Influence of Selected Heavy Metals on Cell Growth and Camphor Secretion in Achillea gypsicola Hub. Mor. In vitro Cell Cultures
Yıl 2023,
Cilt: 40 Sayı: 1, 11 - 18, 30.04.2023
Muhammed Akif Açıkgöz
,
Ebru Batı Ay
,
Şevket Metin Kara
,
Ahmet Aygün
Öz
The use of abiotic and biotic elicitors for increasing the accumulation of pharmaceutical active ingredients in plant tissues has gained an increasing interest worldwide. This study was intented to provide promoting accumulation of camphor and phenolic compound using cadmium chloride (CdCl2) and silver nitrate (AgNO3) in cell culture of Achillea gypsicola. Growing cells from 8-day-old cultures were treated with three concentrations (5, 25 and 50 µM) of CdCl2 and AgNO3, along with the control. The quantification of camphor and phenolic compound were performed using Headspace-GC-MS and spectrophotometer, respectively. The content of camphor and phenolic compound, cell number and cell dry weight were significantly affected by increasing doses of AgNO3 and CdCl2. The highest significant change in camphor content was observed in cell treated with 25 µM CdCl2 and AgNO3 with a 6.88 and 6.32 fold increase, respectively. The application of 50 µM AgNO3 and CdCl2, however, resulted in a rapid decine in all attributes studied, implying that culture of A. gypsicola is susceptible to elicitation by high concentrations of these elicitors. In conclusion, using AgNO3 and CdCl2 elicitors in cultured tissues of A. gypsicola would be of great importance to enhanced production of desired bioactive compounds of medicinal importance
Destekleyen Kurum
TUBITAK
Proje Numarası
No: 1001 - 114O564
Teşekkür
The authors gratefully thank to the Scientific and Technological Research Council of Turkey (TUBITAK) for the funding this study under grant No: 1001 - 114O564. This work is a part of the PhD thesis of M.A. Açıkgöz.
Kaynakça
- Açıkgöz, M. A. 2017. Achillea gypsicola türünde kallus kültürü ile sekonder metabolit üretim potansiyelinin belirlenmesi. Ordu University (Doctoral dissertation, PhD Thesis (Printed), Ordu).
- Açıkgöz, M. A., Yarılgaç, T., & Kara, Ş. M. 2018a. Enhancement of phytochemical compounds using biotic and abiotic elicitors in purple coneflower (Echinacea purpurea L.). Indian J Pharm Educ Res, 52, 140-145. https://doi.org/10.5530/ijper.52.4s.90
- Açıkgöz, M. A., Kara, Ş. M., Ebru, B. A., & Odabaş, S. 2018b. Effect of light on biosynthesis of alkamide, caffeic acid derivatives and echinacoside in Echinacea purpurea L. callus cultures. Akademik Ziraat Dergisi, 7(2), 179-184. https://doi.org/10.29278/azd.476349
- Açıkgöz, M. A. 2019. Evaluation of Phytochemical Compositions and Biological Properties of Achillea gypsicola at Different Phenological Stages. Chemistry & Biodiversity, 16(12), e1900373. https://doi.org/10.1002/cbdv.201900373
- Açıkgöz, M.A., Kara, S.M., Aygun, A., Ozcan, M.M. & Ay, E.B. 2019. Effects of methyl jasmonate and salicylic acid on the production of camphor and phenolic compounds in cell suspension culture of endemic Turkish yarrow (Achillea gypsicola) species. Turkish Journal of Agriculture and Forestry 43:19. https://doi.org/10.3906/tar-1809-54
- Açıkgöz, M. A. 2020a. Establishment of cell suspension cultures of Ocimum basilicum L. and enhanced production of pharmaceutical active ingredients. Industrial crops and products, 148, 112278. https://doi.org/10.1016/j.indcrop.2020.112278
