1516 8913 Babt 60 E17160542
1516 8913 Babt 60 E17160542
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ABSTRACT
Fungal endophytes constitute a major part of the unexplored fungal diversity. Endophytic fungi (EF) are an
important source for novel, potential and active metabolites. Plant-endophyte interaction and endophyte endophyte
interactions study provide insights into mutualism and metabolite production by fungi. Bioactive compounds
produced by endophytes main function are helping the host plants to resist external biotic and abiotic stress, which
benefit the host survival in return. These organisms mainly consist of members of the Ascomycota, Basidiomycota,
Zygomycota and Oomycota. Recently, the genome sequencing technology has emerged as one of the most efficient
tools that can provide whole information of a genome in a small period of time. Endophytes are fertile ground for
drug discovery. EFare considered as the hidden members of the microbial world and represent an underutilized
resource for new therapeutics and compounds. Endophytes are rich source of natural products displaying broad
spectrum of biological activities like anticancer, antibacterial, antiviral, immunomodulatory, antidiabetic,
antioxidant, anti-arthritis and anti-inflammatory.
*
Author for correspondence: vvraophd@gmail.com
INTRODUCTION
Endophytic fungi [EF] are organisms which live in all healthy plant tissues
without signs of disease or morphological changes for at least part or the whole
life cycle of the plant [1]. The existence of fungi inside the plants has been known
since the end of the 19th century, and the term endophyte was first coined in
1866 by de Bary. EF has been associated with plants for over 400 million years
[2]. An endophytic fungus lives in mycelial form in biological association with
the living plant. EF are found in all kinds of plants, i.e. trees, grasses, algae and
herbaceous plants. Endophyte and endophytic fungi have been frequently used to
describe the internal mycota of living plants. EF are now considered as an
important components of biodiversity [ 3,4].EF are highly diverse, with the
reported majority being ascomycetes, also lack a of teleomorphic state [ 5]. In one
survey it is estimated that over one million fungal endophytes exist in nature [ 6].
EF is an important source of novel, potential and active metabolites [7-12].
Bioactive compounds produced by EF main function are helping the host plants
to resist external biotic and abiotic stress, which benefit the host survival in
return. Plants lack immune response to certain pathogens, but the endophytes that
reside inside the plant tissue enhance the immune response of the plants to fight
against invading pathogens [13]. Plant EF has the ability to produce the same or
similar kind of compounds of from their originated host plants. Fungal endophyte
communities differ in species composition, host and tissue preference worldwide
distribution and differ in the polyketide and synthesis and production of bioactive
compounds [14]. In the last few years, considerable knowledge has been
accumulated on the biology of endophytic microorganisms [15]. The study of
endophytes distribution, biodiversity and their biochemical characteristics has
huge importance in plant sciences to understand and to improve plant fitness [ 16].
Endophytes commonly increase plant biomass under stressful conditions but the
cellular mechanisms involved in stress tolerance and growth enhancement are
poorly characterized. EF are considered as an important components of
biodiversity as the distribution of endophytic mycoflora differs with the host. The
omnipresence of endophytic fungi symbiosis with the plant, the extent of their
contribution to fungal biodiversity remains unclear [17]. Apart from the above
mentioned myriad of activities for the protection of host plants EF play an
important role to initiate the biological degradation of dead or dying host-plant,
which is necessary for nutrient recycling. The balanced antagonism hypothesis
[18] was initially proposed to address how an endophyte controls host defenses
mechanisms to be activated against it, ensures self-resistance before being
incapacitated by the toxic metabolites of the host, and manages to grow within its
host without causing visible manifestations of infection or disease [ 19,20].
Plant-endophyte interaction
How does an endophyte manage to exist and grow within its host without causing
visible disease symptoms? Is a complex and precisely controlled interaction.
Endophyte-plant symbioses represent a broad continuum of interactions, from
strong antagonisms to obligate mutualisms. Mutualisms are generally thought to
have evolved from antagonistic interactions, mainly parasitic and the same has
been assumed for fungal endophytes of grasses and woody plants. The continuum
of antagonistic-mutualistic interactions for any two interacting species depends
on phylogenetic and life history constraints, geography, interactions with other
species in the community, and abiotic factors. Similarly, the complex microbial
mutualisms with host plants vary along a continuum from pathogenic to
mutualistic, even within the lifespan of the microorganism and host plant. Despite
General Classification
Endophytic fungi mainly consist of members of the Ascomycota [21] or their
mitosporic fungi, as well as some taxa of the Basidiomycota, Zygomycota and
Oomycota [22, 23] and Classification endophytic fungi and existence in plant cell
(Fig.1). But there are also different ways of grouping fungal endophytes are
suggested by [24] the transmission mode in particular, and distinguished between
the endophytes of the Clavicipitaceae (clavicipitaceous endophytes) and the rest
(non-clavicipitaceous endophytes). Several studies have demonstrated that
various fungal endophytic interactions ranging from mutualistic to antagonistic,
depending on host and endophyte genotype, and environmental conditions [25-29].
