Detection of bioactive compounds and amino acids from fruiting bodies of Morchella tridentina
Tariq Saiff Ullah
Researcherhttps://orcid.org/0000-0002-7446-6263
Syeda S. Firdous
Department of Botany, Women University of Azad Jammu and Kashmir Bagh, PakistanAnsar Mehmood
Department of Botany, University of Poonch Rawalakot, 12350 Azad Kashmir, Pakistanhttps://orcid.org/0000-0002-6120-5646
Javaid Q. Swati
Department of Botany, University of Azad Jammu and Kashmir, Muzaffarabad, PakistanMuhammad Usman
Fungal Biology and Systematics Research Laboratory, Institute of Botany, University of the Punjab, Quaid-e-Azam Campus, 54590 Lahore, Pakistanhttps://orcid.org/0000-0002-3490-058X
Abdul N. Khalid
Fungal Biology and Systematics Research Laboratory, Institute of Botany, University of the Punjab, Quaid-e-Azam Campus, 54590 Lahore, Pakistanhttps://orcid.org/0000-0002-5635-8031
Abstract
Morels are well known due to their nutritional and food value since ancient human history. In this study, biochemical and proteomic analyses were carried out on the ascocarp of Morchella tridentina Bres. For this, several ascocarp of M. tridentina were collected from different sites of Neelum Valley Azad Jammu and Kashmir, Pakistan. Identification was confirmed by phylogenetic sequencing using nuclear ribosomal DNA bar-coding technique along with morph-anatomical analysis. During the biochemical analysis, different bioactive compounds used in drugs to treat cancer, heart diseases, edema (veprisinium, visnagin, and bumetanide), and breast cancer (petunidin) were identified. Cerulinin, daidzein, guanthidin and okanin (imperative compounds) were also detected. Furthermore, protein analysis by FTICR/MS/Orbitrap revealed the presence of 921 proteins belonging to 171 protein groups having 165 unique peptide sequences. The study shows that this morel could be used as a source of bioactive substances to develop anticancer, antifungal, and antiviral drugs in the future. This fruitful addition of M. tridentina in Mycota of Pakistan increases the number of morels to three.
Keywords:
liquid chromatography, mass spectrophotometry metabolites Neelum Valley, proteins, MorchellaReferences
Aydoğmuş-Öztürk, F., Jahan, H., Beyazit, N., Günaydın, K., Choudhary, M.I. (2019). The anticancer activity of visnagin, isolated from Ammi visnaga L., against the human malignant melanoma cell lines, HT 144. Mol. Biol. Rep., 46(2), 1709–1714. https://doi.org/10.1007/s11033-019-04620-1 DOI: https://doi.org/10.1007/s11033-019-04620-1
Badshah, H., Ali, B., Shah, S.A., Alam, M.M., Aly, H.I, Mumtaz, A.S. (2018) First record of Morchella pulchella from Pakistan. Mycotaxon. 133(1), 201–207. https://doi.org/10.5248/133.201 DOI: https://doi.org/10.5248/133.201
Bruns, T.D., White, T.J., Taylor, J.W. (1991). Fungal molecular systematics. Annu. Rev. Ecol. Evol. Syst., 22(1), 525–564. https://doi.org/10.1146/annurev.es.22.110191.002521 DOI: https://doi.org/10.1146/annurev.es.22.110191.002521
Cavalieri, C., Bolzoni, L., Bandini, M. (2010). Nicotine determination in mushrooms by LC–MS/MS with preliminary studies on the impact of drying on nicotine formation. Food Addit. Contam., A, 27(4), 473–477. https://doi.org/10.1080/19440040903479768 DOI: https://doi.org/10.1080/19440040903479768
Chen, B., Yun, M., Li, H., Chen, X., Zhang, C., Wang, H., Deng, Z. (2019). The antioxidant activity and active sites of delphinidin and petunidin measured by DFT, in vitro chemical‐based and cell‐based assays. J. Food Biochem., 43(9), e12968. https://doi.org/10.1111/jfbc.12968 DOI: https://doi.org/10.1111/jfbc.12968
Edgar, R.C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res., 32(5), 1792–1797. https://doi.org/10.1093/nar/gkh340 DOI: https://doi.org/10.1093/nar/gkh340
