Epigenetic manipulation for secondary metabolite activation in endophytic fungi: current progress and future directions

References

• Abdulla A, Zhao X, Yang F. 2013. Natural polyphenols inhibit lysine-specific demethylase-1 in vitro. J Biochem Pharmacol Res. 1(1):56.
   PubMedGoogle Scholar
• Aghcheh RK, Kubicek CP. 2015. Epigenetics as an emerging tool for improvement of fungal strains used in biotechnology. Appl Microbiol Biotechnol. 99(15):6167–6181. doi: 10.1007/s00253-015-6763-2.
   PubMed Web of Science ®Google Scholar
• Ahn HJ, Kim YS, Kim JU, Han SM, Shin JW, Yang HO. 2004. Mechanism of taxol‐induced apoptosis in human SKOV3 ovarian carcinoma cells. J Cell Biochem. 91(5):1043–1052. doi: 10.1002/jcb.20006.
   PubMed Web of Science ®Google Scholar
• Akone SH, Mándi A, Kurtán T, Hartmann R, Lin W, Daletos G, Proksch P. 2016. Inducing secondary metabolite production by the endophytic fungus Chaetomium sp. through fungal–bacterial co-culture and epigenetic modification. Tetrahedron. 72(41):6340–6347. doi: 10.1016/j.tet.2016.08.022.
   Web of Science ®Google Scholar
• Akone SH, Pham C-D, Chen H, Ola ARB, Ntie-Kang F, Proksch P. 2019. Epigenetic modification, co-culture and genomic methods for natural product discovery. Phys Sci Rev. 4(4):20180118. doi: 10.1515/psr-2018-0118.
   Web of Science ®Google Scholar
• Aldholmi M, Wilkinson B, Ganesan A. 2020. Epigenetic modulation of secondary metabolite profiles in Aspergillus calidoustus and Aspergillus westerdijkiae through histone deacetylase (HDAC) inhibition by vorinostat. J Antibiot (Tokyo). 73(6):410–413. doi: 10.1038/s41429-020-0286-5.
   PubMed Web of Science ®Google Scholar
• Aramayo R, Selker EU. 2013. Neurospora crassa, a model system for epigenetics research. Cold Spring Harb Perspect Biol. 5(10):a017921. doi: 10.1101/cshperspect.a017921.
   PubMed Web of Science ®Google Scholar
• Armeev GA, Gribkova AK, Pospelova I, Komarova GA, Shaytan AK. 2019. Linking chromatin composition and structural dynamics at the nucleosome level. Curr Opin Struct Biol. 56:46–55. doi:10.1016/j.sbi.2018.11.006.
   PubMed Web of Science ®Google Scholar
• Asai T, Otsuki S, Sakurai H, Yamashita K, Ozeki T, Oshima Y. 2013. Benzophenones from an endophytic fungus, Graphiopsis chlorocephala, from Paeonia lactiflora cultivated in the presence of an NAD±dependent HDAC inhibitor. Org Lett. 15(8):2058–2061. doi: 10.1021/ol400781b.
   PubMed Web of Science ®Google Scholar
• Barik S, Rai N, Mishra P, Singh SK, Gautam V. 2020. Bioinformatics: how it helps to boost modern biological research. Curr Sci. 118:698–699.
   Web of Science ®Google Scholar
• Baron NC, Rigobelo EC. 2022. Endophytic fungi: a tool for plant growth promotion and sustainable agriculture. Mycol. 13(1):39–55. doi: 10.1080/21501203.2021.1945699.
   PubMedGoogle Scholar
• Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science. 315(5819):1709–1712. doi: 10.1126/science.1138140.
   PubMed Web of Science ®Google Scholar
• Beau J, Mahid N, Burda WN, Harrington L, Shaw LN, Mutka T, Kyle DE, Barisic B, Van Olphen A, Baker BJ. 2012. Epigenetic tailoring for the production of anti-infective cytosporones from the marine fungus Leucostoma persoonii. Mar Drugs. 10(4):762–774. doi: 10.3390/md10040762.
   PubMed Web of Science ®Google Scholar
• Boedi S, Reyes-Dominguez Y, Strauss J. 2012. Chromatin immunoprecipitation analysis in filamentous fungi. Fungal Secondary Metab Methods Protoc. 944:221–236. doi: 10.1007/978-1-62703-122-6_16.
   Google Scholar
• Bok JW, Chiang YM, Szewczyk E, Reyes-Dominguez Y, Davidson AD, Sanchez JF, Lo H-C, Watanabe K, Strauss J, Oakley BR. 2009. Chromatin-level regulation of biosynthetic gene clusters. Nat Chem Biol. 5(7):462–464. doi: 10.1038/nchembio.177.
   PubMed Web of Science ®Google Scholar
• Bono JM, Olesnicky EC, Matzkin LM. 2015. Connecting genotypes, phenotypes and fitness: harnessing the power of CRISPR/Cas9 genome editing. Mol Ecol. 24(15):3810–3822. doi: 10.1111/mec.13252.
   PubMed Web of Science ®Google Scholar
• Brakebusch C. 2021. CRISPR genome editing: how to make a fantastic method even better. Cells MDPI. 10(2):408. doi: 10.3390/cells10020408.
