5):1011–1021. https://doi.org/10.1111/ppa.12825
Sotoodehnia-Korani S, Iranbakhsh A, Ebadi M, Majd A, Ardebili ZO (2020) Selenium nanoparticles induced variations in growth, morphology, anatomy, biochemistry, gene expression, and epigenetic DNA methylation in Capsicum annuum; an in vitro study. Environ Pollut 265,https://doi.org/10.1016/j.envpol.2020.114727
Starič P, Vogel-Mikuš K, Mozetič M, Junkar I (2020) Effects of nonthermal plasma on morphology, genetics and physiology of seeds: a review. Plants 9(12):1736. https://doi.org/10.3390/plants9121736
Suriyasak C, Hatanaka K, Tanaka H, Okumura T, Yamashita D, Attri P, Koga K, Shiratani M, Hamaoka N, Ishibashi Y (2021) Alterations of DNA methylation caused by cold plasma treatment restore delayed germination of heat-stressed rice (Oryza sativa L.) seeds. Agric Sci Technol 1(1):5–10. https://doi.org/10.1021/acsagscitech.0c00070
Tabatabaee S, Iranbakhsh A, Shamili M, Ardebili ZO (2021) Copper nanoparticles mediated physiological changes and transcriptional variations in microRNA159 (miR159) and mevalonate kinase (MVK) in pepper; potential benefits and phytotoxicity assessment. J Environ Chem Eng, 9(5). https://doi.org/10.1016/j.jece.2021.106151
Van Verk MC, Bol JF, Linthorst HJ (2011) WRKY transcription factors involved in activation of SA biosynthesis genes. BMC Plant Biol 11(1):1–12. https://doi.org/10.1186/1471-2229-11-89
Wróbel T, Dreger M, Wielgus K, Słomski R (2018) The application of plant in vitro cultures in cannabinoid production. Biotechnol Lett 40(3):445–454. https://doi.org/10.1007/s10529-017-2492-1
Yang X, Zhou Z, Fu M, Han M, Liu Z, Zhu C, Wang L, Zheng J, Liao Y, Zhang W, Ye J (2021) Transcriptome-wide identification of WRKY family genes and their expression profiling toward salicylic acid in Camellia japonica. Plant signal behav, 16(1). https://doi.org/10.1080/15592324.2020.1844508
Zhang JJ, Jo JO, Mongre RK, Ghosh M, Singh AK, Lee SB, Mok YS, Jeong DK (2017) Growth-inducing effects of argon plasma on soybean sprouts via the regulation of demethylation levels of energy metabolism-related genes. Sci Rep 7(1):1–12. https://doi.org/10.1038/srep41917
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Darigh, F., Iranbakhsh, A., Oraghi Ardebili, Z. et al. Non-thermal plasma improved callogenesis performance and elicited the production of cannabinoids by modifying DNA methylome, expression of WRKY1 and ERF1B transcription factors, and expression of genes that contributed to the biosynthesis of cannabinoids. Protoplasma 260, 159–170 (2023). https://doi.org/10.1007/s00709-022-01769-8
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DOI: https://doi.org/10.1007/s00709-022-01769-8