Published September 30, 2021 | Version v1

Triterpenic and phenolic acids production changed in Salvia officinalis via in vitro and in vivo polyploidization: A consequence of altered genes expression

  • 1. * & Department of Horticultural Science, Faculty of Agriculture, Bu Ali Sina University, 65174, Hamedan, Iran

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Tavan, Mansoureh, Sarikhani, Hassan, Mirjalili, Mohammad Hossein, Rigano, Maria Manuela, Azizi, Ali (2021): Triterpenic and phenolic acids production changed in Salvia officinalis via in vitro and in vivo polyploidization: A consequence of altered genes expression. Phytochemistry (112803) 189: 1-11, DOI: 10.1016/j.phytochem.2021.112803, URL: http://dx.doi.org/10.1016/j.phytochem.2021.112803

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urn:lsid:plazi.org:pub:9553FFB3FFD6FF8234786F4BAE12082D

References

  • Abdollahi-Ghehi, H., Sonboli, A., Ebrahimi, S.N., Esmaeili, M.A., Mirjalili, M.H., 2019. Triterpenic acid content and cytotoxicity of some Salvia species from Iran. Nat. Prod. Commun. 14 (5), 1-6. https://doi.org/10.1177/1934578X19842722.
  • Abedi, R., Babaei, A., Karimzadeh, G., 2015. Karyological and flow cytometric studies of Tulipa (Liliaceae) species from Iran. Plant Systemat. Evol. 301 (5), 1473-1484. https://doi.org/10.1007/s00606-014-1164-z.
  • Aghaei Jeshvaghani, Z., Rahimmalek, M., Talebi, M., Goli, S.A.H., 2015. Comparison of total phenolic content and antioxidant activity in different Salvia species using three model systems. Ind. Crop. Prod. 77, 409-414. https://doi.org/10.1016/j. indcrop.2015.09.005.
  • Ali, M., Hussain, R.M., Rehman, N.U., She, G., Li, P., Wan, X., Guo, L., Zhao, J., 2018. De novo transcriptome sequencing and metabolite profiling analyses reveal the complex metabolic genes involved in the terpenoid biosynthesis in Blue Anise Sage (Salvia guaranitica L.). DNA Res. 25 (6), 597-617. https://doi.org/10.1093/dnares/dsy028.
  • Ali, M., Li, P., She, G., Chen, D., Wan, X., Zhao, J., 2017. Transcriptome and metabolite analyses reveal the complex metabolic genes involved in volatile terpenoid biosynthesis in garden sage (Salvia officinalis). Sci. Rep. 7 (1), 16074. https://doi. org/10.1038/s41598-017-15478-3.
  • Aminfar, Z., Rabiei, B., Tohidfar, M., Mirjalili, M.H., 2019. Identification of key genes involved in the biosynthesis of triterpenic acids in the mint family. Sci. Rep. 9 (1), 15826. https://doi.org/10.1038/s41598-019-52090-z.
  • An, T., Zha, W., Zi, J., 2020. Biotechnological production of betulinic acid and derivatives and their applications. Appl. Microbiol. Biotechnol. 104 (8), 3339-3348. https://doi.org/10.1007/s00253-020-10495-1.
  • Aqafarini, A., Lotfi, M., Norouzi, M., Karimzadeh, G., 2019. Induction of tetraploidy in garden cress: morphological and cytological changes. Plant Cell Tissue Organ Cult. 137 (3), 627-635. https://doi.org/10.1007/s11240-019-01596-5.
  • Bakhtiar, Z., Mirjalili, M., Sonboli, A., Farimani, M., Ayyari, M., 2014. In vitro propagation, genetic and phytochemical assessment of Thymus persicus-a medicinally important source of pentacyclic triterpenoids. Biologia 69 (5), 594-603. https://doi.org/10.2478/s11756-014-0346-z.
  • Bendif, H., Peron, G., Miara, M.D., Sut, S., Dall' Acqua, S., Flamini, G., Maggi, F., 2020. Total phytochemical analysis of Thymus munbyanus subsp. coloratus from Algeria by HS-SPME-GC-MS, NMR and HPLC-MS studies. J. Pharmaceut. Biomed. Anal. 186, 113330. https://doi.org/10.1016/j.jpba.2020.113330.