Proteomic analysis
Proteins secreted by fungal hyphae play an important role in the plant cell during
symbiosis these molecules used in establishing and maintaining a successful
symbiotic relationship among them. Proteomics appears as a powerful tool
(Fig.2) to gain a global picture and our perception of plantmicrobe interactions.
2-Dimentional Electrophorisis (2-DE) is a tool used to compare infected and
noninfected plant proteomes it also provides a way of identifying plant and fungal
proteins differentially regulated in this symbiosis [91]. Proteins were extracted
from Undifilum oxytropis and analysed using 2-DE and liquid chromatography
tandem mass spectrometry (LC-MS/MS) [92] and found large group proteins were
related to stress and heat shock proteins. EST-based approach was used for
identification of proteins from filamentous fungal endophyte based on [93].
Protein extraction was followed according to [ 94] and further 2-DE analysis was
done for the proteins of Piriformospora indica [95].
Genomic analysis
The field of fungal genomics and with that of eukaryotic genomics, started with
the report on the complete sequence of the yeast S. cerevisiae [96]. Recently, the
genome sequencing technology has emerged as one of the most efficient tools
that can provide whole information of a genome in a small period of time.
Identification of genes expressed during different phases of endophytism such as
pre-penetration, plant tissue penetration and plant colonization is important task
for the fungal genomics. The rapid development in molecular biology and
genomics in the recent advances offers a lot of scope for unraveling the various
facets of the ecology and phylogenetics for the horizontally transmitted
endophytes. Now a days Genomic analysis was done by BLAST search,
Homology modeling tools.
montagnei Sacc
Pichia guilliermondii B. sublitis, Clavibacter
michiganensis, E. coli, H.
pylori, Micrococcus
lysoleikticus, P. aeruginosa,
Sarcina lutea, Staphylococcus
Paris polyphylla var.
aureus, Streptococcus lactis,
yunnanensis [117]
fungi (i.e. Alternaria
brassicae, Botrytis cinerea, C.
albicans, Colletotirchum
gloeosporioides,
F.graminearum, Phytophthora
capsici and Valsa mali
Fusarium sp, Staphylococcus aureus, B.
Sesbania grandiflora
Phaeoacremonium sp., subtilis, E.coli, Pseudomonas,
(L.) Pers., [118]
Acremonium sp., Aeruginosa, C. albicans
.
Cladosporium sp and Cryptococcus neoformans
Colletotrichum
gloeosporioides Penz.,
Phomopsis archeri B.
Sutton, A. flavus gr.,
Nigrospora
sphaerica(Sacc.)Mason,
Colletotrichum
gloeosporioides Penz.,
B. subtilis S. aureus, B.
Phomopsis sp. aff. P.
Vitex negundo Linn, Cereus, E. coli, Klebsilla
archeri B. Sutton, [119]
pneumoniae and S.
Alternaria raphani JW
typhimurium
Groves &skolko, Mucor
hiemalis Wehmer,
Monodictys paradoxa
(Corda) Hughes, Mucor
hiemalis Wehmer,
Nigrospora state of
Khuskia oryzae H.J.
Hudson
A. fumigates, A.
japonicas, A. niger,
Fusarium semitectum,
Ricinus communis Curvularia pallescens, B,subtilis, Enterococcous sp.,
(Aurundi) Phoma hedericola, K, pneumoniae, E, coli, S. [120]
Alternaria tenuissima, typhimurium and S. aureus.
F, solani, Drechslera
australien and A. repens
Aspergillus flavus,
Cladosporium sp.,
Xylaria sp. Adhatoda
Bacillus cereus, Bacillus
Achyranthes aspera, zeylanica Aspergillus
subtilis , Escherichia coli,
Adhatoda zeylanica, sp., Chaetomium
Klebsiella pneumoniae,
Aegle marmelos, spirale, Curvularia
Proteus sp, Pseudomonas sp, [121]
Leucas aspera, clavata, Penicillium sp.