   PubMed Web of Science ®Google Scholar
• Brakhage AA. 2013. Regulation of fungal secondary metabolism. Nat Rev Microbiol. 11(1):21–32. doi: 10.1038/nrmicro2916.
   PubMed Web of Science ®Google Scholar
• Brakhage AA, Schroeckh V. 2011. Fungal secondary metabolites–strategies to activate silent gene clusters. Fungal Genet Biol. 48(1):15–22. doi: 10.1016/j.fgb.2010.04.004.
   PubMed Web of Science ®Google Scholar
• Bumpus SB, Evans BS, Thomas PM, Ntai I, Kelleher NL. 2009. A proteomics approach to discovering natural products and their biosynthetic pathways. Nat Biotechnol. 27(10):951–956. doi: 10.1038/nbt.1565.
   PubMed Web of Science ®Google Scholar
• Candido EPM, Reeves R, Davie JR. 1978. Sodium butyrate inhibits histone deacetylation in cultured cells. Cell. 14(1):105–113. doi: 10.1016/0092-8674(78)90305-7.
   PubMed Web of Science ®Google Scholar
• Chen HJ, Awakawa T, Sun JY, Wakimoto T, Abe I. 2013. Epigenetic modifier-induced biosynthesis of novel fusaric acid derivatives in endophytic fungi from Datura stramonium L. Nat Prod Bioprospect. 3(1):20–23. doi: 10.1007/s13659-013-0010-2.
   Google Scholar
• Chujo T, Scott B. 2014. Histone H 3 K 9 and H 3 K 27 methylation regulates fungal alkaloid biosynthesis in a fungal endophyte–plant symbiosis. Mol Microbiol. 92(2):413–434. doi: 10.1111/mmi.12567.
   PubMed Web of Science ®Google Scholar
• Cichewicz RH. 2010. Epigenome manipulation as a pathway to new natural product scaffolds and their congeners. Nat Prod Rep. 27(1):11–22. doi: 10.1039/B920860G.
   PubMed Web of Science ®Google Scholar
• Collemare J, Seidl MF. 2019. Chromatin-dependent regulation of secondary metabolite biosynthesis in fungi: is the picture complete? FEMS Microbiol Rev. 43(6):591–607. doi: 10.1093/femsre/fuz018.
   PubMed Web of Science ®Google Scholar
• Conway KR, Boddy CN. 2012. ClusterMine360: a database of microbial PKS/NRPS biosynthesis. Nucleic Acids Res. 41(D1):D402–D407. doi: 10.1093/nar/gks993.
   PubMed Web of Science ®Google Scholar
• Davie JR. 2003. Inhibition of histone deacetylase activity by butyrate. J Nutr. 133(7):2485S–2493S. doi: 10.1093/jn/133.7.2485S.
   PubMed Web of Science ®Google Scholar
• Dwibedi V, Kalia S, Saxena S. 2019. Isolation and enhancement of resveratrol production in Xylaria psidii by exploring the phenomenon of epigenetics: using DNA methyltransferases and histone deacetylase as epigenetic modifiers. Mol Biol Rep. 46(4):4123–4137. doi: 10.1007/s11033-019-04862-z.
   PubMed Web of Science ®Google Scholar
• Ehrenhofer‐Murray AE. 2004. Chromatin dynamics at DNA replication, transcription and repair. European J Mol Biol Biochem. 271(12):2335–2349. doi: 10.1111/j.1432-1033.2004.04162.x.
   Google Scholar
• Feng T, Wei C, Deng X, Chen D, Wen Z, Xu J. 2022. Epigenetic manipulation induced production of immunosuppressive chromones and cytochalasins from the mangrove endophytic fungus Phomopsis asparagi DHS-48. Mar Drugs. 20(10):616. doi: 10.3390/md20100616.
   PubMed Web of Science ®Google Scholar
• Fisch K, Gillaspy A, Gipson M, Henrikson J, Hoover A, Jackson L, Najar F, Wägele H, Cichewicz R. 2009. Chemical induction of silent biosynthetic pathway transcription in Aspergillus niger. J Ind Microbiol Biotechnol. 36(9):1199–1213. doi: 10.1007/s10295-009-0601-4.
   PubMed Web of Science ®Google Scholar
• Forseth RR, Fox EM, Chung D, Howlett BJ, Keller NP, Schroeder FC. 2011. Identification of cryptic products of the gliotoxin gene cluster using NMR-based comparative metabolomics and a model for gliotoxin biosynthesis. J Am Chem Soc. 133(25):9678–9681. doi: 10.1021/ja2029987.
   PubMed Web of Science ®Google Scholar
• Gacek-Matthews A, Berger H, Sasaki T, Wittstein K, Gruber C, Lewis ZA, Strauss J. 2016. KdmB, a Jumonji histone H3 demethylase, regulates genome-wide H3K4 trimethylation and is required for normal induction of secondary metabolism in Aspergillus nidulans. PLoS Genet. 12(8):e1006222. doi: 10.1371/journal.pgen.1006222.