  • Biswas, T., Dwivedi, U.N., 2019. Plant triterpenoid saponins: biosynthesis, in vitro production, and pharmacological relevance. Protoplasma 256 (6), 1463-1486. https://doi.org/10.1007/s00709-019-01411-0.
  • Chen, E.G., Tsai, K.L., Chung, H.H., Chen, J.T., 2018. Chromosome doubling-enhanced biomass and dihydrotanshinone I production in Salvia miltiorrhiza, a traditional Chinese medicinal plant. Molecules 23 (12), 3106. https://doi.org/10.3390/ molecules23123106.
  • Church, S.A., Spaulding, E.J., 2009. Gene expression in a wild autopolyploid sunflower series. J. Hered. 100 (4), 491-495. https://doi.org/10.1093/jhered/esp008.
  • D' Agostino, N., Buonanno, M., Ayoub, J., Barone, A., Monti, S.M., Rigano, M.M., 2019. Identification of non-specific lipid transfer protein gene family members in Solanum lycopersicum and insights into the features of Sola l 3 protein. Sci. Rep. 9 (1), 1607. https://doi.org/10.1038/s41598-018-38301-z.
  • Dhooghe, E., Van Laere, K., Eeckhaut, T., Leus, L., Van Huylenbroeck, J., 2019. Mitotic chromosome doubling of plant tissues in vitro. Plant Cell Tissue Organ Cult. 104 (3), 359-373. https://doi.org/10.1007/s11240-010-9786-5.
  • Dolezel, J., Bartos, J., Voglmayr, H., Greilhuber, J., 2003. Nuclear DNA content and genome size of trout and human. Cytometry 51 (2), 127-128. https://doi.org/ 10.1002/cyto.a.10013.
  • Doleˇzel, J., Bartoˇs, J., 2005. Plant DNA flow cytometry and estimation of nuclear genome size. Ann. Bot. 95 (1), 99-110. https://doi.org/10.1093/aob/mci005.
  • Dong, L., Pollier, J., Bassard, J.-E., Ntallas, G., Almeida, A., Lazaridi, E., Khakimov, B., Arendt, P., de Oliveira, L.S., Lota, F., Goossens, A., Michoux, F., Bak, S., 2018. Coexpression of squalene epoxidases with triterpene cyclases boosts production of triterpenoids in plants and yeast. Metab. Eng. 49, 1-12. https://doi.org/10.1016/j. ymben.2018.07.002.
  • Dweck, A., 2000. The folklore and cosmetic use of various Salvia species. Sage. The genus Salvia. 14, 1-25. https://doi.org/10.1201/9780203304556-11.
  • Ejtahed, R.S., Radjabian, T., Hoseini Tafreshi, S.A., 2015. Expression analysis of phenylalanine ammonia lyase gene and rosmarinic acid production in Salvia officinalis and Salvia virgata shoots under salicylic acid elicitation. Appl. Biochem. Biotechnol. 176 (7), 1846-1858. https://doi.org/10.1007/s12010-015-1682-3.
  • Firuzi, O., Miri, R., Asadollahi, M., Eslami, S., Jassbi, A.R., 2013. Cytotoxic, antioxidant and antimicrobial activities and phenolic contents of eleven salvia species from Iran. Iran. J. Pharm. Res. (IJPR) 12 (4), 801-810.
  • Fraga, C.G., Galleano, M., Verstraeten, S.V., Oteiza, P.I., 2010. Basic biochemical mechanisms behind the health benefits of polyphenols. Mol. Aspect. Med. 31 (6), 435-445. https://doi.org/10.1016/j.mam.2010.09.006.
  • Grouh, M.S.H., Meftahizade, H., Lotfi, N., Rahimi, V., Baniasadi, B., 2011. Doubling the chromosome number of Salvia hains using colchicine: evaluation of morphological traits of recovered plants. J. Med. Plants Res. 5 (19), 4892-4898.
  • Hamill, S., Smith, M., Dodd, W., 1992. In vitro induction of banana autotetraploids by colchicine treatment of micropropagated diploids. Aust. J. Bot. 40 (6), 887-896. https://doi.org/10.1071/BT9920887.
