Endophytic actinobacteria of medicinal plants

23 Pages·2015·0.49 MB·English

by  Patrycja Golinska

AntonievanLeeuwenhoek(2015)108:267–289
DOI10.1007/s10482-015-0502-7
REVIEW PAPER
Endophytic actinobacteria of medicinal plants: diversity
and bioactivity
. . .
Patrycja Golinska Magdalena Wypij Gauravi Agarkar
. .
Dnyaneshwar Rathod Hanna Dahm Mahendra Rai
Received:17April2015/Accepted:4June2015/Publishedonline:21June2015
(cid:2)TheAuthor(s)2015.ThisarticleispublishedwithopenaccessatSpringerlink.com
Abstract Endophytes are the microorganisms that Introduction
exist inside the plant tissues without having any
negative impact on the host plant. Medicinal plants Many types of microbial population such as bacteria
constitutethehugediversityofendophyticactinobac- and fungi have been found to be associated with the
teriaofeconomicalimportance.Thesemicrobeshave internal tissues of plant as endophytes. The term
huge potential to synthesis of numerous novel com- endophyte was coined by De Bary (1866), which
pounds that can be exploited in pharmaceutical, involves the existence of microorganisms inside the
agricultural and other industries. It is of prime infested plant tissues without having negative effects
importance to focus the present research on practical onhostplant(SchulzandBoyle2006).Almostallthe
utilizationofthismicrobialgroupinordertofindout plantshavebeenfoundtobeinfestedwithoneormore
the solutions to the problems related to health, endophytes (Petrini et al. 1992). The microbes are
environmentandagriculture.Anextensivecharacter- producersofgrowthpromotingmetabolites,insectand
izationofdiversepopulationofendophyticactinobac- pest repellents, antimicrobials against plant patho-
teria associated with medicinal plants can provide a gens, protectors in stress conditions and many more
greater insight into the plant-endophyte interactions (Ryaetal.2007;Stanieketal.2008;Raietal.2014a,
andevolutionofmutualism.Inthepresentreview,we b).Theyalsopossessthepotentialtoproduceunique
havediscussedthediversityofendophyticactinobac- secondary metabolites, which can be exploited in
teria of from medicinal plants their multiple pharmaceutical, agricultural and other industries.
bioactivities. Thus, there is a growing interest of researchers in
bioprospecting of endophytic microbial communities
Keywords Actinobacteria(cid:2)Antimicrobialactivity(cid:2) inhabitingtheplantsfromvariousecosystems.
Bioactivecompounds(cid:2)Endophytes(cid:2)Medicinalplants Actinobacteria are Gram-positive typically fila-
mentousbacteria,andisamajorphyluminthedomain
Bacteria (Ludwig and Klenk 2005). Actinobacteria
are widely distributed in both terrestrial and aquatic
P.Golinska(&)(cid:2)M.Wypij(cid:2)D.Rathod(cid:2)H.Dahm
ecosystems.Theyplayimportantrolesindecomposi-
DepartmentofMicrobiology,NicolausCopernicus
University,87100Torun,Poland tion of complex materials from dead plants, animals,
e-mail:[email protected] algae and fungi and in recycling of the nutrients
resulting in humus formation (Sharma 2014). Acti-
G.Agarkar(cid:2)D.Rathod(cid:2)M.Rai
nobacteria are an important and a large group of soil
DepartmentofBiotechnology,SGBAmravatiUniversity,
Amravati444602,Maharashtra,India
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268 AntonievanLeeuwenhoek(2015)108:267–289
microbes with high potential of producing different tissue,geographicalandhabitatdistribution,sampling
bioactive metabolites including antimicrobial, anti- season,surfacesterilants,selectivemediaandculture
cancer and other pharmaceutical compounds (Fiedler conditions(Hallmann2001;Gaieroetal.2013).
