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Antioxidant Fortification of Eggs through Nutrition of Laying Hens Administered...
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Chapter 3
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The Endophytes: A New
Resource for Vulnerable Plant
Bioactive Compounds
Mostafa Fazeli
Abstract
Plant-associated microorganisms that live symbiotically in the plant body without
causing disease symptoms are called endophytic microorganisms. Endophytes,
including bacteria and fungi, can enhance the growth of the host plant and increase its
resistance to pests, phytopathogens, and environmental stresses. In addition, endophytes can regulate the synthesis of plant secondary metabolites. Endophytes are a
new reservoir for the discovery and production of valuable active substances. Some
endophytic secondary metabolites are the same as host plants, such as paclitaxel. This
finding has increased the importance of endophytes because the production of effective substances on an industrial scale in microorganisms is easier than in plants and
has lower environmental costs. Therefore, endophytes need more attention in the
pharmaceutical industry.
Keywords: endophyte, symbiosis, secondary metabolites, Taxol, endophytic fungi
1. Introduction
The rapid growth of human societies has increased the need to improve health
standards and intensify food production. On the other hand, the emergence of drug
resistance in pathogens and pests has become an increasing need to promote the
search for new pharmaceutical and agricultural sources. Medicinal plants have been a
valuable source of bioactive substances for a long time; however, environmental
considerations, labor-intensive, high cost, and time-consuming have limited the use of
these plant resources. On the other hand, the production of plant material in cell
cultures faces technical challenges. The production of effective plant substances
entered a new age with the discovery of the endophytic fungus Taxomyces andreanea
in the yew, which could produce bioactive such as its host. Microorganisms are an
attractive source of new biomaterials; also, they have the potential to increase the
production of existing valuable materials. Plant-associated microorganisms called
endophytes live in symbiosis with the tissues of their host plants. Many microorganisms, such as fungi, bacteria, and actinomycetes, have been discovered in endophytic
relationships with plants [1].
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The endophytes live asymptomatically in mutual association with plants. The
endophytic lifestyle of microbes plays an important role in maintaining the health of
plants by providing nutrients and defending plants against abiotic and abiotic stresses
[2]. In addition, endophytes can produce many bioactive. Some of these substances
are similar to the profile of the host plant’s bioactive, which has increased the hope for
cost-effective and environmentally friendly production. In the pharmaceutical and
agricultural industries, bioactive compounds are known for their many applications.
During the last two decades, endophytes have been recognized as important sources
of bioactive compounds. Also, the proportion of new structures produced by endophyte isolates (51%) is significantly higher than that of soil isolates (38%), which has
made endophytes one of the main natural product screening programs [3].
2. Endophytes
Microorganisms colonize many living plants in nature, and the degree of this
microbial colonization varies by plant species. If the host plant tissue remains stable
during this colonization, the relationship may vary from latent pathogenesis to mutual
symbiosis. These microorganisms may be epiphytes, endophytes, or latent pathogens.
Endophyte refers to microorganisms that are found under normal conditions in the
tissues of living plants, without causing apparent diseases or visible symptoms of
disease [4]. Endophytes are ubiquitous and spend a significant part of their life cycle
without causing negative or obvious symptoms in the living tissues of the host plant.
The word endophyte was first coined in 1866, where “endo” means “inside” and
“phyte” means plant. They are mostly located in internal tissues such as roots, stems,
leaves, flowers, and seeds. Endophytes may be transmitted horizontally or vertically
[2], and some may even be seed-borne and passed on to the next generation [4]. A
large community of endophytes lives inside the tissues of any plant. The diversity of
endophytes is influenced by the host plant and its characteristics, including genotype,
tissue, growth stage (age), and health status [5].
Endophytes have been isolated from all different parts of the plant. More than 200
genera from 16 bacterial phyla have been documented to be associated with endophytes [6]. It is also estimated that out of about 1.5 million species of fungi, one
million of them are endophytic [7].