  • Hannweg, K., Visser, G., De Jager, K., Bertling, I., 2016. In vitro -induced polyploidy and its effect on horticultural characteristics, essential oil composition and bioactivity of Tetradenia riparia. South Afr. J. Bot. 106, 186-191. https://doi.org/10.1016/j. sajb.2016.07.013.
  • Haque, M.S., 1981. Chromosome numbers in the genus salvia linn. Indian Natl. Sci. Acad. Bull. 47, 419-426.
  • Haralampidis, K., Trojanowska, M., Osbourn, A.E., 2002. Biosynthesis of triterpenoid saponins in plants. In: Dutta, N.N., Hammar, F., Haralampidis, K., Karanth, N.G., K¨onig, A., Krishna, S.H., Kunze, G., Nagy, E., Orlich, B., Osbourn, A.E., Raghavarao, K.S.M.S., Riedel, K., Sahoo, G.C., Schom¨acker, R., Srinivas, N.D., Trojanowska, M. (Eds.), Hist Trends Bioprocess Biotransform, vols. 31-49. Springer Berlin Heidelberg, Berlin, Heidelberg.
  • Hoang, T.K., Hwang, Y.J., Lim, J.H., 2020. Chemical polyploidization of Chrysanthemum boreale. Plant Cell Tissue Organ Cult. 140 (3), 677-683. https://doi.org/10.1007/ s11240-019-01761-w.
  • J¨ager, S., Trojan, H., Kopp, T., Laszczyk, M.N., Scheffler, A., 2009. Pentacyclic triterpene distribution in various plants-rich sources for a new group of multi-potent plant extracts. Molecules 14 (6), 2016-2031. https://doi.org/10.3390/ molecules14062016.
  • Javadian, N., Karimzadeh, G., Sharifi, M., Moieni, A., Behmanesh, M., 2017. In vitro polyploidy induction: changes in morphology, podophyllotoxin biosynthesis, and expression of the related genes in Linum album (Linaceae). Planta 245 (6), 1165-1178. https://doi.org/10.1007/s00425-017-2671-2.
  • Kim, O.T., Kim, S.H., Ohyama, K., Muranaka, T., Choi, Y.E., Lee, H.Y., Kim, M.Y., Hwang, B., 2010. Upregulation of phytosterol and triterpene biosynthesis in Centella asiatica hairy roots overexpressed ginseng farnesyl diphosphate synthase. Plant Cell Rep. 29 (4), 403-411. https://doi.org/10.1007/s00299-010-0831-y.
  • Kobayashi, N., Yamashita, S., Ohta, K., Hosoki, T., 2008. Morphological characteristics and their inheritance in colchicine-induced Salvia polyploids. J. Jpn. Soc. Hortic. Sci. 77 (2), 186-191. https://doi.org/10.2503/jjshs1.77.186.
  • Kondo, H., Deguchi, A., Miyoshi, K., 2020. The efficient induction of tetraploid plants via adventitious shoots in Antirrhinum majus L. by in vitro seed treatment with amiprophos-methyl. Plant Cell Tissue Organ Cult. 142 (1), 157-166. https://doi.org/ 10.1007/s11240-020-01849-8.
  • Lavania, U.C., Srivastava, S., Lavania, S., Basu, S., Misra, N.K., Mukai, Y., 2012. Autopolyploidy differentially influences body size in plants, but facilitates enhanced accumulation of secondary metabolites, causing increased cytosine methylation. Plant J. 71 (4), 539-549. https://doi.org/10.1111/j.1365-313X.2012.05006.x.
  • Li, S., Lin, Y., Pei, H., Zhang, J., Zhang, J., Luo, J., 2020. Variations in colchicine-induced autotetraploid plants of Lilium davidii var. unicolor. Plant Cell Tissue Organ Cult. 1-10. https://doi.org/10.1007/s11240-020-01805-6.
  • Lin, X., Zhou, Y., Zhang, J., Lu, X., Zhang, F., Shen, Q., Wu, S., Chen, Y., Wang, T., Tang, K., 2011. Enhancement of artemisinin content in tetraploid Artemisia annua plants by modulating the expression of genes in artemisinin biosynthetic pathway. Biotechnol. Appl. Biochem. 58 (1), 50-57. https://doi.org/10.1002/bab.13.