Gardes, M., White, T.J., Fortin, J.A., Bruns, T.D., Taylor, J.W. (1991). Identification of indigenous and introduced symbiotic fungi in ectomycorrhizae by amplification of nuclear and mitochondrial ribosomal DNA. Can. J. Bot., 69(1), 180–190. https://doi.org/10.1139/b91-026 DOI: https://doi.org/10.1139/b91-026
Hittalmani, S., Mahesh, H.B., Mahadevaiah, C., Prasannakumar, M.K. (2016). De novo genome assembly and annotation of rice sheath rot fungus Sarocladium oryzae reveals genes involved in Helvolic acid and Cerulenin biosynthesis pathways. BMC Genom., 17, 271. https://doi.org/10.1186/s12864-016-2599-0 DOI: https://doi.org/10.1186/s12864-016-2599-0
Jabeen, S. (2016). Ectomycorrhizal fungal communities associated with Himalayan cedar from Pakistan. Doctoral dissertation. University of the Punjab, Lahore. http://173.208.131.244:9060/xmlui/handle/123456789/7646
Kalaras, M.D., Richie, J.P., Calcagnotto, A., Beelman, R.B. (2017). Mushrooms: a rich source of the antioxidants ergothioneine and glutathione. Food Chem. 233, 429–433. https://doi.org/10.1016/j.foodchem.2017.04.109 DOI: https://doi.org/10.1016/j.foodchem.2017.04.109
Kassem, S., Oroszi, T. (2019). Possible therapeutic use of bumetanide in the treatment of autism spectrum disorder. J. Bbiosci. Med., 7(12), 58–67. https://doi.org/10.4236/jbm.2019.712006 DOI: https://doi.org/10.4236/jbm.2019.712006
Kumakura, K., Hori, C., Matsuoka, H., Igarashi, K., Samejima, M. (2019). Protein components of water extracts from fruiting bodies of the reishi mushroom Ganoderma lucidum contribute to the production of functional molecules. J. Sci. Food Agric., 99(2), 529–535. https://doi.org/10.1002/jsfa.9211 DOI: https://doi.org/10.1002/jsfa.9211
Lee, S.R., Roh, H.-S., Lee, S., Park, H.B., Jang, T.S., Ko, Y.-J., Baek K.-H., Kim, K. H. (2018). Bioactivity-guided isolation and chemical characterization of antiproliferative constituents from morel mushroom (Morchella esculenta) in human lung adenocarcinoma cells. J. Funct. Foods, 40, 249–260. https://doi.org/10.1016/j.jff.2017.11.012 DOI: https://doi.org/10.1016/j.jff.2017.11.012
Liu, L., Liang, J., Lu, X., Chen, Z. (2019). Daidzein and its analogues reactivate HIV replication from latently infected CD4 T cells. J. Immunol., 202(1 Suppl.), 197.19. DOI: https://doi.org/10.4049/jimmunol.202.Supp.197.19
Loizides, M., Alvarado, P., Clowez, P., Moreau, P.A., de la Osa, L.R., Palazón, A. (2015). Morchella tridentina, M. rufobrunnea, and M. kakiicolor: a study of three poorly known Mediterranean morels, with nomenclatural updates in section Distances. Mycol. Prog. 14, 1–18. https://doi.org/10.1007/s11557-015-1030-6 DOI: https://doi.org/10.1007/s11557-015-1030-6
Meng, X., Che, C., Zhang, J., Gong, Z., Si, M., Yang, G., Cao, L., Liu, J. (2019). Structural characterization and immunomodulating activities of polysaccharides from a newly collected wild Morchella sextelata. Int. J. Biol. Macromol. 129, 608–614. https://doi.org/10.1016/j.ijbiomac.2019.01.226 DOI: https://doi.org/10.1016/j.ijbiomac.2019.01.226
Moreau, P.-A., Bellanger, J.-M., Clowez, P., Courtecuisse, R., Hansen, K., Knudsen, H., O’Donnell, K., Richard, F. (2014). Proposal to conserve the name Morchella semilibera against Phallus crassipes, P. gigas and P. undosus (Ascomycota). Taxon, 63(3), 677–678. https://doi.org/10.12705/633.20 DOI: https://doi.org/10.12705/633.20
O’Donnell, K., Rooney, A.P., Mills, G.L., Kuo, M., Weber, N.S., Rehner, S.A. (2011). Phylogeny and historical biogeography of true morels (Morchella) reveal an early Cretaceous origin and high continental endemism and provincialism in the Holarctic. Fungal Genet. Biol., 48(3), 252–265. https://doi.org/10.1016/j.fgb.2010.09.006 DOI: https://doi.org/10.1016/j.fgb.2010.09.006
Richard, F., Bellanger, J.-M., Clowez, P., Hansen, K., O’Donnell, K., Urban, A., Sauve, M., Courtecuisse, R., Moreau, P.-A. (2015). True morels (Morchella, Pezizales) of Europe and North America: evolutionary relationships inferred from multilocus data and a unified taxonomy. Mycologia, 107(2), 359–382. https://doi.org/10.3852/14-166 DOI: https://doi.org/10.3852/14-166