   PubMed Web of Science ®Google Scholar
• Gacek-Matthews A, Noble LM, Gruber C, Berger H, Sulyok M, Marcos AT, Strauss J, Andrianopoulos A. 2015. KdmA, a histone H3 demethylase with bipartite function, differentially regulates primary and secondary metabolism in Aspergillus nidulans. Mol Microbiol. 97(3):606. doi: 10.1111/mmi.12977.
   PubMed Web of Science ®Google Scholar
• Gasiunas G, Barrangou R, Horvath P, Siksnys V. 2012. Cas9–crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci. 109(39):E2579–E2586. doi: 10.1073/pnas.1208507109.
   PubMed Web of Science ®Google Scholar
• Gautam VS, Singh A, Kumari P, Nishad JH, Kumar J, Yadav M, Bharti R, Prajapati P, Kharwar RN. 2022. Phenolic and flavonoid contents and antioxidant activity of an endophytic fungus Nigrospora sphaerica (EHL2), inhabiting the medicinal plant Euphorbia hirta (dudhi) L. Arch Microbiol. 204(2):140. doi: 10.1007/s00203-021-02650-7.
   PubMed Web of Science ®Google Scholar
• Gehm BD, McAndrews JM, Chien PY, Jameson JL. 1997. Resveratrol, a polyphenolic compound found in grapes and wine, is an agonist for the estrogen receptor. Proc Natl Acad Sci. 94(25):14138–14143. doi: 10.1073/pnas.94.25.14138.
   PubMed Web of Science ®Google Scholar
• Gnyszka A, Jastrzębski Z, Flis S. 2013. DNA methyltransferase inhibitors and their emerging role in epigenetic therapy of cancer. Anticancer Res. 33(8):2989–2996.
   PubMed Web of Science ®Google Scholar
• González-Menéndez V, Crespo G, Toro C, Martín J, de Pedro N, Tormo JR, Genilloud O. 2019. Extending the metabolite diversity of the endophyte Dimorphosporicola tragani. Metabolites. 9(10):197. doi: 10.3390/metabo9100197.
   PubMed Web of Science ®Google Scholar
• Gubiani JR, Wijeratne EK, Shi T, Araujo AR, Arnold AE, Chapman E, Gunatilaka AL. 2017. An epigenetic modifier induces production of (10′ S)-verruculide B, an inhibitor of protein tyrosine phosphatases by Phoma sp. nov. LG0217, a fungal endophyte of Parkinsonia microphylla. Bioorg Med Chem. 25(6):1860–1866. doi: 10.1016/j.bmc.2017.01.048.
   PubMed Web of Science ®Google Scholar
• Gulyamova T, Abdulmyanova L, Ruzieva D, Rasulova G, Yusupov U, Sattarova R. 2019. Effect of epigenetic modifiers on fermentation parameters of endophytic fungi from plants growing in Uzbekistan. Int J Curr Microbiol Appl Sci. 8(3):851–860. doi: 10.20546/ijcmas.2019.803.102.
   Google Scholar
• Guo DL, Qiu L, Feng D, He X, Li XH, Cao ZX, Gu YC, Mei L, Deng F, Deng Y. 2020. Three new ɑ-pyrone derivatives induced by chemical epigenetic manipulation of Penicillium herquei, an endophytic fungus isolated from Cordyceps sinensis. Nat Prod Res. 34(7):958–964. doi: 10.1080/14786419.2018.1544974.
   PubMed Web of Science ®Google Scholar
• Gupta S, Chaturvedi P, Kulkarni MG, Staden JJBA V. 2020. A critical review on exploiting the pharmaceutical potential of plant endophytic fungi. Biotechnol Adv. 39:107462. doi:10.1016/j.biotechadv.2019.107462.
   PubMed Web of Science ®Google Scholar
• Gupta P, Verma A, Rai N, Singh AK, Singh SK, Kumar B, Kumar R, Gautam V. 2021. Mass spectrometry-based technology and workflows for studying the chemistry of fungal endophyte derived bioactive compounds. ACS Chem Biol. 16(11):2068–2086. doi: 10.1021/acschembio.1c00581.
   PubMed Web of Science ®Google Scholar
• Hardy TM, Tollefsbol TO. 2011. Epigenetic diet: impact on the epigenome and cancer. Epigenomics. 3(4):503–518. doi: 10.2217/epi.11.71.
   PubMed Web of Science ®Google Scholar
• Helaly SE, Thongbai B, Stadler M. 2018. Diversity of biologically active secondary metabolites from endophytic and saprotrophic fungi of the ascomycete order Xylariales. Nat Prod Rep. 35(9):992–1014. doi: 10.1039/C8NP00010G.
   PubMed Web of Science ®Google Scholar
• Hoffmeister D, Keller NP. 2007. Natural products of filamentous fungi: enzymes, genes, and their regulation. Nat Prod Rep. 24(2):393–416. doi: 10.1039/B603084J.
   PubMed Web of Science ®Google Scholar
• Huang PW, Yang Q, Zhu YL, Zhou J, Sun K, Mei YZ, Dai CC. 2020. The construction of CRISPR-Cas9 system for endophytic Phomopsis liquidambaris and its PmkkA-deficient mutant revealing the effect on rice. Fungal Genet Biol. 136:103301. doi: 10.1016/j.fgb.2019.103301.