2.1 Endophytes: Plant interaction
Endophytes can provide benefits to their host plants. They mediate abiotic and
biotic stress tolerance, reduce water consumption, and defend against pests and phytopathogens [8]. This interaction is controlled by endophyte and plant genes. The
endophytic relationship is a novel and cost-effective plant-microbe evolutionary relationship that is driven by location and not defined by function [9]. Endophytic
microbes are chemical synthesizers inside plants [10]. The imperceptible association
of endophytes with the plant enables them to evolve [9]. It is the coevolution between
endophytes and their host plant that determines the production of bioactive compounds. These compounds often play a role in the plant-microbe interaction in different ways and can bring different fitness benefits to the host plant [11, 12].
Plant compounds can be of plant origin or derived from endophytes or even can be
produced by both. In the latter case, the endophyte may be involved in the entire
pathway, but another scenario may be that only parts of the biosynthesis originate
2
The
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Endophytes: A New Resource for Vulnerable Plant Bioactive Compounds
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the endophyte. In plant-endophyte interactions, significant changes appear in
from
secondary metabolism of symbionts, and these changes can be as a result of (i)
the
of
induction
by
the host, (iii) host and endophyte share part of a specific pathway, (iv) the host
metabolizes
compounds. [13]. Endophytes isolated from medicinal plants can produce bioac-
ary
tive
metabolites and play a vital role in inducing secondary metabolite production
host plants [5, 14].
by
3. Secondary
host metabolism by endophyte, (ii) induction of endophyte metabolism
endophyte products, and (v) the endophyte can metabolize host second-
metabolites
Endophytes play a critical role in enhancing plant growth and are also known for
ability to produce bioactive with biotechnological applications. The use of herbal
their
is
medicines
medicine.
rich sources of natural products. They are very valuable for disease prevention
their
treatment [15]. Endophytes communicate with their host plant through metabolic
and
interactions
ing
biological activities. In addition, the coevolution of endophytes with the host plant
enables
bioactive
common in developing countries and up to 80% of people use this
This traditional medicine has a long history. Medicinal plants are known for
[1, 16], which enable them to produce signaling molecules with interest-
them to mimic the biological properties of the host and produce similar
compounds [16].
Endophytes synthesize various bioactive compounds. However, compounds that
shown anticancer properties have attracted more attention, and in the mean-
have
the discovery of paclitaxel production by endophytic fungi has been a turning
time,
in
point
endophyte research.
3.1
Paclitaxel (Taxol)
Paclitaxel, with the brand name Taxol, is a terpenoid that was mainly obtained from
tissues of the yew plant; due to its amazing properties in binding to microtubules
the
inhibiting the division spindle, it is used in the treatment of various types of cancer,
and
especially
plant
and
Therefore,
mercialized.
synthesize
The discovery of
undoubtedly
endophytic
broth
for
this
taxel
including
Pestalotiopsis,
ciency
per
laboratory conditions [84]. Microbial production of paclitaxel by endophytes has
in
3
breast and ovarian cancer. It has been used a lot. However, extraction from
sources due to the slow growth of the plant, the difficulty of purifying paclitaxel,
also its low amount in the plant tissues did not meet the needs of the market.
several methods, such as chemical synthesis, were also developed and com-
The scientists were also looking for alternative sources until the ability to
it in
the endophytic fungi of the host plant was discovered.