  • Loureiro, J., Rodriguez, E., Doleˇzel, J., Santos, C., 2007. Two new nuclear isolation buffers for plant DNA flow cytometry: a test with 37 species. Ann. Bot. 100 (4), 875-888. https://doi.org/10.1093/aob/mcm152.
  • Lu, B.B., Du, Z., Ding, R.X., Zhang, L., Yu, X.J., Liu, C.H., Chen, W.S., 2006. Cloning and characterization of a differentially expressed phenylalanine ammonialyase gene (IiPAL) after genome duplication from tetraploid Isatis indigotica Fort. J. Integr. Plant Biol. 48 (12), 1439-1449. https://doi.org/10.1111/j.1744-7909.2006.00363.x.
  • Lynch, M., 2007. The Origins of Genome Architecture. Sinauer, Sunderland, MA. https:// doi.org/10.1086/596259.
  • Ma, Y.P., Wei, J.X., Yu, Z.Y., Qin, B., Dai, S.L., 2015. Characterization of ploidy levels in Chrysanthemum L. by flow cytometry. J. For. Res. 26 (3), 771-775. https://doi.org/ 10.1007/s11676-015-0071-7.
  • Mishra, B.K., Pathak, S., Sharma, A., Trivedi, P.K., Shukla, S., 2010. Modulated gene expression in newly synthesized auto-tetraploid of Papaver somniferum L. South Afr. J. Bot. 76 (3), 447-452. https://doi.org/10.1016/j.sajb.2010.02.090.
  • Misra, L., Dixit, A., Sharma, R., 1997. High concentration of hepatoprotective oleanolic acid and its derivatives in Lantana camara roots. Planta Med. 63 (6) https://doi.org/ 10.1055/s-2006-957780, 582-582.
  • Misra, R.C., Maiti, P., Chanotiya, C.S., Shanker, K., Ghosh, S., 2014. Methyl jasmonateelicited transcriptional responses and pentacyclic triterpene biosynthesis in sweet basil. Plant Physiol. 164 (2), 1028. https://doi.org/10.1104/pp.113.232884.
  • Miura, K., Kikuzaki, H., Nakatani, N., 2001. Apianane terpenoids from Salvia officinalis. Phytochemistry 58 (8), 1171-1175. https://doi.org/10.1016/S0031-9422(01) 00341-7.
  • Mo, L., Chen, J., Lou, X., Xu, Q., Dong, R., Tong, Z., Huang, H., Lin, E., 2020. Colchicine-induced polyploidy in Rhododendron fortunei lindl. Plants 9 (4), 424. https://doi.org/ 10.3390/plants9040424.
  • Moghaddam, M.G., Ahmad, F.B.H., Samzadeh-Kermani, A., 2012. Biological activity of betulinic acid: a review. Pharmacol. Pharm. 3 (2), 119-123. https://doi.org/ 10.4236/pp.2012.32018.
  • Moses, T., Pollier, J., Thevelein, J.M., Goossens, A., 2013. Bioengineering of plant (tri) terpenoids: from metabolic engineering of plants to synthetic biology in vivo and in vitro. New Phytol. 200 (1), 27-43. https://doi.org/10.1111/nph.12325.
  • Mutnoz-Bertomeu, J., Sales, E., Ros, R., Arrillaga, I., Segura, J., 2007. Up-regulation of an N-terminal truncated 3-hydroxy-3-methylglutaryl CoA reductase enhances production of essential oils and sterols in transgenic Lavandula latifolia. Plant Biotechnol. J. 5 (6), 746-758. https://doi.org/10.1111/j.1467-7652.2007.00286.x.
  • Noori, S.A.S., Norouzi, M., Karimzadeh, G., Shirkool, K., Niazian, M., 2017. Effect of colchicine-induced polyploidy on morphological characteristics and essential oil composition of ajowan (Trachyspermum ammi L.). Plant Cell Tissue Organ Cult. 130 (3), 543-551. https://doi.org/10.1007/s11240-017-1245-0.