   PubMed Web of Science ®Google Scholar
• Iyer LM, Zhang D, Aravind L. 2016. Adenine methylation in eukaryotes: apprehending the complex evolutionary history and functional potential of an epigenetic modification. Bioessays. 38(1):27–40. doi: 10.1002/bies.201500104.
   PubMed Web of Science ®Google Scholar
• Jiang Y, Wang Y, Brudno M. 2012. PRISM: pair-read informed split-read mapping for base-pair level detection of insertion, deletion and structural variants. Bioinformatics. 28(20):2576–2583. doi: 10.1093/bioinformatics/bts484.
   PubMed Web of Science ®Google Scholar
• Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012. A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science. 337(6096):816–821. doi: 10.1126/science.1225829.
   PubMed Web of Science ®Google Scholar
• Jourquin F, Géli V. 2017. Histone purification from Saccharomyces cerevisiae. In: Guillemette B Gaudreau L, editors. Histones, methods in molecular biology. Vol. 1528. New York: Humana Press; p. 69–73.
   Google Scholar
• Keller NP. 2019. Fungal secondary metabolism: regulation, function and drug discovery. Nat Rev Microbiol. 17(3):167–180. doi: 10.1038/s41579-018-0121-1.
   PubMed Web of Science ®Google Scholar
• Keller NP, Turner G, Bennett JW. 2005. Fungal secondary metabolism—from biochemistry to genomics. Nat Rev Microbiol. 3(12):937–947. doi: 10.1038/nrmicro1286.
   PubMed Web of Science ®Google Scholar
• Keshri PK, Rai N, Verma A, Kamble SC, Barik S, Mishra P, Singh SK, Salvi P, Gautam V. 2021. Biological potential of bioactive metabolites derived from fungal endophytes associated with medicinal plants. Mycol Prog. 20(5):577–594. doi: 10.1007/s11557-021-01695-8.
   Web of Science ®Google Scholar
• Khaldi N, Seifuddin FT, Turner G, Haft D, Nierman WC, Wolfe KH, Fedorova ND. 2010. SMURF: genomic mapping of fungal secondary metabolite clusters. Fungal Genet Biol. 47(9):736–741. doi: 10.1016/j.fgb.2010.06.003.
   PubMed Web of Science ®Google Scholar
• Kim HJ, Bae SC. 2011. Histone deacetylase inhibitors: molecular mechanisms of action and clinical trials as anti-cancer drugs. Am J Transl Res. 3(2):166.
   PubMed Web of Science ®Google Scholar
• Knott GJ, Doudna JA. 2018. CRISPR-Cas guides the future of genetic engineering. Science. 361(6405):866–869. doi: 10.1126/science.aat5011.
   PubMed Web of Science ®Google Scholar
• Krautkramer KA, Reiter L, Denu JM, Dowell JA. 2015. Quantification of SAHA-dependent changes in histone modifications using data-independent acquisition mass spectrometry. Proteome Res. 14(8):3252–3262. doi: 10.1021/acs.jproteome.5b00245.
   PubMed Web of Science ®Google Scholar
• Kumar S, Chinnusamy V, Mohapatra T. 2018. Epigenetics of modified DNA bases: 5-methylcytosine and beyond. Front Genet. 9:640. doi:10.3389/fgene.2018.00640.
   PubMed Web of Science ®Google Scholar
• Li G, Kusari S, Golz C, Laatsch H, Strohmann C, Spiteller M. 2017. Epigenetic modulation of endophytic Eupenicillium sp. LG41 by a histone deacetylase inhibitor for production of decalin-containing compounds. J Nat Prod. 80(4):983–988. doi: 10.1021/acs.jnatprod.6b00997.
   PubMed Web of Science ®Google Scholar
• Liu R, Chen L, Jiang Y, Zhou Z, Zou G. 2015. Efficient genome editing in filamentous fungus Trichoderma reesei using the CRISPR/Cas9 system. Cell Discov. 1(1):1–11. doi: 10.1038/celldisc.2015.7.
   Google Scholar
• Lopes A, da Silva D, Lopes N, Pupo M. 2012. Epigenetic modulation changed the secondary metabolite profile in the endophyte Nigrospora sphaerica SS67. Planta Med. 78(14):L38. doi: 10.1055/s-0032-1325180.
   Google Scholar
• Magotra A, Kumar M, Kushwaha M, Awasthi P, Raina C, Gupta AP, Shah BA, Gandhi SG, Chaubey A. 2017. Epigenetic modifier induced enhancement of fumiquinazoline C production in Aspergillus fumigatus (GA-L7): an endophytic fungus from Grewia asiatica L. AMB Express. 7(1):1–10. doi: 10.1186/s13568-017-0343-z.
   PubMedGoogle Scholar
• Makarova KS, Wolf YI, Iranzo J, Shmakov SA, Alkhnbashi OS, Brouns SJ, Charpentier E, Cheng D, Haft DH, Horvath P. 2020. Evolutionary classification of CRISPR–Cas systems: a burst of class 2 and derived variants. Nat Rev Microbiol. 18(2):67–83. doi: 10.1038/s41579-019-0299-x.