,Salmonella typhi,
Azadirachta indica Alternaria alternata,
Staphylococcus aureus,
Aspergillus fumigatus,
Streptococcus pyogens
Aspergillus niger,
Chaetomium globosum,
Cladosporium sp.,
Braz. Arch. Biol. Technol. v.60: e17160542 Jan/Dec 2017
10 Rajamanikyam, M and Vadlapudi, V et al.
Fusarium oxysporum,
Nigrospora oryzae,
Penicillium sp.,
Pestalotia macrotricha,
Phomopsis sp.,
Rhizoctonia sp., Stenella
agalis, Trichoderma sp.,
Verticillium sp.,
Acremonium sp.,
Cladosporium sp.,
Curvularia lunata,
Fusarium oxysporu,
Fusarium solani,
Nigrospora oryzae,
Pestalotiopsis sp.,
Phoma eupyrena,
Phyllostica sp.,
Trichoderma sp.,
Verticillium albo-atrum
Alternaria sp.,
Colletotrichum sp.,
Fusarium sp., Spicaria
sp., Stemphylium sp
Epicoccum sp., Pestaloti
Baccharis trimera opsis sp. , Cochliobolus
Not specified [122]
. lunatus,
and Nigrospora sp
Antifungal activity
Little-studied groups of fungi are considered to be potential sources of novel
natural products for medicine and agriculture [123]. The function of invasive
fungal infections has increased significantly during cancer organ transplantation,
chemotherapy and bone marrow transplantation. Endophytes are presumably
ubiquitous in plants, with populations dependent on host species and location.
During long research only a few numbers of antifungal agents are available for
the treatment of various life threatening fungal infections. The search for new
antifungal agents to overcome the growing human problems of drugs resistance
in microorganisms is growing. Ongoing global efforts to discover new
compounds from EF of medicinal plants are yielding valuable results [124].
Compounds produced by EF are being recognized as a versatile arsenal of
antifungal agents. Many EF have been reported to have fungicidal activity are
listed (Table.3).
Table -3 list of endophytic fungal activity against fungi
Endophyte Host plant Target fungi Ref
Hormonema sp. Juniperus Aspergillus fumigates and [125]
communis Candida sps
Alternaria sp. Paracoccidioides brasiliensi [126]
and Schizosaccharomyces
pombe
Phaeosphaeria Prunus Monilinia fructicola, [127]
nodorum domestica Colletotrichum
gloeosporioides
Chaetomium globosum Ginkgo Rhizopus stolonifer [128]
No.04 biloba Coniothyrium diplodiella.
Colletotrichum Jatropha Fusarium oxysporum, [129]
truncatum, Nigrospora curcas Sclerotinia sclerotiorum
oryzae, Fusarium
proliferatum,
Guignardia
cammillae, Alternaria
destruens, and
Chaetomium sp
Pestalotiopsis Mangifera Candida albicans [130]
mangiferae indica
Trichoderma Allium Fusarium [66]
brevicompactum sativum oxysporum, Colletotrichum
lindemuthianum, C.
ampelinum, Rhizoctonia
solani, Botrytis cinerea
Colletotrichum Michelia Cladosporium [131]
gloeosporioides champaca cladosporioides, C.
sphaerospermum
Botryosphaeria Melia Alternaria solani [132]
dothidea azedarach
Chaetomium,
Zopfiella, Fusarium,
Purpureocillium,
Arthrinium, Sclerotinia sclerotiorum,
Nigrospora, Eurotium, Phytophthora parasitica var.
Aspergillus, nicotianae, Phytophthora
Tephrosia
Penicillium, melonis, Botrytis cinerea, [133]
purpurea
Neosartorya, Colletotrichum
Talaromyces, gloeosporioides, Rhizoctonia
Alternaria, solani
Curvularia,
Leptosphaerulina,
Bipolaris, Periconia
Cephalotax
us Rhizoctonia solani, Fusarium
Phomopsis quercella [134]
hainanensi oxysporum
s
Suaeda
Alternaria alternate,
maritima , [135]
Aspergillus flavus, Trichophyton rubrum
Suaeda
A.terreus , A.niger
monoica.
Rhizoctonia solani, Fusarium
Ocimum
oxysporum, Colletotrichum
Not specified sanctum, [136]
falcatum and
Aloe vera
Helminthosporium maydis.
Cymbopog
Curvularia lunata Candida albicans ,
on caesius [137]
Trichophyton rubrum
Xylaria sp. strain Haematoxy Alternaria solani, Fusarium [138]
PB3f3 lon oxysporum
brasiletto
Cladosporium, humifusa
Cryptococcus,
Curvularia, Diaporthe,
Epicoccum,
Paraconiothyrium,
Pestalotiopsis and
Phoma
Antiviral compounds
The discovery of the potential antiviral compounds from EF is still in its infancy.