  • Osborn, T.C., Pires, J.C., Birchler, J.A., Auger, D.L., Chen, Z.J., Lee, H.S., Comai, L., Madlung, A., Doerge, R., Colot, V., 2003. Understanding mechanisms of novel gene expression in polyploids. Trends Genet. 19 (3), 141-147. https://doi.org/10.1016/ S0168-9525(03)00015-5.
  • Osbourn, A., Goss, R.J., Field, R.A., 2011. The saponins: polar isoprenoids with important and diverse biological activities. Nat. Prod. Rep. 28 (7), 1261-1268. https://doi.org/10.1039/c1np00015b.
  • Pan-pan, H., Wei-xu, L., Hui-hui, L., 2018. In vitro induction and identification of autotetraploid of Bletilla striata (Thunb.) Reichb. f. by colchicine treatment. Plant Cell Tissue Organ Cult. 132 (3), 425-432. https://doi.org/10.1007/s11240-017- 1339-8.
  • Pereira, R.C., Santos, N.D.S., Bustamante, F.D.O., Mittelmann, A., Techio, V.H., 2017. Stability in chromosome number and DNA content in synthetic tetraploids of Lolium multiflorum after two generations of selection. Ciˆencia Rural. 47 (2), 1-5. https://doi. org/10.1590/0103-8478cr20150767.
  • Pisha, E., Chai, H., Lee, I.S., Chagwedera, T.E., Farnsworth, N.R., Cordell, G.A., Beecher, C.W., Fong, H.H., Kinghorn, A.D., Brown, D.M., 1995. Discovery of betulinic acid as a selective inhibitor of human melanoma that functions by induction of apoptosis. Nat. Med. 1 (10), 1046-1051. https://doi.org/10.1038/ nm1095-1046.
  • Qiao, G., Liu, M., Song, K., Li, H., Yang, H., Yin, Y., Zhuo, R., 2017. Phenotypic and comparative transcriptome analysis of different ploidy plants in Dendrocalamus latiflorus Munro. Front. Plant Sci. 8 https://doi.org/10.3389/fpls.2017.01371, 1371- 1371.
  • Ranjbar, M., Pakatchi, A., Babataheri, Z., 2015. Chromosome number evolution, biogeography and phylogenetic relationships in Salvia (Lamiaceae). Webbia 70 (2), 293-312. https://doi.org/10.1080/00837792.2015.1057982.
  • Sabzehzari, M., Hoveidamanesh, S., Modarresi, M., Mohammadi, V., 2019. Morphological, anatomical, physiological, and cytological studies in diploid and tetraploid plants of Plantago psyllium. Plant Cell Tissue Organ Cult. 139 (1), 131-137. https://doi.org/10.1007/s11240-019-01670-y.
  • Salma, U., Kundu, S., Hazra, A.K., Ali, M.N., Mandal, N., 2018. Augmentation of wedelolactone through in vitro tetraploid induction in Eclipta alba (L.) Hassk. Plant Cell Tissue Organ Cult. 133 (2), 289-298. https://doi.org/10.1007/s11240-018- 1381-1.
  • Salma, U., Kundu, S., Mandal, N., 2017. Artificial polyploidy in medicinal plants: advancement in the last two decades and impending prospects. J. Crop Sci. Biotechnol. 20 (1), 9-19. https://doi.org/10.1007/s12892-016-0080-1.
  • Seo, J.-W., Jeong, J.-H., Shin, C.-G., Lo, S.-C., Han, S.-S., Yu, K.-W., Harada, E., Han, J.- Y., Choi, Y.-E., 2005. Overexpression of squalene synthase in Eleutherococcus senticosus increases phytosterol and triterpene accumulation. Phytochemistry 66 (8), 869-877. https://doi.org/10.1016/j.phytochem.2005.02.016.
  • Siljak-Yakovlev, S., Pustahija, F., ˇSoli´c, E., Bogunic ´, F., Muratovi´c, E., Baˇsic ´, N., Catrice, O., Brown, S., 2010. Towards a genome size and chromosome number database of Balkan flora: C-values in 343 taxa with novel values for 242. Adv. Sci. Lett. 3 (2), 190-213. https://doi.org/10.1166/asl.2010.1115.