Taxomyces andreanea from the Pacific yew, Taxus brevifolia,
a
turning point in the field of bioprospecting for endophytes. This
fungus demonstrated the ability to synthesize paclitaxel in the culture
same as its host plant [17]. Microbial production of paclitaxel is very important
the development of the first billion-dollar anticancer drug business [17, 18]. Since
important discovery, several other endophytic fungi and bacteria showing pacli-
production from yew and other plant species have been discovered (Table 1),
Alternaria, Bartalinia, Fusarium, Lasiodiplodia, Metarhizium, Monochaetia,
Penicillium, Phoma, and Spomatoichoanthermium [13, 81–83]. The effi-
of
paclitaxel among these fungal species varies [from nanograms to milligrams
liter], and their productivity is often lost during several generations of cultivation
was
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Secondary
metabolite
Paclitaxel
(Taxol)
Host Endophyte Yield
Taxus brevifolia Taxomyces andreanae 0.02–0.05 [17]
T. wallichiana Pestalotiopsis microspora 0.06–0.07 [19]
Taxodium distichum Pestalotiopsis microspora Cp-4 0.05–1.49 [20]
Taxus cuspidata Alternaria sp. Ja-69 0.16 [19]
Taxus baccata Fusarium lateritium Tbp-9 0.13
T. baccata Monochaetia sp. Tbp-2 0.10
T. baccata Pestalotia bicilia Tbx-2 1.08
T. cuspidata Pestalotiopsis microspora Ja-73 0.27
T. wallachiana Pestalotiopsis microspora Ne-32 0.5
T. sumatrana Pithomyces sp. P-96 0.095
T. canadensis Erwinia taxi* 2.5–15 [21]
Wollemia nobilis Pestalotiopsis guepinii W-1f-2 0.49 [22]
Torreya grandifolia Periconia sp. No. 2026 0.03–0.83 [23]
Ginkgo biloba Alternaria sp. 0.12–0.26 [24]
T. baccata Kitasatospora sp. * 120 [25]
T. baccata Penicillium sp. 111
T. canadensis,T. brevifolia,
T. hunnewelliana, T.
baccata,T. cuspidata
Tremacron mairei Tubercularia sp. TF5 185.4 [27]
T. yunnanensis Taxomyces sp. 2.3
T. chinensis var. mairei Ozonium sp. BT2 4–18 [28]
T. cuspidata Botrytis sp. HD181–23 206.34 [29]
T. chinensis var. mairei Botrytis sp. XT2 161.24
T. chinensis var. mairei Ectostroma sp. XT5 276.75
T. chinensis var. mairei Papulaspora sp. XT17 10.25
T. chinensis Alternaria alternata
chinensis var. mairei Fusarium mairei Y1117 2.7 [31]
T.
T. chinensis var. mairei Ozonium sp. EFY-21 21 [32]
Aegle marmelos Bartalinia robillardoides AMB9 187.6 [33]
Cardiospermum
helicacabum
T. chinensis Fusarium mairei UH23 286.4 [35]
Citrus medica Phyllosticta citricarpa No.598 265 [36]
Podocarpus sp Aspergillus fumigatus EPTP-1 557.8 [37]
T. baccata Botryodiplodia theobromae BT115 280.5 [38]
T. cuspidata Fusarium arthrosporioides F-40 131 [39]
Bacillus cereus ssp. taxi, Bacillus megaterium
ssp. taxi, Pantoea sp., Bacillus cereus, Bacillus
subtilis ssp. taxi, Bacillus megaterium,
Curtobacterium sp., Sphingomonas ssp. taxi*
TPF6 84.5 [30]
Pestalotiopsis pauciseta CHP-11 113.3 [34]
(μg/L)
1–25 [26]
Ref
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Endophytes: A New Resource for Vulnerable Plant Bioactive Compounds
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Secondary
metabolite
Corylus avellana and
T. baccata
YieldEndophyteHost
(μg/L)
Phyllosticta spinarumCupressus sp [40]235No.625
Phyllosticta tabernaemontanaeWrightia tinctoria [41]461
Fusarium solaniThysanophrys celebica [42]1.6
Aspergillus nigerT. cuspidata var. taxi HD86– [43]273.69
F. solaniIT. chinensis [44]163.35Tax- 3
Metarhizium anisopliaeT. chinensis [45]846.1H- 27
Cladosporium cladosporioidesT. media [46]800MD2
Aspergillus candidusT. media [47]112MD3
Mucor rouxianusT. chinensis [48]NDDA10
Phyllosticta dioscoreaeHibiscus rosa-sinensis [49]298No.605
Chaetomella raphigeraTerminalia arjuna 79.6TAC15 –211.1 [50]
Pestalotiopsis terminaliaeTerminalia arjuna [51]211