et al. 2008; Schulz et al. 2009). These microbes have In general, the isolation protocol involves the
beenthelargestproducersofdifferentantibioticssince collection of plant parts such as leaves, stem, roots
thediscoveryofPenicillinin1928andprovidedthevast thatshouldbeprocessedfreshlyorstoredat4 (cid:3)Cuntil
diversity of antibiotics against many deadly diseases. isolation within 24 h. These explants are washed in
Total number of bioactive metabolites produced by running tap water to remove adhered epiphytes, soil
microorganismsarearound23,000outofwhich10,000 debris or dust particles on the surface, followed by
(45 % of all bioactive metabolites) are produced by surface sterilization using one or more different
actinobacteriaaloneandamongthisgroupofbacteria, surface sterilizing agents. The most commonly used
7600 (76 %) compounds are reported from a single surfacesterilantsincludeethanolandastrongoxidant
genusStreptomyces(Berdy2012).Thissignifiestheir orgeneraldisinfectantlikehouseholdbleach(NaOCl)
primeimportanceintheworldofpharmaceuticals. with 2–5 % (w/v), available chlorine (for 2–4 min).
It is well known that the medicinal plants are the Qin et al. (2008b) and Dochhil et al. (2013) applied
rich sources of precious bioactive compounds. As a combinationof5 %sodiumchlorate(NaClO ),2.5 %
3
consequence of long term association of endophytes sodiumthiosulfate(Na S O ),75 %ethanoland10 %
2 2 3
with such plants, the former may also participate in sodiumbicarbonate(NaHCO )assterilizingagentsto
3
metabolic pathways and enhance its own natural inhibitthegrowthoffungalendophytes.Thestrength
bioactivity or may gain some genetic information to ofsterilizingchemicalsdependsonpermeabilityofthe
producespecificbiologicallyactivecompoundsimilar sample. Otherwise, the internal tissues will be steril-
to the host plant (Stierle et al. 1993; Eyberger et al. ized(Hallmannetal.2006).Alltheexplantsarefinally
2006;Mitchelletal.2010;Kumaretal.2013;Chithra rinsed with sterile distilled water, divided into small
et al. 2014; Rai et al. 2014a, b). Therefore, the fragments (1 cm for steam or roots and 1 cm 2 for
endophytes isolated from medicinal plants are of leaves)andinoculatedonappropriateagarmedium.In
immensesignificance. anothermethod,thesurfacesterilizedplanttissuesare
The beneficial interactions of endophytic acti- macerated and thoroughly homogenized with phos-
nobacteria with plants are being considered as an phate buffer or other suitable liquid medium. This
important area of research. These endophytic acti- suspension is serially diluted as 10-1 to 10-5 and
nobacteria are attractive source of novel bioactive spreadonagarmediuminordertoobtainendophytic
compounds and therefore, many research groups are actinobacteria. The media are supplemented with
involved in the study of their bioactivities and antifungal antibiotics such as nystatin and cyclohex-
industrialapplications.Thepresentreviewisfocused imide(50or100 lg/ml)tosuppressthefungalgrowth.
ontheadvancesinendophyticactinobacteriaisolated After incubation at 26 ± 2 (cid:3)C for 15–30 days, indi-
from medicinal plants including their diversity and vidualcolonieswithcharacteristicactinomycetemor-
broad-spectrumbioactivities. phology emerging out from the plant tissue are
isolated.Thepureculturesoftheisolatesareobtained
bystreakingonfreshmediaplates.Theefficacyofthe
Isolationofendophyticactinobacteria surface sterilization method, resulting from lack of
microbialgrowth,canbeauthenticatedbyinoculating
Different methods have been used by researchers for thelastwashingwaterintothesamemediaplates.
isolationofendophyticactinobacteria.Takahashiand Varioustypesofgrowthmediahavebeendescribed
Omura (2003) emphasized that the diversity of by the authors for the isolation of endophytic
actinobacteria depend mainly on the methods of actinobacteria such as starch casein (Ku¨ster and
isolation. The most frequently employed method for Williams 1964), starch casein nitrate (SCNA), acti-
their detection and enumeration involves isolation nomycetes isolation, soybean (Williams and Davies
from surface-sterilized host plant tissue. Isolation of 1965), chitin-vitamin B (Hayakawa and Nonomura
endophytic actinobacteria depend on various factors, 1987),tapwater-yeastextract(TWYE;Crawfordetal.