- Açıkgöz, M. A. 2020b. Determination of essential oil compositions and antimicrobial activity of Achillea gypsicola Hub.-Mor. at different plant parts and phenological stages. Journal of Essential Oil Research, 32(4), 331-347. https://doi.org/10.1080/10412905.2020.1750496
- Açıkgöz, M. A. 2021. Effects of sorbitol on the production of phenolic compounds and terpenoids in the cell suspension cultures of Ocimum basilicum L. Biologia, 76(1), 395-409. https://doi.org/10.2478/s11756-020-00581-0
- Açıkgöz, M. A., Ebru, B. A., Aygün, A., & Kara, Ş. M. 2022. Light-Mediated Biosynthesis of Phenylpropanoid Metabolites in Cell Suspension Cultures of Turkish Yarrow (Achillea gypsicola Hub. Mor.). Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 25(6), 1234-1242. https://doi.org/10.18016/ksutarimdoga.vi.926160
- Ashtiani, S.R., Hasanloo, T. & Bihamta, M.R. 2010. Enhanced production of silymarin by Ag+ elicitor in cell suspension cultures of Silybum marianum. Pharmaceutical Biology 48 (6): 708-715. https://doi.org/10.3109/13880200903264426
- Baser, K.H.C. 2002. Aromatic biodiversity among the flowering plant taxa of Turkey. Pure Applied Chemistry 74: 527-545. https://doi.org/10.1351/pac200274040527
- Bourgaud, F., Gravot, A., Milesi, S. & Gontier, E. 2001. Production of plant secondary metabolites, a historical perspective. Plant Science 5: 839-851. https://doi.org/10.1016/S0168-9452(01)00490-3
- Cai, Z., Kastell, A., Knorr, D. & Smetanska, I. 2012. Exudation: an expanding technique for continuous production and release of secondary metabolites from plant cell suspension and hairy root cultures. Plant Cell Reports 31: 461-477. https://doi.org/10.1007/s00299-011-1165-0
- Cetin, E.S., Babalik, Z., Hallac-Turk, F. & Gokturk-Baydar, N. 2014. The effects of cadmium chloride on secondary metabolite production in Vitis vinifera cv. cell suspension cultures. Biological Research 47:47. https://doi.org/10.1186/0717-6287-47-47
- Dağlioğlu, Y., Açıkgöz, M. A., Özcan, M. M., & Kara, Ş. M. 2022. Impact of application of alumina oxide nanoparticles on callus induction, pigment content, cell damage and antioxidant enzyme activities in Ocimum basilicum. Journal of International Environmental Application and Science, 17(1), 22-33.
- Dai, G.H., Andary, C., Mondolot, L. & Boubals, D. 1995. Involment of phenolic compounds in the resistance of grapevine callus to downy mildew (Plasmopara viticola). European Journal of Plant Pathology 101: 541-547. https://doi.org/10.1007/BF01874479
- Davies, K.M. & Deroles, S.C. 2014. Prospects for the use of plant cell cultures in food biotechnology. Current Opinion in Biotechnology 26:133-140. https://doi.org/10.1016/j.copbio.2013.12.010
- Demirci, B., Baser, K.H.C., Aytac, Z., Khan, S.I., Jacob, M.R. & Tabanca, N. 2018. Comparative study of three Achillea essential oils from eastern part of Turkey and their biological activities. Records of Natural Products 12: 195-200. https://dx.doi.org/10.25135/rnp.09.17.03.019
- Ebru, B. A., Kocaman, B., Öner, E. K., & Açıkgöz, M. A. (2022). Effects of elicitors on secondary metabolite (SM) production and antioxidant activity in sweet basil (Ocimum basilicum L.) cell suspension cultures. Notulae Scientia Biologicae, 14(2), 11246-11246. https://doi.org/10.55779/nsb14211246
- Georgiev, M.I., Weber, J. & Maciuk, A. 2009. Bioprocessing of plant cell cultures for mass production of targeted compounds. Applied Microbiology and Biotechnology 83: 809-823. https://doi.org/10.1007/s00253-009-2049-x
- Ghanati, F., Bakhtiarian, S., Parast, B.M. & Behrooz, M.K. 2014. Production of new active phytocompounds by Achillea millefolium L. after elicitation with silver nanoparticles and methyl jasmonate. Biosciences Biotechnology Research Asia 11(2): 391-399. http://dx.doi.org/10.13005/bbra/1287