   PubMed Web of Science ®Google Scholar
• Mao XM, Xu W, Li D, Yin WB, Chooi YH, Li YQ, Tang Y, Hu Y. 2015. Epigenetic genome mining of an endophytic fungus leads to the pleiotropic biosynthesis of natural products. Angew Chem. 127(26):7702–7706. doi: 10.1002/ange.201502452.
   Google Scholar
• Marks PA, Breslow R. 2007. Dimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug. Nat Biotechnol. 25(1):84–90. doi: 10.1038/nbt1272.
   PubMed Web of Science ®Google Scholar
• Marmann A, Aly AH, Lin W, Wang B, Proksch P. 2014. Co-cultivation—a powerful emerging tool for enhancing the chemical diversity of microorganisms. Mar Drugs. 12(2):1043–1065. doi: 10.3390/md12021043.
   PubMed Web of Science ®Google Scholar
• Matsu-Ura T, Baek M, Kwon J, Hong C. 2015. Efficient gene editing in Neurospora crassa with CRISPR technology. Fungal Biol Biotechnol. 2(1):1–7. doi: 10.1186/s40694-015-0015-1.
   PubMedGoogle Scholar
• Meeran SM, Ahmed A, Tollefsbol TO. 2010. Epigenetic targets of bioactive dietary components for cancer prevention and therapy. Clin Epigenetics. 1(3):101–116. doi: 10.1007/s13148-010-0011-5.
   PubMedGoogle Scholar
• Meier JL, Niessen S, Hoover HS, Foley TL, Cravatt BF, Burkart MD. 2009. An orthogonal active site identification system (OASIS) for proteomic profiling of natural product biosynthesis. ACS Chem Biol. 4(11):948–957. doi: 10.1021/cb9002128.
   PubMed Web of Science ®Google Scholar
• Mousa WK, Raizada MN. 2013. The diversity of anti-microbial secondary metabolites produced by fungal endophytes: an interdisciplinary perspective. Front Microbiol. 4:65. doi:10.3389/fmicb.2013.00065.
   PubMed Web of Science ®Google Scholar
• Nierman WC, Pain A, Anderson MJ, Wortman JR, Kim HS, Arroyo J, Berriman M, Abe K, Archer DB, Bermejo C. 2005. Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature. 438(7071):1151–1156. doi: 10.1038/nature04332.
   PubMed Web of Science ®Google Scholar
• Nishad JH, Singh A, Gautam VS, Kumari P, Kumar J, Yadav M, Kharwar RN. 2021. Bioactive potential evaluation and purification of compounds from an endophytic fungus Diaporthe longicolla, a resident of Saraca asoca (Roxb.) Willd. Arch Microbiol. 203(7):4179–4188. doi: 10.1007/s00203-021-02390-8.
   PubMed Web of Science ®Google Scholar
• Orlando V. 2000. Mapping chromosomal proteins in vivo by formaldehyde-crosslinked-chromatin immunoprecipitation. Trends Biochem Sci. 25(3):99–104. doi: 10.1016/S0968-0004(99)01535-2.
   PubMed Web of Science ®Google Scholar
• Osbourn A. 2010. Secondary metabolic gene clusters: evolutionary toolkits for chemical innovation. Trends Genet. 26(10):449–457. doi: 10.1016/j.tig.2010.07.001.
   PubMed Web of Science ®Google Scholar
• Papoutsis AJ, Lamore SD, Wondrak GT, Selmin OI, Romagnolo DF. 2010. Resveratrol prevents epigenetic silencing of BRCA-1 by the aromatic hydrocarbon receptor in human breast cancer cells. J Nutr. 140(9):1607–1614. doi: 10.3945/jn.110.123422.
   PubMed Web of Science ®Google Scholar
• Park PJ. 2009. ChIP–seq: advantages and challenges of a maturing technology. Nat Rev Genet. 10(10):669–680. doi: 10.1038/nrg2641.
   PubMed Web of Science ®Google Scholar
• Pfannenstiel BT, Greco C, Sukowaty AT, Keller NP. 2018. The epigenetic reader SntB regulates secondary metabolism, development and global histone modifications in Aspergillus flavus. Fungal Genet. 120:9–18. doi: 10.1016/j.fgb.2018.08.004.
   PubMed Web of Science ®Google Scholar
• Poças-Fonseca MJ, Cabral CG, Manfrão-Netto JHC. 2020. Epigenetic manipulation of filamentous fungi for biotechnological applications: a systematic review. Biotechnol Lett. 42(6):885–904. doi: 10.1007/s10529-020-02871-8.
   PubMed Web of Science ®Google Scholar
• Pohl C, Kiel JA, Driessen AJ, Bovenberg RA, Nygard Y. 2016. CRISPR/Cas9 based genome editing of Penicillium chrysogenum. ACS Synth Biol. 5(7):754–764. doi: 10.1021/acssynbio.6b00082.
   PubMed Web of Science ®Google Scholar
• Qu X, Lei C, Liu W. 2011. Transcriptome mining of active biosynthetic pathways and their associated products in Streptomyces flaveolus. Angew Chem Int Ed. 50(41):9651–9654. doi: 10.1002/anie.201103085.
