Abstract
Biological control and plant growth promotion by plant beneficial microbes has been viewed as an alternative to the use of chemical pesticides and fertilizers. Bacteria and fungi that are naturally associated with plants and have a beneficial effect on plant growth by the alleviation of biotic and abiotic stresses were isolated and developed into biocontrol (BCA) and plant growth-promoting agents (PGPA). Actinobacteria are a group of important plant-associated spore-forming bacteria, which have been studied for their biocontrol, plant growth promotion, and interaction with plants. This review summarizes the effects of actinobacteria as BCA, PGPA, and its beneficial associations with plants.
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Abdel-Fattah GM, Mohamedin AH (2000) Interactions between a vesicular–arbuscular mycorrhizal fungus (Glomus intraradices) and Streptomyces coelicolor and their effects on sorghum plants grown in soil amended with chitin of brawn scales. Biol Fertil Soils 32:401–409
Agbessi S, Beausejour J, Dery C, Beaulieu C (2003) Antagonistic properties of two recombinant strains of Streptomyces melanosporofaciens obtained by intraspecific protoplast fusion. Appl Microbiol Biotechnol 62(2–3):233–238
Aldesuquy HS, Mansour FA, Abo-Hamed SA (1998) Effect of the culture filtrates of Streptomyces on growth and productivity of wheat plants. Folia Microbiologia 43(5):465–470
Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63(10):3523–3543
Barona-Gómez F, Lautru S, Francou FX, Leblond P, Pernodet JL, Challis GL (2006) Multiple biosynthetic and uptake systems mediate siderophore-dependent iron acquisition in Streptomyces coelicolor A3(2) and Streptomyces ambofaciens ATCC 23877. Microbiology 152:3355–3366
Beausejour J, Clermont N, Beaulieu C (2003) Effect of Streptomyces melanosporofaciens strain EF-76 and of chitosan on common scab of potato. Plant Soil 256:463–468
Boukaew S, Plubrukam A, Prasertsan P (2013) Effect of volatile substances from Streptomyces philanthi RM-1-138 on growth of Rhizoctonia solani on rice leaf. BioControl 58(4):471–482
Carpenter-Boggs L, Loynacgan TE, Stahl PD (1995) Spore germination of Gigaspora margarita stimulated by volatiles of soil-isolated actinomycetes. Soil Biol Biochem 27:1445–1451
Carrillo-Castañeda G, Juárez Muños J, Peralta-Videa JR, Gomez E, Tiemannb KJ, Duarte-Gardea M, Gardea-Torresdey JL (2002) Alfalfa growth promotion by bacteria grown under iron limiting conditions. Adv Environ Res 6:391–399
Challis GL, Hopwood DA (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci U S A 100(Suppl 2):14555–14561
Chamberlain K, Crawford DL (1999) In vitro and in vivo antagonism of pathogenic turfgrass fungi by Streptomyces hygroscopicus strains YCED9 and WYE53. J Ind Microbiol Biotechnol 23(1):641–646
Chater KF, Biro S, Lee KJ, Palmer T, Schrempf H (2010) The complex extracellular biology of Streptomyces. FEMS Microbiol Rev 34(2):171–198
Conn VM, Walker AR, Franco CMM (2008) Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana. Mol Plant Microbe Interact 21:208–218
Crowley DE, Wang YC, Reid CPP, Szaniszlo PJ (1991) Mechanisms of iron acquisition from siderophores by microorganisms and plants. Plant Soil 130(1–2):179–198
Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47
Davies PJ (2004) Plant hormones: biosynthesis, signal transduction, action! Springer, Berlin
Dimkpa C, Svatos A, Merten D, Büchel G, Kothe E (2008) Hydroxamate siderophores produced by Streptomyces acidiscabies E13 bind nickel and promote growth in cowpea (Vigna unguiculata L.) under nickel stress. Can J Microbiol 54(3):163–172