Rotzoll, N., Dunkel, A., Hofmann, T. (2005) Activity-guided identification of (S)-malic acid 1-O-d-glucopyranoside (more lid) and γ-aminobutyric acid as contributors to umami taste and mouth-drying oral sensation of morel mushrooms (Morchella deliciosa Fr.). J. Agric. Food Chem. 53(10), 4149–4156. https://doi.org/10.1021/jf050056i DOI: https://doi.org/10.1021/jf050056i
Sherry, S.T., Ward, M.-H., Kholodov, M., Baker, J., Phan, L., Smigielski, E.M., Sirotkin, K. (2001). dbSNP: the NCBI database of genetic variation. Nucleic Acids Res., 29(1), 308–311. https://doi.org/10.1093/nar/29.1.308 DOI: https://doi.org/10.1093/nar/29.1.308
Shivasaraun, U.V., Sureshkumar, R., Karthika, C., Puttappa, N. (2018). Flavonoids as adjuvant in psoralen based photochemotherapy in the management of vitiligo/leucoderma. Med. Hypothes., 121, 26–30. https://doi.org/10.1016/j.mehy.2018.09.011 DOI: https://doi.org/10.1016/j.mehy.2018.09.011
Taofiq, O., Barreiro, M.F., Ferreira, I.C. (2020). Role of bioactive compounds and other metabolites from mushrooms against skin disorders-a systematic review assessing their cosmeceutical and nutricosmetic outcomes. Curr. Med. Chem., 27(41), 6926–6965. https://doi.org/10.2174/0929867327666200402100157 DOI: https://doi.org/10.2174/0929867327666200402100157
Tietel, Z., Masaphy, S. (2018). True morels (Morchella) – nutritional and phytochemical composition, health benefits and flavor: a review. Crit. Rev. Food Sci. Nutr., 58(11), 1888–1901. https://doi.org/10.1080/10408398.2017.1285269 DOI: https://doi.org/10.1080/10408398.2017.1285269
Vieira, V., Fernandes, Â., Barros, L., Glamočlija, J., Ćirić, A., Stojković, D., Ferreira, I.C. (2016). Wild Morchella conica Pers. from different origins: a comparative study of nutritional and bioactive properties. J. Sci. Food Agric., 96(1), 90–98. https://doi.org/10.1002/jsfa.7063 DOI: https://doi.org/10.1002/jsfa.7063
Wagay, J.A., Nayik, G.A., Wani, S.A., Mir, R.A., Ahmad, M.A., Rahman, Q. I., Vyas, D. (2019). Phenolic profiling and antioxidant capacity of Morchella esculenta L. by chemical and electrochemical methods at multiwall carbon nanotube paste electrode. J. Food Meas. Charact., 1–15. https://doi.org/10.1007/s11694-019-00099-3 DOI: https://doi.org/10.1007/s11694-019-00099-3
Wang, J., Xiao, J., Geng, F., Li, X., Yu, J., Zhang, Y., Liu, D. (2019). Metabolic and proteomic analysis of morel fruiting body (Morchella importuna). J. Food Compos. Anal., 76, 51–57. https://doi.org/10.1016/j.jfca.2018.12.006 DOI: https://doi.org/10.1016/j.jfca.2018.12.006
Wang, Z., Ma, H., Smith, K., Wu, S. (2018). Two-dimensional separation using high pH and low pH reversed phase liquid chromatography for top-down proteomics. Int. J. Mass Spectr., 427, 43–51. https://doi.org/10.1016/j.ijms.2017.09.001 DOI: https://doi.org/10.1016/j.ijms.2017.09.001
Xu, Z., Fu, L., Feng, S., Yuan, M., Huang, Y., Liao, J., Ding, C. (2019). Chemical composition, antioxidant and antihyperglycemic activities of the Wild Lactarius deliciosus from China. Molecules, 24(7), 1357. https://doi.org/10.3390/molecules24071357 DOI: https://doi.org/10.3390/molecules24071357
Department of Botany, Women University of Azad Jammu and Kashmir Bagh, Pakistan
Department of Botany, University of Poonch Rawalakot, 12350 Azad Kashmir, Pakistan https://orcid.org/0000-0002-6120-5646
Department of Botany, University of Azad Jammu and Kashmir, Muzaffarabad, Pakistan
Fungal Biology and Systematics Research Laboratory, Institute of Botany, University of the Punjab, Quaid-e-Azam Campus, 54590 Lahore, Pakistan https://orcid.org/0000-0002-3490-058X
Fungal Biology and Systematics Research Laboratory, Institute of Botany, University of the Punjab, Quaid-e-Azam Campus, 54590 Lahore, Pakistan https://orcid.org/0000-0002-5635-8031
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