   PubMed Web of Science ®Google Scholar
• Rai N, Gupta P, Keshri PK, Verma A, Mishra P, Kumar D, Kumar A, Singh SK, Gautam V. 2022. Fungal endophytes: an accessible source of bioactive compounds with potential anticancer activity. Appl Biochem Biotechnol. 194(7):3296–3319. doi: 10.1007/s12010-022-03872-1.
   PubMed Web of Science ®Google Scholar
• Rai N, Keshri PK, Verma A, Kamble SC, Mishra P, Barik S, Kumar Singh S, Gautam V. 2021. Plant associated fungal endophytes as a source of natural bioactive compounds. Mycology. 12(3):139–159. doi: 10.1080/21501203.2020.1870579.
   PubMedGoogle Scholar
• Raimi A, Adeleke R. 2021. Bioprospecting of endophytic microorganisms for bioactive compounds of therapeutic importance. Arch Microbiol. 203(5):1917–1942. doi: 10.1007/s00203-021-02256-z.
   PubMed Web of Science ®Google Scholar
• Reddy BVB, Milshteyn A, Charlop-Powers Z, Brady SF. 2014. eSnapd: a versatile, web-based bioinformatics platform for surveying and mining natural product biosynthetic diversity from metagenomes. Chem Biol. 21(8):1023–1033. doi: 10.1016/j.chembiol.2014.06.007.
   PubMedGoogle Scholar
• Rokas A, Mead ME, Steenwyk JL, Raja HA, Oberlies NH. 2020. Biosynthetic gene clusters and the evolution of fungal chemodiversity. Nat Prod Rep. 37(7):868–878. doi: 10.1039/C9NP00045C.
   PubMed Web of Science ®Google Scholar
• Rutledge PJ, Challis GL. 2015. Discovery of microbial natural products by activation of silent biosynthetic gene clusters. Nat Rev Microbiol. 13(8):509–523. doi: 10.1038/nrmicro3496.
   PubMed Web of Science ®Google Scholar
• Sagita R, Quax WJ, Haslinger K. 2021. Current state and future directions of genetics and genomics of endophytic fungi for bioprospecting efforts. Front Bioeng Biotechnol. 9:649906. doi:10.3389/fbioe.2021.649906.
   PubMed Web of Science ®Google Scholar
• Salvi P, Mahawar H, Agarrwal R, Gautam V, Deshmukh R. 2022. Advancement in the molecular perspective of plant-endophytic interaction to mitigate drought stress in plants. Front Microbiol. 13:981355. doi:10.3389/fmicb.2022.981355.
   PubMed Web of Science ®Google Scholar
• Santi DV, Norment A, Garrett CE. 1984. Covalent bond formation between a DNA-cytosine methyltransferase and DNA containing 5-azacytosine. Proc Natl Acad Sci. 81(22):6993–6997. doi: 10.1073/pnas.81.22.6993.
   PubMed Web of Science ®Google Scholar
• Sarma H, Islam N, Prasad R, Prasad M, Ma LQ, Rinklebe J. 2021. Enhancing phytoremediation of hazardous metal (loid) s using genome engineering CRISPR–Cas9 technology. J Hazard Mater. 414:125493. doi:10.1016/j.jhazmat.2021.125493.
   PubMed Web of Science ®Google Scholar
• Schley C, Altmeyer MO, Swart R, Müller R, Huber CG. 2006. Proteome analysis of Myxococcus x anthus by off-line two-dimensional chromatographic separation using monolithic poly-(styrene-divinylbenzene) columns combined with ion-trap tandem mass spectrometry. J Proteome Res. 5(10):2760–2768. doi: 10.1021/pr0602489.
   PubMed Web of Science ®Google Scholar
• Schüller A, Wolansky L, Berger H, Studt L, Gacek-Matthews A, Sulyok M, Strauss J. 2020. A novel fungal gene regulation system based on inducible VPR-dCas9 and nucleosome map-guided sgRNA positioning. Appl Microbiol Biotechnol. 104(22):9801–9822. doi: 10.1007/s00253-020-10900-9.
   PubMed Web of Science ®Google Scholar
• Seto E, Yoshida M. 2014. Erasers of histone acetylation: the histone deacetylase enzymes. Cold Spring Harb Perspect Biol. 6(4):a018713. doi: 10.1101/cshperspect.a018713.
   PubMed Web of Science ®Google Scholar
• Seyedsayamdost MR. 2014. High-throughput platform for the discovery of elicitors of silent bacterial gene clusters. Proc Natl Acad Sci. 111(20):7266–7271. doi: 10.1073/pnas.1400019111.
   PubMed Web of Science ®Google Scholar
• Sharma VK, Kumar J, Singh DK, Mishra A, Verma SK, Gond SK, Kumar A, Singh N, Kharwar RN. 2017. Induction of cryptic and bioactive metabolites through natural dietary components in an endophytic fungus Colletotrichum gloeosporioides (Penz.) Sacc. Front Microbiol. 8:1126. doi:10.3389/fmicb.2017.01126.
   PubMed Web of Science ®Google Scholar
• Shwab EK, Bok JW, Tribus M, Galehr J, Graessle S, Keller NP. 2007. Histone deacetylase activity regulates chemical diversity in Aspergillus. Eukaryot Cell. 6(9):1656–1664. doi: 10.1128/ec.00186-07.