which include- host plant species, age and type of 1993) agars and humic acid vitamin B (HV), yeast
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AntonievanLeeuwenhoek(2015)108:267–289 269
extract casamino acid (YECA), synthetic (Mincer leaves (Qin et al. 2009; Gangwar et al. 2014). The
etal.2002),modifiedGausse(Ivantiskayaetal.1978) woody plants conferred far greater diversity of acti-
andglycine–glycerol(Ku¨ster1959)media.Zhaoetal. nobacteria in comparison to herbaceous plants. The
(2011)alsounderlined the need ofusing widerrange high rate of occurrence of actinobacteria in roots as
ofisolationmethodstoacquiremoreknowledgeabout compared to other tissues is very common. This
species diversity of actinobacteria within medicinal underlines the fact that the actinobacteria are natural
plants.AmodifiedmethodemployedbyMachavariani dwellers of soil that easily come in contact with the
etal.(2014)describesthepre-treatmentofleaveswith rootsofplantsandmayformthesymbioticassociation
solutions of heteroauxin and zircon, which helped to with them by entering the plant tissues. The results
isolateandincreasethenumbersofrareactinobacteria obtained by Nimnoi et al. (2010) suggested that
frommedicinalplants. different locations within the plant also differ in the
diversity of actinomycete flora. Strobel and Daisy
(2003)reportedthatthegreaterdiversityofendophytes
Diversityofendophyticactinobacteriainmedicinal is probable to occur in the tropical and temperate
plants regions. Du et al. (2013a) analyzed the endophytic
diversityof37medicinalplantsandreported600 acti-
Current identification and classification of actinobac- nobacteria belonging to 34 genera and 7 unknown
teria are based a polyphasic approach, comprising taxa. The authors depicted that there was no direct
morphological, physiological and molecular studies relationshipbetweenhostplantsandtheirendophytic
(Goodfellowetal.2012)basedoneachtaxonshouldbe flora regarding the utilization of sole carbon source,
described and differentiated from related taxa. The fermentationofcarbonsourcesforproductionofacids
sequencing of highly conserved macromolecules, and enzymes, rather the physiological characteristics
notably 16S rRNA genes, has provided valuable data ofendophyticisolateswererelatedtothegeographical
for constructing phylogenies at and above the genus distributionoftheirhostplants.
level (Ludwig and Klenk 2005). The DNA: DNA The measures of functional biodiversity may be
relatedness, molecular fingerprinting and phenotypic more reliable and powerful than the taxonomic
techniquesaremethodsofchoicefordelineatingtaxaat measures in order to recognize mechanistic basis of
and below the rank of species (Rossello´-Mora and diversity and its effects on the plant-endophyte
Amann 2001). Distinguishing phenotypic differences interactions(Parrentetal.2010).Speciesdistribution
arerequiredforthedescriptionofanewspecies(Wayne and biological diversity of endophytic actinobacteria
et al. 1987). Exploring the diversity of endophytic of medicinal plants are extensively influenced by
actinobacteria is indispensable for screening of bene- ecologicalenvironment(Houetal.2009).El-Shatoury
ficialstrainsandunderstandingtheirecologicalniche. et al. (2013) interpreted that the plant species can be
Endophyticactinobacteriaareabletoassociatewith separated into three clusters representing high, mod-
their host at a very early stage of the plant develop- erate and low endophytic diversity on the basis of
ment (Hasegawa et al. 2006). Minamiyama et al. genericdiversityanalysisofendophytes.Theauthors
(2003) noticed in SEM studies that mycelia of also reported that the endophytes represent high
Streptomycesgalbus,whichwasspreadonthesurface functional diversity, based on forty four different
of the tissue-culture medium in which rhododendron traitsincludingcatabolicandplantgrowthpromotion
seedlings were growing, grew on leaf surfaces and traitsandsuchtraitsmaycharacterizeakeycriteriafor
enteredintotheleaftissuesviastomata.Further,they successful habitation of endophytes within the endo-
also observed that the internal mycelia grew out of sphere. Furthermore, the stress-tolerance traits were
stomata after internal multiplication within host more predictive measure of functional diversity of
leaves. Moreover, the authors observed that within endophyticactinobacteria(El-Shatouryetal.2013).