Dimkpa CO, Merten D, Svatos A, Büchel G, Kothe E (2009) Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J Appl Microbiol 107(5):1687–1696
D’Onofrio A, Crawford JM, Stewart EJ, Witt K, Gavrish E, Epstein S, Clardy J, Lewis K (2010) Siderophores from neighboring organisms promote the growth of uncultured bacteria. Chem Biol 17(3):254–264
Elliott M, Shamoun SF, Sumampong G, James D, Masri S, Varga A (2009) Evaluation of several commercial biocontrol products on European and North American populations of Phytophthora ramorum. Biocontrol Sci Technol 19(10):1007–1021
El-Tarabily KA (2003) An endophytic chitinase-producing isolate of Actinoplanes missouriensis, with potential for biological control of root rot of lupine caused by Plectosporium tabacinum. Aust J Bot 51:257–266
El-Tarabily KA (2008) Promotion of tomato (Lycopersicon esculentum Mill.) plant growth by rhizosphere competent 1-aminocyclopropane-1-carboxylic acid deaminase-producing streptomycetes actinomycetes. Plant Soil 308:161–174
El-Tarabily KA, Sykes ML, Kurtboke ID, Hardy GESJ, Barbosa AM, Dekker RFH (1996) Synergistic effects of a cellulase-producing Micromonospora carbonacea and an antibiotic producing Streptomyces violascens on the suppression of Phytophthora cinnamomi root-rot of Banksia grandis. Can J Bot 74:618–624
El-Tarabily KA, Hardy GESJ, Sivasithamparam K, Hussein AM, Kurtboke DI (1997) The potential for the biological control of cavity-spot disease of carrots, caused by Pythium coloratum, by streptomycete and non-streptomycete actinomycetes. New Phytol 137:495–507
El-Tarabily KA, Soliman MH, Nassar AH, Al-Hassani HA, Sivasithamparam K, McKenna F, Hardy GESJ (2000) Biological control of Sclerotinia minor using a chitinolytic bacterium and actinomycetes. Plant Pathol 49:573–583
El-Tarabily KA, Nassar AH, Hardy GE, Sivasithamparam K (2009) Plant growth promotion and biological control of Pythium aphanidermatum, a pathogen of cucumber, by endophytic actinomycetes. J Appl Microbiol 106(1):13–26
El-Tarabilya KA, Sivasithamparam K (2006) Non-streptomycete actinomycetes as biocontrol agents of soil-borne fungal plant pathogens and as plant growth promoters. Soil Biol Biochem 38:1505–1520
Francis I, Holsters M, Vereecke D (2010) The gram-positive side of plant-microbe interactions. Environ Microbiol 12(1):1–12
Franco-Correaa M, Quintanaa A, Duquea C, Suareza C, Rodrígueza MX, Bareab JM (2010) Evaluation of actinomycete strains for key traits related with plant growth promotion and mycorrhiza helping activities. Appl Soil Ecol 45:209–217
Froes A, Macrae A, Rosa J, Franco M, Souza R, Soares R, Coelho R (2012) Selection of a Streptomyces strain able to produce cell wall degrading enzymes and active against Sclerotinia sclerotiorum. J Microbiol 50(5):798–806
Gadkari D, Morsdorf G, Meyer O (1992) Chemolithoautotrophic assimilation of dinitrogen by Streptomyces thermoautotrophicus UBT1: identification of an unusual N2-fixing system. J Bacteriol 174:6840–6843
Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251(1):1–7
Gregor AK, Klubek B, Varsa EC (2003) Identification and use of actinomycetes for enhanced nodulation of soybean co-inoculated with Bradyrhizobium japonicum. Can J Microbiol 49:483–491
Gurtler H, Pedersen R (1994) Albaflavenone, a sequiterpene ketone with a zizaene skeleton produced by a Streptomycete with a new rope morphology. J Antibiot 47(4):434–439
Hamdali H, Bouizgarne B, Hafidi M, Lebrihi A, Virolle MJ, Ouhdouch Y (2008a) Screening for rock phosphate solubilizing actinomycetes from Moroccan phosphate mines. Appl Soil Ecol 38:12–19