  • Skendi, A., Irakli, M., Chatzopoulou, P., 2017. Analysis of phenolic compounds in Greek plants of Lamiaceae family by HPLC. J. Appl. Res. Med. Aromat. Plants. 6, 62-69. https://doi.org/10.1016/j.jarmap.2017.02.001.
  • Tarkesh Esfahani, S., Karimzadeh, G., Naghavi, M.R., Vrieling, K., 2021. Altered gene expression and root thebaine production in polyploidized and methyl jasmonateelicited Papaver bracteatum Lindl. Plant Physiol. Biochem. 158, 334-341. https://doi. org/10.1016/j.plaphy.2020.11.021.
  • Tavan, M., Azizi, A., Sarikhani, H., Mirjalili, M.H., Rigano, M.M., 2020. Phenolics diversity among wild populations of Salvia multicaulis: as a precious source for antimicrobial and antioxidant applications. Nat. Prod. Res. 1-5 https://doi.org/ 10.1080/14786419.2020.1864369.
  • Tavan, M., Mirjalili, M.H., Karimzadeh, G., 2015. In vitro polyploidy induction: changes in morphological, anatomical and phytochemical characteristics of Thymus persicus (Lamiaceae). Plant Cell Tissue Organ Cult. 122 (3), 573-583. https://doi.org/ 10.1007/s11240-015-0789-0.
  • Topcu, G., 2006. Bioactive triterpenoids from Salvia species. J. Nat. Prod. 69 (3), 482-487. https://doi.org/10.1021/np0600402.
  • Ulubelen, A., 2000. III. Chemical Constituents 4. Terpenoids in the Genus Salvia. Genus Salvia 55.
  • Wang, L.J., Zhang, Q., Cao, Q.Z., Gao, X., Jia, G.X., 2020. An efficient method for inducing multiple genotypes of tetraploids Lilium rosthornii Diels. Plant Cell Tissue Organ Cult. 1-12. https://doi.org/10.1007/s11240-020-01807-4.
  • Wei, K.H., Xu, J.P., Li, L.X., Cai, J.Y., Miao, J.H., Li, M.H., 2018. In vitro induction and generation of tetraploid plants of Sophora tonkinensis Gapnep. Phcog. Mag. 14 (54), 149. https://doi.org/10.4103/pm.pm_170_17.
  • Widoretno, W., 2016. In vitro induction and characterization of tetraploid Patchouli (Pogostemon cablin Benth.) plant. Plant Cell Tissue Organ Cult. 125 (2), 261-267. https://doi.org/10.1007/s11240-016-0946-0.
  • Xie, Y., Chen, X., 2013. Structures required of polyphenols for inhibiting advanced glycation end products formation. Curr. Drug Metabol. 14 (4), 414-431. https://doi. org/10.2174/1389200211314040005.
  • Xie, Y., Yang, W., Chen, X., Xiao, J., 2014. Inhibition of flavonoids on acetylcholine esterase: binding and structure-activity relationship. Food Funct 5 (10), 2582-2589. https://doi.org/10.1039/c4fo00287c.
  • Zhou, J., Guo, F., Fu, J., Xiao, Y., Wu, J., 2020. In vitro polyploid induction using colchicine for Zingiber Officinale Roscoe cv. 'Fengtou' ginger. Plant Cell Tissue Organ Cult. 142 (1), 87-94. https://doi.org/10.1007/s11240-020-01842-1.
  • Zhou, Y., Kang, L., Liao, S., Pan, Q., Ge, X., Li, Z., 2015. Transcriptomic analysis reveals differential gene expressions for cell growth and functional secondary metabolites in induced autotetraploid of Chinese woad (Isatis indigotica Fort.). PloS One 10 (3), e0116392. https://doi.org/10.1371/journal.pone.0116392.
  • Zonneveld, B.J., 2019. The DNA weights per nucleus (genome size) of more than 2350 species of the Flora of The Netherlands, of which 1370 are new to science, including the pattern of their DNA peaks. Forum. Geobot. 8, 24-78. https://doi.org/10.3264/ FG.2019.1022.