host leaves, hyphae of S. galbus were present Hasegawa et al. (1978) reported a new genus of
individually or in colonies in intercellular spaces but actinobacteria namely Actinosynnema, from a grass
notinsideepidermalormesophyllcells. blade, which was probably the first report of an
Themaximumendophyticactinobacteriahavebeen actinomycete of plant origin. A comprehensive liter-
recovered from roots followed by stems and least in ature survey has revealed the huge diversity of
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270 AntonievanLeeuwenhoek(2015)108:267–289
endophyticactinobacteriaisolatedfrominteriortissues In2012b,Qinandco-workersstudiedthediversity
ofstem,leavesandrootsofmedicinalplants(Table 1). of endophytic actinobacteria recovered from root,
Taechowisan et al. (2003) studied the diversity of stem and leaf tissues of Maytenus austroyunnanens
actinobacteria residing in medicinal plants based on which was collected from tropical rainforest in
their morphology and the amino acid composition of Xishuangbanna, China. Later the authors concluded
thewhole-cellextractandanalysedthepercentageof thediversityofisolatesbycombinationofcultivation
endophytic actinobacteria recovered from different and culture-independent analysis and based on 16S
explants:64 %isolatesfromroots,29 %fromleaves, rRNA gene sequencing. Further by using different
and6 %fromstemsof36differentplantspecies. selective isolation media and methods total of 312
JansoandCarter(2010)alsoassessedthediversity actinobacteriawereisolatedfromaboveplantswhich
of endophytic actinobacteria, including those from were affiliated with the order Actinomycetales (dis-
medicinal plants, albeit by ribotyping with Pvu II tributed into 21 genera). Based on a protocol for
restriction enzyme to digest the genomic DNA. endophytes enrichment, three 16S rRNA gene clone
Ribotypes were then compared to each other using librarieswere constructedand 84 distinct operational
appropriate software (Janso and Carter 2010). The taxonomic units were identified and they distributed
authors have found that 85 % of 123 isolates studied among the orders Actinomycetales and Acidimicro-
were determinedto beunique at the strain level.The biales,includingeightsubordersandatleast38genera
isolateswereclassifiedtosixfamiliesand17different with a number of rare actinobacteria genera. More-
genera. Streptomyces accounts for the dominant over, six genera from the order Actinomycetales and
genus, which is most commonly isolated as endo- uncultured clones from Acidimicrobiales were found
phyticactinomycete(Qinetal.2009;Zhaoetal.2011; tobeunknownandreportedasfirsttime endophytes.
Shutsrirung et al. 2014; Gangwar et al. 2014) while This study confirms abundant endophytic actinobac-
others include genera such as Micromonospora, terialconsortiumintropicalrainforestnativeplantand
Actinopolyspora,Saccharopolyspora,Nocardia,Oer- suggests that this special habitat still represents an
skovia, Nonomuraea, Streptoverticillium, Microbis- underexplored reservoir of diverse and novel acti-
pora, Streptosporangium, Promicromonospora and nobacteria of potential interest for bioactive com-
Rhodococcus (Verma et al. 2009; Zhao et al. 2011). poundsdiscovery.