Nodulisporium sylviformeTaxus cuspidata [52]450
Lasiodiplodia theobromaeMorinda citrifolia [53]245
Pestalotiopsis malicolaRhizosphere [54]186
Phoma betaeGinkgo biloba [55]795
Stemphylium sedicolaT. baccata [56]6.9SBU-16
F. redolensT. baccata [57]66
Penicillium aurantiogriseum [58]70NRRL 62431
P. medicaginisT. wallichiana [59]1125
Aspergillus aculeatinusT. chinensis var. mairei [60]334.92Tax-6
Aspergillus terreusPodocarpus gracilior [61]20EFB108
Aspergillus flavipesRhizosphere 185– [62]850
Penicillium chrysogenumRhizosphere [62]85
Alternaria brassicicolaTerminalia arjuna [63]140.8
Aspergillus fumigatusTaxus sp. [64]1590TPF-06
Cladosporium cladosporioidesCatheranthus roseus [65]700
Aspergillus oryzaeTarenna asiatica [66]95.04
Epicoccum nigrumT. baccata [67]61.35TXB502
Bacillus flexusSargassum polycystum [68]NDDMTMMB08*
Bacillus licheniformis
DMTMMB10*
Oceanobacillus picturaeAcanthaphora specifera DMTMMB24*
Penicillium polonicumGinkgo biloba [69]90.53AUMC14487
ColletotrichumMangifera indica [70]NDsp. MIP-5
AnnulohypoxylonT. wallichiana [71]282.05sp. MUS1
Ref
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Secondary
metabolite
baccatin III T. chinensis Didmyostilbe sp. DF110 ND [78]
10-deacetyl
baccatin III
Some strains that are only capable of producing precursors, such as baccatin III and 10-DAB, are listed separately.
*
Reveals bacterial producers.
Host Endophyte Yield
Persea americana Neopestalotiopsis clavispora KY624416 100.6 [72]
Moringa, Hibiscus Penicillium sp. No.5 54.42–184.3 [73]
Aspergillus niger No.10 43.95
Fusarium sp. No.8 26.8
Corylus avellana Stemphylium vesicarium CA18 1400 [74]
Corylus avellana Melanconium hedericola CA12 1000
Calotropis procera,
Catharanthus roseus
Millingtonia hortensis Cochliobolus hawaiiensis 282 [76]
T. wallichiana Aspergillus sp. GBPI TWR F5 5450 [77]
T. wallichiana Diaporthe phaseolorum 219 [79]
T. wallichiana Trichoderma sp. IRB54a 187.56 [80]
Corylus avellana Melanconium hedericola CA12 22,100 [74]
Penicillium singorense 13 [75]
Aspergillus microcysticus CA3 20,400
Arthrinium arundinis CA2 16,400
(μg/L)
Ref
Table 1.
Production of paclitaxel and some of its precursors by endophytic microorganisms; due to the multiplicity of
different isolates from the same species, the name of the strain is also mentioned, as well as the amount of
production in the strains noticed without subsequent manipulations and optimizations.
been observed mostly in fungal isolates. However, there are limited reports of the
production of paclitaxel and some of its precursors by several strains of endophytic
bacteria, such as Erwinia taxi, Micromonospora sp., Streptomyces sp., Kitasatospora sp.,
Bacillus cereus, B. megaterium, Sphingomonas ssp. taxi, B. subtilis, Pantoea sp., and
Curtobacterium sp. [85]. Also, the discovery of paclitaxel-producing bacteria symbi-
otic with marine macroalgae Sargassum polycystum and Acanthaphora specifera showed
that the search for endophytic sources of paclitaxel should not be limited to plants and
terrestrials [68].
In addition to paclitaxel production, some endophytes can increase paclitaxel production in plants. Endophytic Pseudodidymocyrtis lobariellae fermentation broth can
effectively increase paclitaxel accumulation in T. chinensis by regulating phytohormone metabolism and signal transduction and further regulating the expression of
several key genes involved in paclitaxel biosynthesis [86]. The fermentation broth of
Kocuria sp., Micromonospora sp., and Sphingomonas sp. also significantly increased the
accumulation of taxanes in the stem cells of T. yunnanensis [87].
3.2 Vinca alkaloids
Vinblastine and vincristine are vinca alkaloids from Catharanthus roseus plant [88].