Hamdali H, Hafidi M, Virolle MJ, Ouhdouch Y (2008b) Growth promotion and protection against damping-off of wheat by two rock phosphate solubilizing actinomycetes in a P-deficient soil under greenhouse conditions. Appl Soil Ecol 40:510–517
Hamdali H, Hafidi M, Virolle MJ, Ouhdouch Y (2008c) Rock phosphate-solubilizing actinomycetes: screening for plant growth-promoting activities. World J Microbiol Biotechnol 24:2565–2575
Hasegawa S, Meguro A, Shimizu M, Nishimura T, Kunoh H (2006) Endophytic actinomycetes and their interactions with host plants. Actinomycetologica 20(2):72–81
Herrington PR, Craig JT, Sheridan JE (1987) Methyl vinyl ketone: a volatile fungistatic inhibitor from Streptomyces griseoruber. Soil Biol Biochem 19(5):509–512
Hsu SY (2010) IAA Production by Streptomyces scabies and its role in Plant Microbe Interaction. Cornell University
Hwang BK, Kim BS (1995) In vivo efficacy and in vitro activity of tubercidin, an antibiotic nucleoside, for control of Phytophthora capsici blight in Capsicum annuum. Pestic Sci 44:255–260
Hwang BK, Lee JY, Kim BS, Moon SS (1996) Isolation, structure elucidation, and antifungal activity of a Manumycin-type antibiotic from Streptomyces flaveus. J Agric Food Chem 44:3653–3657
Hwang BK, Lim SW, Kim BS, Lee JY, Moon SS (2001) Isolation and in vivo and in vitro antifungal activity of phenylacetic acid and sodium phenylacetate from Streptomyces humidus. Appl Environ Microbiol 67(8):3739–3745
Ismet A, Vikinesawary S, Paramaswari S, Wong WH, Ward A, Seki T, Fiedler HP, Goodfellow M (2004) Production and chemical characterization of antifungal metabolites from Micromonospora sp. M39 isolated from mangrove rhizosphere soil. World J Microbiol Biotechnol 20:523–528
Isono K, Nagatsu J, Kawashima Y, Suzuki S (1965) Studies on polyoxins, antifungal antibiotics. Part I. Isolation and characterization of polyoxins A and B. Agric Biol Chem 29:848–854
Iwasa T, Higashide E, Yamamoto H, Shibata M (1971) Studies on validamycins, new antibiotics. II Production and biological properties of validamycins A and B. J Antibiot XXIV:107–113
Iwasa T, Suetomi K, Kusuka T (1978) Taxonomic study and fermentation of producing organism and antimicrobial activity of mildiomycin. J Antibiot 31:511–518
Jinhua C, Yang SH, Palaniyandi SA, Han JS, Yoon T-M, Kim T-J, Suh J-W (2010) Azalomycin F complex is an antifungal substance produced by Streptomyces malaysiensis MJM1968 isolated from agricultural soil. J Korean Soc Appl Biol Chem 53(5):545–552
Jobin G, Couture G, Goyer C, Brzezinski R, Beaulieu C (2005) Streptomycete spores entrapped in chitosan beads as a novel biocontrol tool against common scab of potato. Appl Microbiol Biotechnol 68:104–110
Joo GJ (2005) Purification and characterization of an extracellular chitinase from the antifungal biocontrol agent Streptomyces halstedii. Biotechnol Lett 27(19):1483–1486
Joshi MV, Loria R (2007) Streptomyces turgidiscabies possesses a functional cytokinin biosynthetic pathway and produces leafy galls. Mol Plant Microbe Interact 20:751–758
Jurkevitch E, Hadar Y, Chen Y (1986) Remedy of lime-induced chlorosis in peanuts by Pseudomonas sp. siderophores. J Plant Nutr 9:535–545
Khamna S, Yokota A, Lumyong S (2009) Actinomycetes isolated from medicinal plant rhizosphere soils: diversity and screening of antifungal compounds, indole-3-acetic acid and siderophore production. World J Microbiol Biotechnol 25:649–655
