<table><caption>Table 1. Cont.</caption><thead><tr><th>Sr. No.</th><th>Fungus</th><th>Source</th><th>Locality</th><th>Compounds Isolated</th><th>Biological Target</th><th>Biological Activity (MIC/IC<sub>50</sub>/ID<sub>50</sub>)</th><th>Reference</th></tr></thead><tbody><tr><td>170</td><td>Exserohilum rostratum</td><td>Phanera splendens (Kunth) Vaz</td><td></td><td>Ravenelin (440)</td><td>Bacillus subtilis and Staphylococcus aureus</td><td>MICs, 7.5 and 484 µM</td><td>[190]</td></tr><tr><td rowspan="3">171</td><td rowspan="3">Exserohilum rostratum</td><td rowspan="3">Bauhinia guianensis</td><td rowspan="3"></td><td>Monocerin (441)</td><td>P. aeruginosa</td><td>MIC, 62.5 µg/mL</td><td rowspan="3">[191]</td></tr><tr><td>Annularin I (442)</td><td>E. coli and B. subtilis</td><td>MIC, 62.50 and 31.25 µg/mL</td></tr><tr><td>Annularin J (443)</td><td>E. coli and B. subtilis</td><td>MIC, 62.50 µg/mL each</td></tr><tr><td colspan="8"><strong>Basidiomycete</strong></td></tr><tr><td>172</td><td>Psathyrella candolleana</td><td>Ginkgo biloba</td><td></td><td>Quercetin (444), carboxybenzene (445), and nicotinamide (446)</td><td>S. aureus</td><td>MIC 0.3906, 0.7812 and 6.25 µg/mL</td><td>[192]</td></tr><tr><td>173</td><td>Irpex lacteus DR10-1</td><td>Distylium chinense</td><td>Banan district of Chongqing in the TGR area, China</td><td>Irpexlacte A (447), irpexlacte B-D (448–450)</td><td>P. aeruginosa</td><td>MIC values ranging from 23.8 to 35.4 µM</td><td>[193]</td></tr><tr><td colspan="8"><strong>Zygomycetes</strong></td></tr><tr><td>174</td><td>Mucor irregularis</td><td></td><td></td><td>Chlorflavonin (451)</td><td></td><td></td><td>[194]</td></tr></tbody></table>
## 4. Methods Used for Activation of Silent Biosynthetic Genes

It has been reported that fungi have various unexpressed gene clusters related to bioactive secondary metabolites, which do not express in mass multiplications of the axenic form [213,214]. The expression of such gene clusters directly or indirectly depends on the surrounding environment of the microorganism. In axenic form, various induction or activation signals are or may be absent for some bioactive molecule production in the culture, which are usually present in natural habitats [215]. Such biosynthetic gene clusters (BGC) are part of the heterochromatin of fungal chromosomes, which do not express at laboratory conditions [216].

To induce such silent biosynthetic gene clusters two major approaches have been reported, including pleiotropic- and pathway-specific approaches, which include various techniques like knocking down, mutation induction [217], co-culture methods [218], heterologous expression [219,220], interspecies crosstalk [221], one strain many compounds (OSMAC) [222] and epigenetic manipulation [223]. Changes in media composition and physical factors like pH, temperature, light, salt concentration, metal and elicitor also support the induction of silent BGC and improve production of secondary metabolites in microbes. The generation of various types of stresses significantly affects the metabolic activities of growing culture and microbes to release compounds for their survival under stress conditions. Changes in physical conditions or stresses impacted gene regulation by upregulating or downregulating the gene expression [126,224]. Nowadays, high throughput elicitor screening technique (HiTES) is also employed to save time in exposing culture against various types of elicitors. In this technique selected culture is grown in 96 well plates with various elicitors in each well and after the incubation period metabolites are identified by mass spectrometry or assay system.

The mutation is one of the other approaches to induce silent biosynthetic gene clusters (BGC). Mutation in RNA polymerase genes and ribosomal proteins changes the transcription and translational process and upregulates the expression of biosynthetic gene clusters. Some of the genes related to biosynthetic gene clusters are silent from decades and overexpression of *adpA*, a global regulatory gene, induced the expression of silent lucensomycin in *Streptomyces cyanogenus* S136 [225]. Cloning is another type of molecular technique used to express the silent BGC incompatible strains. In the cloning method, isolation of high-quality DNA, fragmentation, library construction and development of suitable expression vectors for large sequences of BGC is a challenging task and many groups are working on this aspect [226]. In addition to this, use of bioinformatics also helps in direct cloning of silent BGCs and their expression for secondary metabolites production. Development of various bioinformatics tools such as PRISM3, BiG-SCAPE and anti-SMASH etc facilitated the scientist to identify bioactive gene clusters in unknown strains without time consumption used in identification of active BGC sites [227]. The CRISPR-Cas system is also a excellent tool for cloning system or genome editing that provides better expression of silent BGC in comparison to conventional molecular techniques [228]. Similarly, promoter engineering, transcriptional regulation engineering and ribosome engineering also support the activation of silent BGC through molecular approaches [229]. Recent use of Cpf1 nuclease in genome editing was also found to be a suitable tool for induction of silent BGC [230].

### 4.1. Epigenetic Modification

On the other hand, epigenetic modification played a great role to induce the silent genes related to bioactive molecules, which are actively produced under symbiotic interactions. Epigenetics refers to the study of DNA sequences that do not changes in mutation but change in gene function [231]. The epigenetic regulations such as methylation, demethylation, acetylation, deacetylation and phosphorylation of histones also regulate the transcription of biosynthetic genes of fungi and are helpful in silencing or expression of such genes related to the production of secondary metabolites [232]. The importance of epigenetic regulation in secondary metabolite production by fungi has been shown in a few reports published [231,233–236]. Modification or alteration in DNA or chromatin changes
the expression level of the selected genes, which directly impacted the biosynthesis of the
metabolites in the strain.