These compounds were the first herbal anticancer agents that were introduced to the
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Endophytes: A New Resource for Vulnerable Plant Bioactive Compounds
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clinical
cancer,
was
pounds
induce
described
market. In the 1960s, vinblastine was used to treat breast cancer, testicular
and Hodgkin’s disease. Three years later, its oxidized derivative, vincristine,
introduced, which was widely used in the treatment of leukemia. These com-
inhibit the division spindle by irreversibly binding to microtubules and finally
apoptosis. Vinblastine production from endophytic Alternaria was first
in
1998, followed by Lingqi et al. discovered an endophytic Fusarium
oxysporum from C. roseus that successfully produced vincristine [89, 90]. These dis-
coveries
tine.
sparked a global hunt for new alternative sources of vinblastine and vincris-
Vincristine is most valuable as an anticancer agent. Endophytic F. oxysporum
successfully biotransformed vinblastine to vincristine [91].
Palem et al. isolated an endophytic
produce
sphaerica
tine
tine
to
have
[94,
C.
Some of these isolates can biotransform vinblastine into vincristine. Also, some isolates only can synthesize vindoline as a
valuable precursor of anticancer drugs.
vinblastine and vincristine [92]. Ayob et al. isolated an endophyte Nigrospora
from C. roseus that can produce vinblastine. This fungus produced vinblaswith 10-fold better cytotoxicity to a breast cancer cell line compared to vinblasextracted from C. roseus [93]. Endophytic fungal and bacterial species were found
have the ability to synthesize Vindoline —the precursor of vinca alkaloids— and
a
high potential to be used as a biological elicitor in the production of vincristine
95]. Also, a species of Streptomyces spp. was isolated from the rhizosphere soil of
roseus, which can produce vinblastine and vincristine, (Table 2) [104].
AlternariaCatharanthus roseus [89]FungalVinblastinesp.
F. oxysporum [90]FungalVincristine
Fusarium solani [97]FungalVinblastine, Vincristine
F. oxysporum [98]FungalVinblastine, Vincristine
Talaromyces radicus [92]FungalVinblastine, Vincristine
Eutypella [99]FungalVincristinesp.
Nigrospora sphaerica [93]FungalVinblastine
Microbacterium [94]BacterialVindolinesp.
Chaetomim globosum [101]FungalVinblastine
Curvularia verruculosa [102]FungalVinblastine
Botryosphaeria laricina [103]FungalVinblastine, Vincristine
C. roseus
Rhizospheric Soil
Streptomyces spp. [104]BacterialVinblastine, Vincristine
F. oxysporumC. roseus [105]FungalVinblastine, Vincristine
Alternaria sesami [95]FungalVindoline
Nigrospora zimmermanii [106]FungalVincristine
Thalaromyces radicus from C. roseus that
RefStrainVinca alkaloidsEndophyteHost plant
[96]FungalVincristineMycelia sterilia 97CY-3
[100]FungalVinblastine, VincristineUnidentified
could
Table 2.
Microbial production of vinca alkaloids by endophytic microorganisms; endophytic producers of vinca alkaloids
have so far only been isolated from C. roseus or its rhizosphere soil.
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3.3 Camptothecin
Camptothecin (CPT) is a pentacyclic quinoline alkaloid isolated from the wood of
Camptotheca acuminata and the root of Nothapodytes foetida. Several reports show the
therapeutic potential of CPT and its derivatives for the treatment of colon, cervical,
uterine, lung, and ovarian cancer. Most of the two promising anticancer activities [107]
are related to its main derivatives, 9-methoxycamptothecin and 10-hydroxycamptothecin, because CPT is not directly used as an anticancer drug due to its low solubility,
short half-life, and toxicity [108–110]. These cytotoxic agents act by selectively
inhibiting topoisomerase 1. and thereby disrupting the DNA replication process.
In 2005, the CPT-producing endophytic fungus Entrophospora infrequens was isolated
from N. foetida [109]. Endophyte Neurospora crassa and Nodulisporium sp. isolated from
N. foetida produces CPT in culture medium [111, 112]. There are also examples of
endophytes that can produce hydroxylated CPT derivatives, for example, Mycelia sterilia
XK001 can produce 10-hydroxycamptothecin, which is the clinically active derivative of
CPT [107]. Most CPT-producing endophytes are fungi; however, there are also reports
of bacterial producers (Table 3)[116,121,123,126].ACPT-producingendophytic
fungus from the marine sponge Cliona sp. It has been isolated that unlike other endophytes isolated from soil and plant environments, and it has been isolated and identified
from the marine environment and aquatic organisms [131].