There is only limited number of compounds reported as antiviral agents from
fungal endophytes. The main limitation to antiviral compound discovery is most
probably related to the absence of antiviral screening systems. Altertoxins was
isolated [141] from Alternaria tenuissima QUE1Se have HIV-1 virus activity.
Several hundred endophytic fungal extracts were evaluated on HIV-1 replication
in T-lymphocytes, and out of that four extracts are non-toxic and exhibited
inhibitory with the range of 75% to 99% and out of three of these extracts were
fractionated and fraction DB-2 completely inhibited HIV-1 replication at
concentration that was also found it is not cytotoxic [ 142] . In antiviral activity was
reported against influenza A viral (HN) [143] for the compounds emerimidine
(A, B) ,emeriphenolicins (A,D), aspernidine (A , B) austin, austinol,
dehydroaustin, and acetoxy dehydroaustin for Emericella sp.(HK-ZJ) which is
isolated from of plant Aegiceras corniculatum. A source of several natural
products has been in the endophytic fungi that live within desert plants. [144]
purified coumarins from Alternaria Species in Calophyllum inophyllum.
Endophytes Aspergillus, Curvularia, Fusicoccum, Guignardia, Muscodor,
Penicillium, Pestalotiopsis, and Phomopsis spp isolated [145] from Garcinia
plants and evaluated against Herpes simplex virus type 1 (HSV-1 ATCC VR-
260) and most of fungi exhibited weak to moderate antiviral activity against. EF
isolated [146] from 81 thai medicinal plant species out of 582 pure isolates
obtained 40 species have strong anti-viral activity against HSV-1.
Anticancer substances
Cancer is a group of diseases that can affect various organs of the body, and is
characterized by the uncontrolled growth of abnormal cells and lead to death. It is
a major cause of death worldwide. So far chemical inhibitors of carcinogenesis
are mostly kinase inhibitors in the form of small molecules, antibodies and
organic chemicals. The research and development of anticancer drugs is
expensive which places a high financial burden on individual healthcare costs and
government budgets. Medicinal plants are being reduced significantly due to
over-harvesting, illegal exploitation and destruction of ecological habitat [147] to
conserve endangered medicinal plants and need to develop new alternative
resources for harvesting anticancer compounds from plants. Anti-cancer drugs of
natural products from EF are of are cheap and great value. The EF has been
recognized as a possible useful source of bioactive secondary metabolites,
especially in anticancer application [148]. More than 60% of the anticancer and
70% of the antimicrobial drugs and compounds are currently in clinical use are
natural products or natural product derivatives. There is an increase in need for a
universal natural bioactive compound that can be used to suppress carcinogenic
growth potential [149]. Likewise, there are large numbers of anticancer agents
produced by fungal endophytes inhabiting different medicinal plants. For the sake
of convenience, some of the endophytic fungi showed anticancer activity against
cell lines are presented in the form of a table (Table.4).
Antidiabetic activity
The nature has provided abundant natural resources which can be explored for their
medicinal uses. Diabetes, often referred to by doctors as diabetes mellitus, describes
a group of metabolic diseases in which the person has high blood glucose (blood
sugar), either because insulin production is inadequate, or because the body's cells do
not respond properly to insulin, or both [176]. Nowadays diabetes is growing as
important serious public health problem, particularly in developed countries as a
major threat to global development. We need to find natural and effective
antidiabetic drugs. Several researchers are investigated antidiabetic and
hypolipidemic activity of EF [177, 178]. [179] isolated antidiabetic peptide from EF
Aspergillus awamori from medicinal plant Acacia nilotica and its purified compound
was further identified using HPLC. Lectin (N-acetylgalactosamine, 64 kDa) was
isolated from EF, Alternaria species from plant Viscum album tested for In vitro and
in vivo antidiabetic activity on rats [180].14 endophytic fungi isolated from Taxus
sumatrana and tested for alpha-glucosidase inhibitor activity[181].