   PubMedGoogle Scholar
• Singh A, Singh DK, Kharwar RN, White JF, Gond SK. 2021. Fungal endophytes as efficient sources of plant-derived bioactive compounds and their prospective applications in natural product drug discovery: Insights, avenues, and challenges. Microorganisms. 9(1):197. doi: 10.3390/microorganisms9010197.
   PubMed Web of Science ®Google Scholar
• Soukup A, Keller NP. 2013. Western analysis of histone modifications (Aspergillus nidulans). Bio-protocol. 3(7):e424–e424. doi: 10.21769/BioProtoc.424.
   PubMedGoogle Scholar
• Srinivasa C, Mellappa G, Patil SM, Ramu R, Shreevatsa B, Dharmashekar C, Kollur SP, Syed A, Shivamallu C. 2022. Plants and endophytes - a partnership for the coumarin production through the microbial systems. Mycology. 13(4):243–256. doi: 10.1080/21501203.2022.2027537.
   PubMedGoogle Scholar
• Sterner DE, Berger SL. 2000. Acetylation of histones and transcription-related factors. Microbiol Mol Biol Rev. 64(2):435–459. doi: 10.1128/mmbr.64.2.435-459.2000.
   PubMed Web of Science ®Google Scholar
• Stierle A, Strobel G, Stierle D. 1993. Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of Pacific yew. Science. 260(5105):214–216. doi: 10.1126/science.8097061.
   PubMed Web of Science ®Google Scholar
• Strahl BD, Allis CD. 2000. The language of covalent histone modifications. Nature. 403(6765):41–45. doi: 10.1038/47412.
   PubMed Web of Science ®Google Scholar
• Strobel GA. 2002. Rainforest endophytes and bioactive products. Crit Rev Biotechnol. 22(4):315–333. doi: 10.1080/07388550290789531.
   PubMed Web of Science ®Google Scholar
• Sun J, Awakawa T, Noguchi H, Abe I. 2012. Induced production of mycotoxins in an endophytic fungus from the medicinal plant Datura stramonium L. Bioorganic Med Chem Lett. 22(20):6397–6400. doi: 10.1016/j.bmcl.2012.08.063.
   PubMed Web of Science ®Google Scholar
• Suryanarayanan T, Thirunavukkarasu N, Govindarajulu M, Sasse F, Jansen R, Murali T. 2009. Fungal endophytes and bioprospecting. Fungal Biol Rev. 23(1–2):9–19. doi: 10.1016/j.fbr.2009.07.001.
   Google Scholar
• Swartjes T, Staals RH, van der Oost J. 2020. Editor’s cut: DNA cleavage by CRISPR RNA-guided nucleases Cas9 and Cas12a. Biochem Soc Trans. 48(1):207–219. doi: 10.1042/BST20190563.
   PubMed Web of Science ®Google Scholar
• Taiwo O, Wilson GA, Morris T, Seisenberger S, Reik W, Pearce D, Beck S, Butcher LM. 2012. Methylome analysis using MeDIP-seq with low DNA concentrations. Nat Protoc. 7(4):617–636. doi: 10.1038/nprot.2012.012.
   PubMed Web of Science ®Google Scholar
• Tiwari P, Bae H. 2022. Endophytic fungi: key insights, emerging prospects, and challenges in natural product drug discovery. Microorganisms. 10(2):360. doi: 10.3390/microorganisms10020360.
   PubMed Web of Science ®Google Scholar
• Toghueo K, Dinkar S, Boyom F. 2016. Stimulation of the production of new volatile and non-volatile metabolites by endophytic Aspergillus niger using small organic chemicals. Curr Res Environ Appl Mycol. 6(4):256–267. doi: 10.5943/cream/6/4/3.
   Google Scholar
• Toghueo RMK, Sahal D, Boyom FF. 2020. Recent advances in inducing endophytic fungal specialized metabolites using small molecule elicitors including epigenetic modifiers. Phytochemistry. 174:112338. doi: 10.1016/j.phytochem.2020.112338.
   PubMed Web of Science ®Google Scholar
• Udwary DW, Gontang EA, Jones AC, Jones CS, Schultz AW, Winter JM, Yang JY, Beauchemin N, Capson TL, Clark BR. 2011. Significant natural product biosynthetic potential of actinorhizal symbionts of the genus Frankia, as revealed by comparative genomic and proteomic analyses. Appl Environ Microbiol. 77(11):3617–3625. doi: 10.1128/AEM.00038-11.
   PubMed Web of Science ®Google Scholar
• Ul-Hassan SR, Strobel GA, Booth E, Knighton WB, Floerchinger C, Sears J. 2012. Modulation of volatile organic compound formation in the Mycodiesel-producing endophyte Hypoxylon sp. CI-4. Microbiology. 158(2):465–473. doi: 10.1099/mic.0.054643-0.
   PubMedGoogle Scholar
• Uzma F, Mohan CD, Hashem A, Konappa NM, Rangappa S, Kamath PV, Singh BP, Mudili V, Gupta VK, Siddaiah CN. 2018. Endophytic fungi—alternative sources of cytotoxic compounds: A review. Front Pharmacol. 9:309. doi:10.3389/fphar.2018.00309.