Secondary metabolite Host plant Endophyte Strain Ref
CPT Nothapodytes foetida Entrophospora infrequens Fungal [109]
Neanotis foetida Neurospora sp. Fungal [111]
Camptotheca
acuminata
N. foetida Nodulisporium sp. Fungal [112]
N. nimmoniana Botryosphaeria parva Fungal [113]
Apodytes dimidiata F. solani Fungal [114]
C. acuminata Trichoderma atroviride Fungal [115]
Miquelia dentata
Bedd.
M. dentata Bedd. Fomitopsis sp., Alternaria alternata,
C. acuminata Fusarium nematophilum, Alternaria
N. foetida Fusarium oxysporum Fungal [119]
Catharanthus roseus F. solani Fungal [120]
C. acuminata Paenibacillus polymyxa Fungal [121]
N. nimmoniana Colletotrichm fructicola, Corynespora
N. nimmoniana F. solani Fungal [110]
Pyrenacantha
volubilis
Piper betel L. Aspergillus niger Fungal [124]
F. solani Fungal [108]
Bacillus subtilis, Bacillus sp., Bacillus
cereus, Lysinibacillus sp.
Phomposis sp.
Alternata, Phomopsis vaccinii
cassiicola
Bacillus sp., B. subtilis, Bacillus
amyloliquefaciens
Bacterial [116]
Fungal [117]
Fungal [118]
Fungal [122]
Fungal [123]
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Chonemorpha
fragrans
Ophiorrhiza mungos Meyerozyma sp.,Talaromyces [127]Fungalsp.
sponge Penicillium chrysogenumCliona sp. [131]Fungal
10-hydroxyCPT No. nimmoniana [107]FungalMycelia sterilia_ XK001
Podophyllotoxin Podophyllum
hexandrum
D. veitchii [136]FungalPenicillium implicatum
Solanum
hexandrum
Deoxypodophyllotoxin Aspergillus fumigatesJ. communis [151]Fungal
Huperzine A AcremoniumHuperzia serrata [152]Fungalsp.
Phlegmariurus
cryptomerianus
F. solani [125]Fungal
Kytococcus schroeterEphedra foliata [126]bacterial
Alternaria alstroemeriae, AlternariaN. nimmoniana
burnsii
Phyllosticta elongataCipadessa baccifera [129]Fungal
Aspergillus terreus, Aspergillus flavusFicus elastica [130]Fungal
Aspergillus terreusCestrum parqui [132]Fungal
DiaportheNo. nimmoniana [133]Fungalsp. F18
Alternaria sp., Penicillium [134]Fungalsp.
PenicilliumDiphylleia sinensis Fungalsp.
MoniliaDysosma veitchii sp., Penicillium Fungalsp.
Penicillium implicatumD. sinensis [135]Fungal
AlternariaJuniperus vulgaris [137]Fungalsp.
Phialocephala fortiniiP. peltatum [138]Fungal
Trametes hirsutaP. hexandrum [139]Fungal
Alternaria neesexP. hexandrum [140]Fungal
Fusarium oxysporumJuniperus recurva [141]Fungal
F. solaniP. hexandrum [142]Fungal
Mucor fragilis [143]Fungal
Alternaria tenuissimaPodophyllum emodi [144]Fungal
PenicilliumD. sinensis sp. [145]Fungal
Chaetomium globosum, PseudallescheriaP. hexandrum
sp.
FusariumDysosma versipellis [147]Fungalsp.
PenicilliumP. hexandrum [148]Fungalsp.
PenicilliumDysosma difformis sp., Trametes sp.,
Purpureocillium sp., Aspergillus sp.,
Ganoderma sp.
Fusarium proliferatumD. difformis [150]Fungal
Blastomyces [153]Fungalsp.
Botrytis Fungalsp.
RefStrainEndophyteSecondary metabolite Host plant
Fungal [128]
[146]Fungal
[149]Fungal
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