Antioxidant activities
Antioxidants have become the topic of interest recently. The field of free radical
chemistry is gaining more attention now a days. Free radicals are reactive oxygen
and nitrogen species which are generated by various physiological processes in
the body. Uncontrolled generation of free radicals leads to attack on membrane
lipids, proteins, enzymes and DNA causing oxidative stress and ultimately cell
death. These ROS are responsible for many degenerative human diseases like
neurodegenerative disorders, cancer, Alzheimers disease, ageing, Parkinsons
disease, diabetes mellitus, atherosclerosis, and inflammatory diseases. Protection
against free radicals can be enhanced by taking sufficient amounts of exogenous
antioxidants. An antioxidant is a stable molecule which donates an electron to a
rampaging free radical and terminates the chain reaction before vital molecules
are damaged. Dietary antioxidants, including polyphenolic compounds, vitamin E
and C are believed to be the effective nutrients in the prevention of oxidative
stress related diseases. Fungal endophytes represent an abundant and dependable
source of novel antioxidant compounds [182-184]. Lot of studies were conducted as
antiviral, anticancer, antidiabetic and antimicrobial effects to test the potential
effects of fungal endophytes, but very few scientists worked on their antioxidant
capacity [185,186]. [187] was conducted antioxidant properties using EF Phyllosticta
sp. which is isolated from medicinal plant Guazuma tomentosa and also
quantified phenol and flavonoid content. Antioxidant was screened [188] with the
2,2-azinodi(3-ethylbenzthiazoline-6-sulfonic acid) (ABTS) decolorization assay
and 2,2-diphenyl-1-picrylhydrazyl (DPPH) found this EF have potential novel
source of natural antioxidants. Antioxidant was screened for EF in medicinal
plants Rhodiola crenulata, R. angusta, and R. sachalinensis [189]. DPPH, FRAP,
and Iron chelating activity are conducted using endophytes Asperigillus niger ,
Penicillium sp. and Trichoderma sp. [190]. Antioxidant compounds isolated from
Acremonium sp identified as sesquiterpene 3,5-dihydroxy-2,5-dimethyltrideca-
2,9,11-triene- 4,8-dione findings based on spectroscopic data, including 1 H-
NMR, 13C-NMR, HMQC, HMBC, and COSY [191].
Historically, the best resources for novel scaffolds have always been natural
products. Immune system of our body plays a crucial role, as an overactive
immune system may lead to certain fatal disease like arthritis. Rhematoid
arthritis(RA) is chronic, inflammatory, and systemic autoimmune disease,
symptoms include pain, swelling, and destruction of cartilage and bone as a result
of which permanent disabilities occur but the exact etiology is unknown.
Nowadays, researcher shows a great interest in those finding medicinal agents
that are derived from microbial source because of the currently available drugs
are either have certain side effects or are highly expensive [192]. Endophytic fungi
Talaromyces wortmannii isolated from medicinal plant Aloe vera and further
seperated as several pure substances and out of that component C showed potent
anti-inflammatory activity and this ability was gained for this metabolite is due to
inhibition of IL-8 release by blocking NF-B and AP-1 activation[193].
Compound Mutolide was isolated from the coprophilous
fungus Lepidosphaeria sp. (PM0651419) and showed good anti-inflammatory
activity and in future it can be used as druggable candidate for the treatment of
inflammatory diseases like RA[194]. The primary purpose for such broad-based
screening of endophytic fungi was to identify novel inhibitors of pro-
inflammatory cytokines involved in various immunological pathways. Ergoflavin
a pigment isolated from EF which is growing on the leaves of an Indian
medicinal plant Mimosops elengi (bakul) showed good anti-inflammatory activity
[195]. Endophytes alternative to chemical comounds which are shown excellent
anti-inflammatory and various biological activities (Figure. 4).
CONCLUSION
Endophytic fungi can produce same or similar compounds originated from their
host plants. Endophytic microorganisms are a huge reservoir of genetic diversity.
Insights gained into endophyte-endophyte and plant-endophyte communication
can be beneficial to biomedical community and the endophyte synthesized and
secreted chemicals can be of importance to the society for the development of
novel antibiotics against deadly pathogens. However, only a few numbers of
antifungal agents are now available for the treatment of various life threatening
fungal infections. There is an ongoing need for novel drugs that are highly
effective in the treatment of cancer, drug resistant bacteria, and fungal infections.
However, the application of microorganisms by the pharmaceutical and food
industries to obtain different compounds of interest is still modest. Antioxidants
have become the topic of interest recently. Fungal endophytes represent an
abundant and dependable source of novel antioxidant compounds. There has been
Braz. Arch. Biol. Technol. v.60: e17160542 Jan/Dec 2017
16 Rajamanikyam, M and Vadlapudi, V et al.
ACKNOWLEDGMENTS
VVR would like to thank to Ministry of Earth Sciences, New Delhi, India (MoES /
36 / OOIS / Extra / 18 /2013) for financial support.
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