   PubMed Web of Science ®Google Scholar
• VanderMolen KM, Darveaux BA, Chen W-L, Swanson SM, Pearce CJ, Oberlies NH. 2014. Epigenetic manipulation of a filamentous fungus by the proteasome-inhibitor bortezomib induces the production of an additional secondary metabolite. RSC Adv. 4(35):18329–18335. doi: 10.1039/C4RA00274A.
   PubMed Web of Science ®Google Scholar
• Vel Szic KS, Ndlovu MN, Haegeman G, Berghe WV. 2010. Nature or nurture: let food be your epigenetic medicine in chronic inflammatory disorders. Biochem Pharmacol. 80(12):1816–1832. doi: 10.1016/j.bcp.2010.07.029.
   PubMed Web of Science ®Google Scholar
• Wang D, Jin S, Lu Q, Chen Y. 2023. Advances and challenges in CRISPR/Cas-based fungal genome engineering for secondary metabolite production: A review. J Fungi. 9(3):362. doi: 10.3390/jof9030362.
   Web of Science ®Google Scholar
• Wang Q, Cobine PA, Coleman JJ. 2018. Efficient genome editing in Fusarium oxysporum based on CRISPR/Cas9 ribonucleoprotein complexes. Fungal Genet Biol. 117:21–29. doi:10.1016/j.fgb.2018.05.003.
   PubMed Web of Science ®Google Scholar
• Weber T, Blin K, Duddela S, Krug D, Kim HU, Bruccoleri R, Lee SY, Fischbach MA, Müller R, Wohlleben W. 2015. antiSMASH 3.0—a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res. 43(W1):W237–W243. doi: 10.1093/nar/gkv437.
   PubMed Web of Science ®Google Scholar
• Wenderoth M, Pinecker C, Voß B, Fischer R. 2017. Establishment of CRISPR/Cas9 in Alternaria alternata. Fungal Genet Biol. 101:55–60. doi:10.1016/j.fgb.2017.03.001.
   PubMed Web of Science ®Google Scholar
• Williams RB, Henrikson JC, Hoover AR, Lee AE, Cichewicz RH. 2008. Epigenetic remodeling of the fungal secondary metabolome. Org Biomol Chem. 6(11):1895–1897. doi: 10.1039/B804701D.
   PubMed Web of Science ®Google Scholar
• Wu G, Zhou H, Zhang P, Wang X, Li W, Zhang W, Liu X, Liu HW, Keller NP, An Z. 2016. Polyketide production of pestaloficiols and macrodiolide ficiolides revealed by manipulations of epigenetic regulators in an endophytic fungus. Org Lett. 18(8):1832–1835. doi: 10.1021/acs.orglett.6b00562.
   PubMed Web of Science ®Google Scholar
• Xi Y, Li W. 2009. BSMAP: whole genome bisulfite sequence MAPping program. BMC Bioinform. 10(1):1–9. doi: 10.1186/1471-2105-10-232.
   PubMedGoogle Scholar
• Xu X, Huang R, Yin W-B. 2021. An optimized and efficient CRISPR/Cas9 system for the endophytic fungus Pestalotiopsis fici. J Fungi. 7(10):809. doi: 10.3390/jof7100809.
   Web of Science ®Google Scholar
• Xu Z, Xiong B, Xu J. 2021. Chemical investigation of secondary metabolites produced by mangrove endophytic fungus Phyllosticta capitalensis. Nat Prod Res. 35(9):1561–1565. doi: 10.1080/14786419.2019.1656624.
   PubMed Web of Science ®Google Scholar
• Xue M, Hou X, Fu J, Zhang J, Wang J, Zhao Z, Xu D, Lai D, Zhou L. 2023. Recent advances in search of bioactive secondary metabolites from fungi triggered by chemical epigenetic modifiers. J Fungi. 9(2):172. doi: 10.3390/jof9020172.
   Web of Science ®Google Scholar
• Yang XL, Awakawa T, Wakimoto T, Abe I. 2013. Induced biosyntheses of a novel butyrophenone and two aromatic polyketides in the plant pathogen Stagonospora nodorum. Nat Prod Bioprospect. 3(4):141–144. doi: 10.1007/s13659-013-0055-2.
   Google Scholar
• Yang XL, Huang L, Ruan XL. 2014. Epigenetic modifiers alter the secondary metabolite composition of a plant endophytic fungus, Pestalotiopsis crassiuscula obtained from the leaves of Fragaria chiloensis. J Asian Nat Prod Res. 16(4):412–417. doi: 10.1080/10286020.2014.881356.
   PubMed Web of Science ®Google Scholar
• Yoshida M, Kijima M, Akita M, Beppu T. 1990. Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin a. J Biol Chem. 265(28):17174–17179. doi: 10.1016/S0021-9258(17)44885-X.
   PubMed Web of Science ®Google Scholar
• Zhang HW, Song YC, Tan RX. 2006. Biology and chemistry of endophytes. Nat Prod Rep. 23(5):753–771. doi: 10.1039/B609472B.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9(9):1–9. doi: 10.1186/gb-2008-9-9-r137.
   Web of Science ®Google Scholar