## 4.2. *The Co-Culture Strategy*

The co-culture is another method to induce the silent biosynthetic gene clusters by interspecies cross-talking of microorganisms. In this method, various combinations of inducers with producer microbial strains are screened for the production of novel molecules. In co-culture technique real-time bioactivity screening can also be measured by the growth of pathogen as co-culture [218]. Recently, Kim et al. [237] reviewed the co-culture interactions of fungi with various actinomycetes for induction of silent biosynthetic gene clusters and reported upregulation and production of novel antibiotics and bioactive compounds. Co-culturing of microbes provides the habitat type environment to producers and helps to promote silent BGCs by producing signal molecules. Exchange of chemical signals of growing organisms is helpful in the induction of defense molecules and other silent BGC, and usually results in the production of new natural products or secondary metabolites in the culture [238].

Another concept has also been introduced to elicit the production of silent secondary
metabolites by scaffold technique. In this technique, two types of scaffold named cotton
and talc powder are introduced in the medium which physically interacts with the grown
culture and elicit chemical signaling of the culture and activate the production of silent
BGC. The addition of scaffold in the medium supports the grown culture in formation of
biofilm and provides a mimic architecture of natural habitat [239,240]. The addition of
scaffold in medium affects the morphology of growing culture and sporulation pattern like
an agglomeration of spores, oxygen diffusion in comparison to non-scaffold containing
medium and then facilitates more metabolites production [241].

4.3. OSMAC

In the OSMAC technique different cultivation approaches are applied to induce silent
bioactive gene clusters to promote more production of secondary metabolites including
media variations, variation in media composition, co-cultivation with other strains and
variations in cultivations strategy [222,242]. Variation in growth conditions also supports
the induction of silent biosynthetic gene clusters and the production of novel compounds.
Scherlach and Hertweck [243] and Scherlach et al. [244] reported the production of novel
aspoquinolone and aspernidine alkaloid compounds from *Aspergillus nidulans* by variation
in growth conditions.

5. Conclusions

Increasing resistance among microbial pathogens against existing antibiotics has been a
major concern during the past several decades. Scientists are exploring new sources of novel
antibiotics and other bioactive compounds that can curb pathogenic infections and over-
come antimicrobial resistance. Endophytic fungi have been reported to secrete a wide spec-
trum of bioactive compounds to counter pathogens. In the current review, we have reported
453 new bioactive compounds, including volatile compounds, isolated during the period of
2015-21 from various endophytic fungi belonging to the Ascomycetes, Basidiomycetes, and
Zygomycetes classes. Newly reported bioactive compounds have shown activity against
various pathogenic bacteria and shown scaffold similarity with alkaloids, benzopyranones,
chinones, cytochalasins, mullein, peptides, phenols, quinones, flavonoids, steroids, ter-
penoids, sesquiterpene, tetralones, xanthones, and others. The lowest in vitro activity in
terms of minimum inhibitory concentrations (MICs) in the 0.1–1 µg/mL range against
various pathogens was reported for the compounds vochysiamides A (23) and B (24), col-
letotrichone A (376), 15-hydroxy-1,4,5,6-tetra-epi-koninginin G (322), trichocadinin G (330)
and eupenicinicol D (435). Compounds like fusarubin (287), chetomin (62), chaetocochin
C (63), and dethiotetra(methylthio)chetomin (64), pretrichodermamide A (296), terpestacin
(105), fusaproliferin (106), mutolide (108), isoeugenitol (120) and nigrosporone B (417) were
reported to have significant in vitro anti-mycobacterial activity and could be developed as potential drugs against resistant mycobacterial infections. The production of such bioactive compounds and their activity is also affected by the surrounding environment and conditions. Various techniques related to induction of silent gene clusters such as epigenetic modifications, co-culture, OSMAC and mutation have been reported

In most of cases only in vitro data against a limited number of bacteria is reported and there is a great need for extensive in vitro studies including their mode of action, kill curve studies, mutation induction frequency, resistance occurrence frequency studies, in vitro cytotoxicity and initial in vivo evaluation followed by formulation studies. Moreover, there is also a need to perform extensive in vitro efficacy testing studies using panels of references strains and clinical strains to establish MIC90 and MIC50 values. Generation of comparative efficacy data with benchmark clinical compounds is very important from a further development perspective. These extensive studies also help to generate data for understanding the scope of work when we consider such potent molecules for semisynthetic work. The exact studies to be performed during screening and further shortlisting of semi-synthetic molecules can be extracted from this initial extensive work.

Still, more research is required to investigate a new generation of antibiotics which can control the increasing resistance of infectious microorganisms in a sustainable manner. The success of this exploration depends upon screening more and more endophytic fungi and ways of their isolation, fermentation and scale-up.

**Author Contributions:** Conceptualization: (S.K.D., L.D.), Literature search and compilation: (S.K.D., H.C., S.S.); Writing abstract, introduction, conclusion, proof reading: (S.K.D., G.B.M., S.S., H.C., M.K.G.). Preparation of data tables: (M.K.G., S.K.D.). Generating structures: M.K.G., S.K.D. Overall compilation and coordination: (S.K.D., L.D.). All authors have read and agreed to the published version of the manuscript.

**Funding:** This research received no external funding.

**Institutional Review Board Statement:** Not Applicable.

**Informed Consent Statement:** Not Applicable.

**Data Availability Statement:** Not Applicable.

**Conflicts of Interest:** The authors declare no conflict of interest.

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