- Halder, M., Sarkar, S. & Jha, S. 2019. Elicitation: A biotechnological tool for enhanced production of secondary metabolites in hairy root cultures. Engineering in Life Sciences 19: 880-895. https://doi.org/10.1016/j.copbio.2013.12.010
- Isah, T., Umar, S., Mujib, A., Sharma, M.P., Rajasekharan, P.E., Zafar, N. & Frukh, A. 2018. Secondary metabolism of pharmaceuticals in the plant in vitro cultures: strategies, approaches, and limitations to achieving higher yield. Plant Cell, Tissue and Organ Culture 132: 239-265. https://doi.org/10.1007/s11240-017-1332-2
- Jamwal, K., Bhattacharya, S. & Puri, S. 2018. Plant growth regulator mediated consequences of secondary metabolites in medicinal plants. Journal of Applied Research on Medicinal and Aromatic Plants 9: 26-38. https://doi.org/10.1016/j.jarmap.2017.12.003
- Kim, O.T., Kim, M.Y., Hong, M.H., Ahn, J.C. & Hwang, B. 2004. Stimulation of asiaticoside accumulation in the whole plant cultures of Centella asiatica (L.) Urban by elicitors. Plant Cell Reportes 23: 339-344. https://doi.org/10.1016/j.jarmap.2017.12.003
- Laloue, M., Courtois, D. & Manigault, P. 1980. Convenient and rapid fluorescent staining of plant cell nuclei with “33258” Hoechst. Plant Science Letter 17: 175-179. https://doi.org/10.1016/0304-4211(80)90145-5
- Matkowski, A. 2008. Plant in vitro culture for the production of antioxidants – A review. Biotechnology Advances 26: 548-560. https://doi.org/10.1016/j.biotechadv.2008.07.001
- Mohammadhosseini, M., Sarker, S.D. & Akbarzadeh, A. 2017. Chemical composition of the essential oils and extract of Achillea species and their biological activities: a review. Journal of Ethnopharmacology 199: 257-315. https://doi.org/10.1016/j.jep.2017.02.010
- Moroff, G., Eich, J. & Dabay, M. 1994. Validation of use of the Nageotte hemocytometer to count low levels of white cells in white cell reduced platelet components. Transfusion 34: 35-38. https://doi.org/10.1046/j.1537-2995.1994.34194098600.x
- Murthy, H.N., Lee, E.J. & Paek, K.Y. 2014. Production of secondary metabolites from cell and organ cultures: strategies and approaches for biomass improvement and metabolite accumulation. Plant Cell, Tissue and Organ Culture 118:1-16. https://doi.org/10.1007/s11240-014-0467-7
- Namdeo, AG., Patil, S. & Fulzele, D.P. 2002. Influence of fungal elicitors on production of ajmalicine by cell cultures of Catharanthus roseus. Biotechnology Progress 18: 159-162. https://doi.org/10.1021/bp0101280
- Nosov, A.M. 2012. Application of cell technologies for production of plant derived bioactive substances of plant origin. Applied Biochemistry and Microbiology 48(7): 609-624. https://doi.org/10.1134/S000368381107009X
- Park, W.T., Arasu, M.V., Al-Dhabi, N.A., Yeo, S.K., Jeon, J., Park, J.S. & Park, S.U. 2016. Yeast extract and silver nitrate induce the expression of phenylpropanoid biosynthetic genes and induce the accumulation of rosmarinic acid in Agastache rugosa cell culture. Molecules, 21: 426. https://doi.org/10.3390/molecules21040426
- Pitta–Alvarez, S.I., Spollansky, T.C. & Giulietti, A.M. 2000. The influence of different biotic and abiotic elicitors on the production and profile of tropane alkaloids in hairy root cultures of Brugmansia candida. Enzyme and Microbial Technology 26: 252-258. https://doi.org/10.1016/S0141-0229(99)00137-4