Some rare actinobacteria like Dietzia, Blastococcus,
Dactylosporangium, Actinocorallia, Jiangella,
Promicromonospora, Oerskovia, Microtetraspora Bioactivitiesofendophyticactinobacteria
and Intrasporangium were also reported as endo-
phytes (Qin et al. 2009; Zhao et al. 2011; Qin et al. The plant endosphere consists of a large variety of
2012b;El-Shatouryetal.2013).Anovelhalotolerant microbial endophytes, which constitute a complex
actinomycete was isolated from a salt marsh plant micro-ecosystem (El-Shatoury et al. 2013). A vast
Dendranthema indicum collected from the coastal diversity of secondary metabolites in actinobacteria
region of China (Zhang et al. 2013). New species of may occur due to the natural adaptations to environ-
endophytic actinobacteria such as Rhodococcus cer- ment, as apart ofcompetition for common resources
cidiphylli and Saccharopolyspora endophytica were suchasplantmatterinsoil.Ithasbeenobservedthat
isolated from leaf of Cercidiphyllum japonicum (Li thegenesresponsiblefortheproductionofindividual
et al. 2008) and root of Maytenus austroyunnanensis secondary metabolites were found almost always
(Qin et al. 2008a), respectively. Du et al. (2013b) located as a cluster in the genome and referred to as
proposed a new genus and species, Allonocardiopsis biosynthetic gene clusters (Doroghazi and Metcalf
opalescensgen.nov.,sp.nov.,basedonthepolyphasic 2013).Although,there isnodataavailableaboutfull
taxonomic study, within the suborder Streptospo- genomesequencingonactinobacteriafrommedicinal
rangineae.Wangetal.(2008)studiedthediversityof plants it has been known, that whole genomes of
uncultured microbes associated with medicinal plant Streptomyces sp. and non-Streptomyces non-endo-
Mallotusnudiflorusandconcludedthatactinobacteria phyticactinobacteriasuchasStreptomycesavermitilis
were the most dominant microbes, covering about MA-4680 (O¯mura et al. 2001; Ikeda et al. 2003) and
37.7 %ofwholeendophyticisolates. StreptomycescoelicolorA(3)2(Bentleyetal.2002)as
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AntonievanLeeuwenhoek(2015)108:267–289 271
09) kly
0 d
Reference Akshathaetal.(2014) Bascom-Slacketal.(2 Bianetal.(2012b) Bianetal.(2012a) Carusoetal.(2000) Castilloetal.(2002) Castilloetal.(2003) Castilloetal.(2006) Chenetal.(2009) Chenetal.(2011) Contietal.(2012) Dochhiletal.(2013) Duetal.(2013b) El-GendyandEL-Bon(2010)
n,
ari
m
u
o
c
yl
n
e
h
D ylp
d 5 x
Bioactivecompounds ND ND ND ND Paclitaxel MunumbicinsA,B,Can Kakadumycins MunumbicinsE-4andE- ND ND ND Indoleaceticacid(IAA) ND Vanillin, p5,7-dimethoxy-4--metho Saadamycin
e
c
n
e
nts Tissue Stem,leaf,infloresc Stem ND Root Wood/innercorticaltissues Stem Stem ND Innertissue Rootnodules Leaf Root,stem,leaf Fruit Innerhealthytissue
a
pl
isolatedfrommedicinal Hostplant Rauwolfiadensiflora Siparunacrassifolia, Calycophyllumacreanum, Capironadecorticans, Ocotealongifolia, Aspidospermasp, Palicourealongifolia, Monsteraspruceana, Crotonlechleri, Cantuabuxifolia, Banisteriopsiscaapi, Iryantheralaevis, Euchariscyaneosperma Limoniumsinensis Curcumaphaeocaulis Taxusbaccata Kennedianigriscans Grevilleapteridifolia Kennedianigriscans Lobeliaclavatum Elaeagnusangustifolia Spermacoceverticillata Centellaasiatica Loniceramaackii Aplysinafistularis
a
eri
ct
a
Table1Endophyticactinob Speciesofactinomycetes Streptomyceslongisporoflavus, Streptomycessp. Amycolatopsissp., Micromonosporasp., Streptomycessp. Kineococcusendophytica Streptomycesphytohabitans Kitasatosporasp. Streptomycessp.NRRL30562 Streptomycessp.NRRL30566 Streptomycessp.NRRL30562 Pseudonocardiaendophytica Micromonosporasp., Nonomuraeasp., Planotetrasporsp., Pseudonocardiasp. Microbisporasp. Streptomycessp. Allonocardiopsisopalescens Streptomycessp.Hedaya48
123
272 AntonievanLeeuwenhoek(2015)108:267–289
6) 9)
(200 (200 011) 014) 06)
Reference El-Shatouryetal. El-Shatouryetal. Ezraetal.(2004) Gangwaretal.(2 Gangwaretal.(2 Igarashi(2004) Igarashietal.(20
n,