- Prior, R.L., Fan, E., Ji, H., Howell, A., Nio, C., Payne, M.J. & Reed, J. 2010. Multi‐laboratory validation of a standard method for quantifying proanthocyanidins in cranberry powders. Journal of the Science of Food and Agriculture 90(9): 1473-1478. https://doi.org/10.1002/jsfa.3966
- Radman, R., Saez, T., Bucke, C. & Keshavarz, T. 2003. Elicitation of plants and microbial cell systems. Biotechnology and Applied Biochemistry 37: 91-102. https://doi.org/10.1042/BA20020118
- Ramakrishna, A. & Ravishankar, G.A. 2011. Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behavior 6(11): 1720-1731. https://doi.org/10.4161/psb.6.11.17613
- Ramirez-Estrada, K., Vidal-Limon, H., Hidalgo, D., Moyano, E., Golenioswki, M., Cusidó, R.M. & Palazon, J. 2016. Elicitation, an effective strategy for the biotechnological production of bioactive high-added value compounds in plant cell factories. Molecules 21: 182. https://doi.org/10.3390/molecules21020182
- Rao, S.R. & Ravishankar, G.A. 2002. Plant cell cultures: chemical factories of secondary metabolites. Biotechnology Advances 20: 101-153. https://doi.org/10.1016/S0734-9750(02)00007-1
- Qu, J.G., Zhang, W., Jin, M.F. & Yu, X.J. 2006. Effect of homogeneity on cell growth and anthocyanin biosynthesis in suspension cultures of Vitis vinifera. Chinese Journal of Biotechnology 22: 805-510. https://doi.org/10.1016/S1872-2075(06)60057-5
- Smetanska, I. 2008. Production of secondary metabolites using plant cell cultures. Advances in Biochemical Engineering/Biotechnology 111: 187-228. https://doi.org/10.1007/10_2008_103
- Srivastava, M., Singh, G., Sharma, S., Shukla, S. & Misra, P. 2019. Elicitation enhanced the yield of glycyrrhizin and antioxidant activities in hairy root cultures of Glycyrrhiza glabra L. Journal of Plant Growth Regulation 38: 373-384. https://doi.org/10.1007/s00344-018-9847-2
- Thakur, M., Bhattacharya, S., Khosla, P.K. & Puri, S. 2019. Improving production of plant secondary metabolites through biotic and abiotic elicitation. Journal of Applied Research on Medicinal and Aromatic Plants 12: 1-12. https://doi.org/10.1016/j.jarmap.2018.11.004
- Verma, N. & Shukla, S. 2015. Impact of various factors responsible for fluctuation in plant secondary metabolites. Journal of Applied Research on Medicinal and Aromatic Plants 2: 105-113. https://doi.org/10.1016/j.jarmap.2015.09.002
- Yue, W., Ming, Q.L., Lin, B., Rahman, K., Zheng C.J., Ting, H. & Qin, L.P. 2016. Medicinal plant cell suspension cultures: pharmaceutical applications and high-yielding strategies for the desired Yue, W., Ming, Q.L., Lin, B., Rahman, K., Zheng C.J., Ting, H. & Qin, L.P. 2016. Medicinal plant cell suspension cultures: pharmaceutical applications and high-yielding strategies for the desired secondary metabolites. Critical Reviews in Biotechnology 36 (2): 215-232. secondary metabolites. Critical Reviews in Biotechnology 36 (2): 215-232. https://doi.org/10.3109/07388551.2014.923986
- Zhao, J., Davis, L.C. & Werpoorte, R. 2005. Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnology Advances 23: 283-333. https://doi.org/10.1016/j.biotechadv.2005.01.003
- Zhao, J.L., Zhou, L.G. & Wu, J.Y. 2010. Effects of biotic and abiotic elicitors on cell growth and tanshinone accumulation in Salvia miltiorrhiza cell cultures. Applied Microbiology and Biotechnology 87: 137-144. https://doi.org/10.1007/s00253-010-2443-4
- Zafar, N., Mujib, A., Ali, M., Tonk, D., Gulzar, B.., Malik, M.O., Mamgain, J. & Sayeed, R. 2020. Cadmium chloride (CdCl2) elicitation improves reserpine and ajmalicine yield in Rauvolfia serpentina as revealed by high‑performance thin‑layer chromatography (HPTLC). 3 Biotech 10: 344. https://doi.org/10.1007/s13205-020-02339-6
Achillea gypsicola Hub. Mor. In vitro Hücre Kültürlerinde Seçilmiş Ağır Metallerin Hücre Büyümesi ve Kamfor Birikimi Üzerindeki Etkisi
Yıl 2023,
Cilt: 40 Sayı: 1, 11 - 18, 30.04.2023
Muhammed Akif Açıkgöz
,
Ebru Batı Ay
,
Şevket Metin Kara
,
Ahmet Aygün
Öz
Farmasötik aktif bileşenlerin bitki dokularında birikimini arttırmak için abiyotik ve biyotik elisitörlerin kullanımı dünya çapında artan bir ilgi kazanmıştır. Bu çalışma, Achillea gypsicola hücre kültüründe kadmiyum klorür (CdCl2) ve gümüş nitrat (AgNO3) kullanılarak kamfor ve fenolik bileşik birikimini teşvik etmeyi amaçlamıştır. Sekiz günlük kültürlerden büyüyen hücreler, kontrol ile birlikte üç konsantrasyonda (5, 25 ve 50 uM) CdCl2 ve AgNO3 ile muamele edildi. Kamfor ve fenolik bileşik miktar tayini sırasıyla Headspace-GC-MS ve spektrofotometre kullanılarak yapıldı. Kamfor ve fenolik bileşik miktarı, hücre sayısı ve hücre kuru ağırlığı, artan AgNO3 ve CdCl2 dozlarından önemli ölçüde etkilenmiştir. Kamfor miktarındaki en önemli değişiklik, sırasıyla 6.88 ve 6.32 kat artışla 25 uM CdCl2 ve AgNO3 ile muamele edilen hücrede gözlendi. Bununla birlikte, 50 uM AgNO3 ve CdCl2'nin uygulanması, çalışılan tüm özelliklerde hızlı bir düşüşle sonuçlandı ve bu, A. gypsicola'nın süspansiyon kültürünün bu elisitörlerin yüksek konsantrasyonları tarafından ortaya çıkmaya duyarlı olduğunu ima etti. Sonuç olarak, A. gypsicola'nın kültürlenmiş dokularında AgNO3 ve CdCl2 elisitörlerinin kullanılması, tıbbi öneme sahip arzu edilen biyoaktif bileşiklerin üretiminin arttırılması için büyük önem taşıyacaktır.
Proje Numarası
No: 1001 - 114O564
Kaynakça
- Açıkgöz, M. A. 2017. Achillea gypsicola türünde kallus kültürü ile sekonder metabolit üretim potansiyelinin belirlenmesi. Ordu University (Doctoral dissertation, PhD Thesis (Printed), Ordu).
- Açıkgöz, M. A., Yarılgaç, T., & Kara, Ş. M. 2018a. Enhancement of phytochemical compounds using biotic and abiotic elicitors in purple coneflower (Echinacea purpurea L.). Indian J Pharm Educ Res, 52, 140-145. https://doi.org/10.5530/ijper.52.4s.90
- Açıkgöz, M. A., Kara, Ş. M., Ebru, B. A., & Odabaş, S. 2018b. Effect of light on biosynthesis of alkamide, caffeic acid derivatives and echinacoside in Echinacea purpurea L. callus cultures. Akademik Ziraat Dergisi, 7(2), 179-184. https://doi.org/10.29278/azd.476349
- Açıkgöz, M. A. 2019. Evaluation of Phytochemical Compositions and Biological Properties of Achillea gypsicola at Different Phenological Stages. Chemistry & Biodiversity, 16(12), e1900373. https://doi.org/10.1002/cbdv.201900373
- Açıkgöz, M.A., Kara, S.M., Aygun, A., Ozcan, M.M. & Ay, E.B. 2019. Effects of methyl jasmonate and salicylic acid on the production of camphor and phenolic compounds in cell suspension culture of endemic Turkish yarrow (Achillea gypsicola) species. Turkish Journal of Agriculture and Forestry 43:19. https://doi.org/10.3906/tar-1809-54
- Açıkgöz, M. A. 2020a. Establishment of cell suspension cultures of Ocimum basilicum L. and enhanced production of pharmaceutical active ingredients. Industrial crops and products, 148, 112278. https://doi.org/10.1016/j.indcrop.2020.112278
- Açıkgöz, M. A. 2020b. Determination of essential oil compositions and antimicrobial activity of Achillea gypsicola Hub.-Mor. at different plant parts and phenological stages. Journal of Essential Oil Research, 32(4), 331-347. https://doi.org/10.1080/10412905.2020.1750496