erophore, hore, Novobioci
Bioactivecompounds ND Siderophores,Chitinase Coronamycin ND Hydroxamate-typeofsid Catechol-typeofsiderop Indoleaceticacid(IAA) Fistupyrone 07-Demethylnovobiocin, 005-demethylnovobiocin, 6-Prenylindole, Anicemycin PteridicacidsAandB Clethramycin CedarmycinsAandB Pterocidin
s
part eaf eaf
erial em,l em,l
Tissue Greena ND Stem Root,st Root,st Leaf Stem ND Twig ND
a
Hostplant Artemisiaherbaalba-, Echinopsspinosus, Menthalongifolia, Ballotaundulate Achilleafragrantissim Monsterasp. Aloevera, Mentha, Ocimumsanctum Aloevera, Menthaarvensis, Ocimumsanctum Alliumfistulosum Pteridiumaquilinum ND Cryptomeriajaponica ND
P- P- P-
T T T
Table1continued Speciesofactinomycetes Streptomycessp. Kibdelosporangiumsp., Kitasatosporiasp., Nocardiasp., Nocardioidessp., Promicromonosporasp. Pseudonocardiasp., Streptomycessp. Streptomycessp.MSU-2110 Actinopolysporasp., Micromonosporasp., Saccharopolysporasp., Streptomycessp. Actinopolysporasp., Micromonosporasp., Saccharopolysporasp., Streptomycessp. Streptomycessp.TP-A0569, StreptomyceshygroscopicusA0451, StreptomyceshygroscopicusA0326, Streptomycessp.TP-A0456 StreptomyceshygroscopicusA0451
123
AntonievanLeeuwenhoek(2015)108:267–289 273
4)
1
Reference Igarashietal.(2007) KafurandKhan(2011) Kimetal.(2006) Kumaretal.(2011) Linetal.(2008) LuandShen(2003) LuandShen(2007) Machavarianietal.(20
A)
n
B) ci
y
d m
Bioactivecompounds Lupinacidins ND 6-Alkylsalicylicacids(salaceyinsAan ND Tyrosol(possibleligandforGPR12) Phenylethylaminederivatives, Cyclicdipeptides, Nucleosidesandtheiraglycones, N-acetyltryptamineand Pyrrole-2-carboxylicacid 24-demethyl-bafilomycinC1(Naphtho NaphthomycinK,AandE ND
s
e
ur
af ult
e c
Tissue ND Leaf Stem Twig,l Root ND Tissue Leaf
s,
Hostplant ND Catharanthesroseus Ricinuscommunis Emblicaofficinalis Cistanchesdeserticola Maytenushookeri Maytenushookeri Achilleamillefolium, Aloearborescens, Anthoxantumodoratum, Arctiumlappa, Convallariamajalis, Fragariavesca, Geraniumpretense, Hippophaerhamnoides, Lysimachianummularia, Matricariamatricarioide Melilotusofficinalis, Menthaarvensis, Plantagomajor, Rosacinnamomea, Rubusidaeus, Tanacetumvulgare, Taraxacumofficinale, Trifoliumpretense Urticadioica, Violaodorata
cetes ni nsis MS53
Table1continued Speciesofactinomy Micromonosporalupi StreptomycescavoureAB184264.1 Streptomyceslaceyi Actinomycetessp. Streptomycessp. Streptomycessp.CS Streptomycessp.CS Micromonosporasp., Nocardiopsissp., Streptomycessp.
123
274 AntonievanLeeuwenhoek(2015)108:267–289
2)
Reference MiniPriya(2012) Moussaetal.(2011) Passarietal.(2015) Pujiyantoetal.(201
Cs), Cs),
O O
V e, V
unds( MC-as unds( sidase
Bioactivecompounds Volatileorganiccompo Diffusiblemetabolites Chitinase,Cellulases,C Volatileorganiccompo Diffusiblemetabolites ND Inhibitorofalpha-gluco
er
w
o
fl
ot, m
o e
r st
e stem, leaf,
Tissu Root ND Leaf, Root,
Hostplant Phyllanthusniruri, Withaniasomnifera, Catharanthusroseus, Hemidesmusindicus Achilleafragrantissima, Catharanthusroseus, Artemisiaherbaalba,- A.judaica, Jasoniamontan, Launaesp., Echinopsspinosissimus, Pulicariasp., Centauriasp., Neriumoleander Mirabilisjalapa, Clerodendrumcolebrookianu, Eupatoriumodoratum, Alstoniascholaris Musasuperba Tinosporacrispa Phaleriamacrocarpa, Curcumaaeruginosa, Andrographispaniculata, Caesalpiniasappan, Curcumaxanthoriza, Gynuraprocumbens, Physalisperuviana, Hibiscussabdariffa
s
e
n
e
Table1continued Speciesofactinomycetes Actinomadurasp. Kibdelosporangiumsp., Kitasatosporiasp., Nocardioidessp., Pseudonocardiasp., Streptomycessp., Undefiniedactinomycetes Actinomadurasp., Kibdelosporangiumsp., Kitasatosporiasp., Nocardiasp., Nocardioidessp., Pseudonocardiasp., Streptomycessp., Undefiniedactinomycetes Actinomycetesp., Brevibacteriumsp., Leifsoniasp., Microbacteriumsp., Streptomycessp. Streptomycesolivochromog
123
AntonievanLeeuwenhoek(2015)108:267–289 275
002) 8b) 9) 1) 2a) 2b)
2 0 0 1 1 1
( 0 0 0 0 0
e al. (2 (2 (2 (2 (2
nc et al. al. al. al. al.
ere en et et et et et
Ref Pull Qin Qin Qin Qin Qin
B
ds d
n n
u a
o A
p
m s
co ycin
e m
Bioactiv Celastra ND ND ND ND ND
af
e
l
m,
e
e st
Tissu ND Root Root Root Stem Root,
a,
s
Hostplant Maytenusaquifolia, Putterlickiaretrospino Putterlickiaverrucosa Carexbaccans Scopariadulcis, Maytenusaustroyunnanensis Jatrophacurcas Jatrophacurcas Maytenusaustroyunnanensis
8
Table1continued Speciesofactinomycetes Streptomycessetonii, Streptomycessampsonii, Streptomycessp.Q21, Streptomycessp.MaB-QuH- Glycomycesendophyticus Glycomycesmayteni Glycomycesscopariae Pseudonocardiasichuanensis Nocardioidespanzhihuaensis Actinomadurasp., Amycolatopsissp, Cellulosimicrobiumsp., Glycomycessp., Gordoniasp., Janibactersp., Jiangellasp., Microbacteriumsp., Micromonosporasp., Mycobacteriumsp., Nocardiasp., Nocardiopsissp., Nonomuraeasp., Plantactinosporasp, Polymorphosporasp., Promicromonosporasp., Pseudonocardiasp., Saccharopolysporasp, Streptomycessp, Streptosporangiumsp., Tsukamurellasp.
123
276 AntonievanLeeuwenhoek(2015)108:267–289
7)
0
g, 20
Reference Shenpagametal.(2012) SunaryantoandMahsunah(2013) TaechowisanandLumyon(2003) Taechowisanetal.(2003) Taechowisanetal.(2005, Taechowisanetal.(2006) Vermaetal.(2009) Wangetal.(2014) Zhangetal.(2013)
n,
ari
m
u
o
c
yl
n
ylphe marin
ds methox nylcou
Bioactivecompoun ND ND ND ND p5,7-dimethoxy-4-- 5,7-dimethoxy-4-phe ActinomycinD ND Alkaloids ND
af af af,
e e e
l l l
m, m, m,
af e e e
e le st st st
Tissu Root, Root, Root Root, Root Root Root, Root Stem
Hostplant Azadiractaindica, Ocimumsanctum, Phyllanthusamarus Curcumadomestica, Phaleriamacrocarpa, Isotomalongiflora, Symplocoscochinensis Zingiberofficinale, Alpiniagalanga Zingiberofficinale, Alpiniagalanga Zingiberofficinale Alpiniagalanga Azadirachtaindica Xylocarpusgranatum Dendranthemaindicum
e
a
1 m
1 e
1 h
Table1continued Speciesofactinomycetes Streptomycessp. Streptomycesantibioticus StreptomycesaureofaciensCMUAc130 Microbisporasp, Micromonosporasp., Nocardiasp., Streptomycessp., Unidentifiedisolates StreptomycesaureofaciensCMUAc130 Microbisporasp., Micromonosporasp. Nocardiasp., Streptomycessp.Tc022, Unidentifiedisolates Microbisporasp., Nocardiasp., Sacchromonosporasp., Streptomycessp., Streptosporangiumsp., Streptoverticilliumsp. Jishengellaendophytica161 Saccharopolysporadendrant
123