- Açıkgöz, M. A. 2021. Effects of sorbitol on the production of phenolic compounds and terpenoids in the cell suspension cultures of Ocimum basilicum L. Biologia, 76(1), 395-409. https://doi.org/10.2478/s11756-020-00581-0
- Açıkgöz, M. A., Ebru, B. A., Aygün, A., & Kara, Ş. M. 2022. Light-Mediated Biosynthesis of Phenylpropanoid Metabolites in Cell Suspension Cultures of Turkish Yarrow (Achillea gypsicola Hub. Mor.). Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 25(6), 1234-1242. https://doi.org/10.18016/ksutarimdoga.vi.926160
- Ashtiani, S.R., Hasanloo, T. & Bihamta, M.R. 2010. Enhanced production of silymarin by Ag+ elicitor in cell suspension cultures of Silybum marianum. Pharmaceutical Biology 48 (6): 708-715. https://doi.org/10.3109/13880200903264426
- Baser, K.H.C. 2002. Aromatic biodiversity among the flowering plant taxa of Turkey. Pure Applied Chemistry 74: 527-545. https://doi.org/10.1351/pac200274040527
- Bourgaud, F., Gravot, A., Milesi, S. & Gontier, E. 2001. Production of plant secondary metabolites, a historical perspective. Plant Science 5: 839-851. https://doi.org/10.1016/S0168-9452(01)00490-3
- Cai, Z., Kastell, A., Knorr, D. & Smetanska, I. 2012. Exudation: an expanding technique for continuous production and release of secondary metabolites from plant cell suspension and hairy root cultures. Plant Cell Reports 31: 461-477. https://doi.org/10.1007/s00299-011-1165-0
- Cetin, E.S., Babalik, Z., Hallac-Turk, F. & Gokturk-Baydar, N. 2014. The effects of cadmium chloride on secondary metabolite production in Vitis vinifera cv. cell suspension cultures. Biological Research 47:47. https://doi.org/10.1186/0717-6287-47-47
- Dağlioğlu, Y., Açıkgöz, M. A., Özcan, M. M., & Kara, Ş. M. 2022. Impact of application of alumina oxide nanoparticles on callus induction, pigment content, cell damage and antioxidant enzyme activities in Ocimum basilicum. Journal of International Environmental Application and Science, 17(1), 22-33.
- Dai, G.H., Andary, C., Mondolot, L. & Boubals, D. 1995. Involment of phenolic compounds in the resistance of grapevine callus to downy mildew (Plasmopara viticola). European Journal of Plant Pathology 101: 541-547. https://doi.org/10.1007/BF01874479
- Davies, K.M. & Deroles, S.C. 2014. Prospects for the use of plant cell cultures in food biotechnology. Current Opinion in Biotechnology 26:133-140. https://doi.org/10.1016/j.copbio.2013.12.010
- Demirci, B., Baser, K.H.C., Aytac, Z., Khan, S.I., Jacob, M.R. & Tabanca, N. 2018. Comparative study of three Achillea essential oils from eastern part of Turkey and their biological activities. Records of Natural Products 12: 195-200. https://dx.doi.org/10.25135/rnp.09.17.03.019
- Ebru, B. A., Kocaman, B., Öner, E. K., & Açıkgöz, M. A. (2022). Effects of elicitors on secondary metabolite (SM) production and antioxidant activity in sweet basil (Ocimum basilicum L.) cell suspension cultures. Notulae Scientia Biologicae, 14(2), 11246-11246. https://doi.org/10.55779/nsb14211246
- Georgiev, M.I., Weber, J. & Maciuk, A. 2009. Bioprocessing of plant cell cultures for mass production of targeted compounds. Applied Microbiology and Biotechnology 83: 809-823. https://doi.org/10.1007/s00253-009-2049-x
- Ghanati, F., Bakhtiarian, S., Parast, B.M. & Behrooz, M.K. 2014. Production of new active phytocompounds by Achillea millefolium L. after elicitation with silver nanoparticles and methyl jasmonate. Biosciences Biotechnology Research Asia 11(2): 391-399. http://dx.doi.org/10.13005/bbra/1287
- Halder, M., Sarkar, S. & Jha, S. 2019. Elicitation: A biotechnological tool for enhanced production of secondary metabolites in hairy root cultures. Engineering in Life Sciences 19: 880-895. https://doi.org/10.1016/j.copbio.2013.12.010
- Isah, T., Umar, S., Mujib, A., Sharma, M.P., Rajasekharan, P.E., Zafar, N. & Frukh, A. 2018. Secondary metabolism of pharmaceuticals in the plant in vitro cultures: strategies, approaches, and limitations to achieving higher yield. Plant Cell, Tissue and Organ Culture 132: 239-265. https://doi.org/10.1007/s11240-017-1332-2
- Jamwal, K., Bhattacharya, S. & Puri, S. 2018. Plant growth regulator mediated consequences of secondary metabolites in medicinal plants. Journal of Applied Research on Medicinal and Aromatic Plants 9: 26-38. https://doi.org/10.1016/j.jarmap.2017.12.003
- Kim, O.T., Kim, M.Y., Hong, M.H., Ahn, J.C. & Hwang, B. 2004. Stimulation of asiaticoside accumulation in the whole plant cultures of Centella asiatica (L.) Urban by elicitors. Plant Cell Reportes 23: 339-344. https://doi.org/10.1016/j.jarmap.2017.12.003
- Laloue, M., Courtois, D. & Manigault, P. 1980. Convenient and rapid fluorescent staining of plant cell nuclei with “33258” Hoechst. Plant Science Letter 17: 175-179. https://doi.org/10.1016/0304-4211(80)90145-5
- Matkowski, A. 2008. Plant in vitro culture for the production of antioxidants – A review. Biotechnology Advances 26: 548-560. https://doi.org/10.1016/j.biotechadv.2008.07.001
- Mohammadhosseini, M., Sarker, S.D. & Akbarzadeh, A. 2017. Chemical composition of the essential oils and extract of Achillea species and their biological activities: a review. Journal of Ethnopharmacology 199: 257-315. https://doi.org/10.1016/j.jep.2017.02.010
- Moroff, G., Eich, J. & Dabay, M. 1994. Validation of use of the Nageotte hemocytometer to count low levels of white cells in white cell reduced platelet components. Transfusion 34: 35-38. https://doi.org/10.1046/j.1537-2995.1994.34194098600.x
- Murthy, H.N., Lee, E.J. & Paek, K.Y. 2014. Production of secondary metabolites from cell and organ cultures: strategies and approaches for biomass improvement and metabolite accumulation. Plant Cell, Tissue and Organ Culture 118:1-16. https://doi.org/10.1007/s11240-014-0467-7
- Namdeo, AG., Patil, S. & Fulzele, D.P. 2002. Influence of fungal elicitors on production of ajmalicine by cell cultures of Catharanthus roseus. Biotechnology Progress 18: 159-162. https://doi.org/10.1021/bp0101280
- Nosov, A.M. 2012. Application of cell technologies for production of plant derived bioactive substances of plant origin. Applied Biochemistry and Microbiology 48(7): 609-624. https://doi.org/10.1134/S000368381107009X
- Park, W.T., Arasu, M.V., Al-Dhabi, N.A., Yeo, S.K., Jeon, J., Park, J.S. & Park, S.U. 2016. Yeast extract and silver nitrate induce the expression of phenylpropanoid biosynthetic genes and induce the accumulation of rosmarinic acid in Agastache rugosa cell culture. Molecules, 21: 426. https://doi.org/10.3390/molecules21040426
- Pitta–Alvarez, S.I., Spollansky, T.C. & Giulietti, A.M. 2000. The influence of different biotic and abiotic elicitors on the production and profile of tropane alkaloids in hairy root cultures of Brugmansia candida. Enzyme and Microbial Technology 26: 252-258. https://doi.org/10.1016/S0141-0229(99)00137-4
- Prior, R.L., Fan, E., Ji, H., Howell, A., Nio, C., Payne, M.J. & Reed, J. 2010. Multi‐laboratory validation of a standard method for quantifying proanthocyanidins in cranberry powders. Journal of the Science of Food and Agriculture 90(9): 1473-1478. https://doi.org/10.1002/jsfa.3966
- Radman, R., Saez, T., Bucke, C. & Keshavarz, T. 2003. Elicitation of plants and microbial cell systems. Biotechnology and Applied Biochemistry 37: 91-102. https://doi.org/10.1042/BA20020118
- Ramakrishna, A. & Ravishankar, G.A. 2011. Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behavior 6(11): 1720-1731. https://doi.org/10.4161/psb.6.11.17613
- Ramirez-Estrada, K., Vidal-Limon, H., Hidalgo, D., Moyano, E., Golenioswki, M., Cusidó, R.M. & Palazon, J. 2016. Elicitation, an effective strategy for the biotechnological production of bioactive high-added value compounds in plant cell factories. Molecules 21: 182. https://doi.org/10.3390/molecules21020182
- Rao, S.R. & Ravishankar, G.A. 2002. Plant cell cultures: chemical factories of secondary metabolites. Biotechnology Advances 20: 101-153. https://doi.org/10.1016/S0734-9750(02)00007-1
- Qu, J.G., Zhang, W., Jin, M.F. & Yu, X.J. 2006. Effect of homogeneity on cell growth and anthocyanin biosynthesis in suspension cultures of Vitis vinifera. Chinese Journal of Biotechnology 22: 805-510. https://doi.org/10.1016/S1872-2075(06)60057-5
- Smetanska, I. 2008. Production of secondary metabolites using plant cell cultures. Advances in Biochemical Engineering/Biotechnology 111: 187-228. https://doi.org/10.1007/10_2008_103
- Srivastava, M., Singh, G., Sharma, S., Shukla, S. & Misra, P. 2019. Elicitation enhanced the yield of glycyrrhizin and antioxidant activities in hairy root cultures of Glycyrrhiza glabra L. Journal of Plant Growth Regulation 38: 373-384. https://doi.org/10.1007/s00344-018-9847-2
- Thakur, M., Bhattacharya, S., Khosla, P.K. & Puri, S. 2019. Improving production of plant secondary metabolites through biotic and abiotic elicitation. Journal of Applied Research on Medicinal and Aromatic Plants 12: 1-12. https://doi.org/10.1016/j.jarmap.2018.11.004
- Verma, N. & Shukla, S. 2015. Impact of various factors responsible for fluctuation in plant secondary metabolites. Journal of Applied Research on Medicinal and Aromatic Plants 2: 105-113. https://doi.org/10.1016/j.jarmap.2015.09.002
- Yue, W., Ming, Q.L., Lin, B., Rahman, K., Zheng C.J., Ting, H. & Qin, L.P. 2016. Medicinal plant cell suspension cultures: pharmaceutical applications and high-yielding strategies for the desired Yue, W., Ming, Q.L., Lin, B., Rahman, K., Zheng C.J., Ting, H. & Qin, L.P. 2016. Medicinal plant cell suspension cultures: pharmaceutical applications and high-yielding strategies for the desired secondary metabolites. Critical Reviews in Biotechnology 36 (2): 215-232. secondary metabolites. Critical Reviews in Biotechnology 36 (2): 215-232. https://doi.org/10.3109/07388551.2014.923986
- Zhao, J., Davis, L.C. & Werpoorte, R. 2005. Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnology Advances 23: 283-333. https://doi.org/10.1016/j.biotechadv.2005.01.003
- Zhao, J.L., Zhou, L.G. & Wu, J.Y. 2010. Effects of biotic and abiotic elicitors on cell growth and tanshinone accumulation in Salvia miltiorrhiza cell cultures. Applied Microbiology and Biotechnology 87: 137-144. https://doi.org/10.1007/s00253-010-2443-4
- Zafar, N., Mujib, A., Ali, M., Tonk, D., Gulzar, B.., Malik, M.O., Mamgain, J. & Sayeed, R. 2020. Cadmium chloride (CdCl2) elicitation improves reserpine and ajmalicine yield in Rauvolfia serpentina as revealed by high‑performance thin‑layer chromatography (HPTLC). 3 Biotech 10: 344. https://doi.org/10.1007/s13205-020-02339-6