Khamna S, Yokota A, Peberdy JF, Lumyong S (2010) Indole-3-acetic acid production by Streptomyces sp. isolated from some Thai medicinal plant rhizosphere soils. Eurasia J Biosci 4:23–32
Kim YS, Kim HM, Chang C, Hwang IC, Oh H, Ahn JS, Kim KD, Hwang BK, Kim BS (2007) Biological evaluation of neopeptins isolated from a Streptomyces strain. Pest Manag Sci 63(12):1208–1214
Kloepper JW, Schroth MN (1978) Plant growth-promoting rhizobacteria on radishes. Paper presented at the Proceedings of the 4th International Conference on Plant Pathogenic Bacteria, Station de Pathologie Vegetale et Phytobacteriologie, INRA, Angers, France
Kono Y, Takeuchi S, Yonehara H (1968) Studies on blasticidin A. J Antibiot XXI:433–438
Leben C, Keitt GW (1954) Antibiotics and plant disease: effects of antibiotics in control of plant diseases. J Agric Food Chem 2:234–239
Lee SY, Tindwa H, Lee YS, Naing KW, Hong SH, Nam Y, Kim KY (2012) Biocontrol of anthracnose in Pepper using chitinase, beta-1,3 glucanase, and 2-furancarboxaldehyde produced by Streptomyces cavourensis SY224. J Microbiol Biotechnol 22(10):1359–1366
Legault GS, Lerat S, Nicolas P, Beaulieu C (2011) Tryptophan regulates thaxtomin A and indole-3-acetic acid production in Streptomyces scabiei and modifies its interactions with radish seedlings. Phytopathology 101(9):1045–1051
Lehr NA, Schrey SD, Bauer R, Hampp R, Tarkka MT (2007) Suppression of plant defence response by a mycorrhiza helper bacterium. New Phytol 174:892–903
Lehr NA, Schrey SD, Hampp R, Tarkka MT (2008) Root inoculation with a forest soil streptomycete leads to locally and systemically increased resistance against phytopathogens in Norway spruce. New Phytol 177:965–976
Li W, Csukai M, Corran A, Crowley P, Solomon PS, Oliver RP (2008) Malayamycin, a new streptomycete antifungal compound, specifically inhibits sporulation of Stagonospora nodorum (Berk) Castell and Germano, the cause of wheat glume blotch disease. Pest Manag Sci 64(12):1294–1302
Li Q, Ning P, Zheng L, Huang J, Li G, Hsiang T (2010) Fumigant activity of volatiles of Streptomyces globisporus JK-1 against Penicillium italicum on Citrus microcarpa. Postharvest Biol Technol 58(2):157–165
Li Q, Ning P, Zheng L, Huang J, Li G, Hsiang T (2012) Effects of volatile substances of Streptomyces globisporus JK-1 on control of Botrytis cinerea on tomato fruit. Biol Control 61(2):113–120
Lin L, Xu X (2013) Indole-3-acetic acid production by endophytic Streptomyces sp. En-1 isolated from medicinal plants. Curr Microbiol 67:209–217
Liu X, Bolla K, Ashforth EJ, Zhuo Y, Gao H, Huang P, Stanley SA, Hung DT, Zhang L (2012) Systematics-guided bioprospecting for bioactive microbial natural products. Antonie Leeuw 101:55–66
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488(7409):86–90
Macagnan D, Romeiro RS, deSouza JT, Pomella AWV (2006) Isolation of actinomycetes and endospore-forming bacteria from the cacao pod surface and their antagonistic activity against the witches’ broom and black pod pathogens. Phytoparasitica 34(2):122–132
Macagnan D, Romeiro RS, Pomella AWV, deSouza JT (2008) Production of lytic enzymes and siderophores, and inhibition of germination of basidiospores of Moniliophthora (ex Crinipellis) perniciosa by phylloplane actinomycetes. Biol Control 47:309–314
Madhaiyan M, Poonguzhali S, Senthilkumar M, Sundaram S, Sa T (2009) Nodulation and plant-growth promotion by methylotrophic bacteria isolated from tropical legumes. Microbiol Res 164(1):114–120
Mahadevan B, Crawford DL (1997) Properties of the chitinase of the antifungal biocontrol agent Streptomyces lydicus WYEC108. Enzyme Microb Technol 20:489–493
Manulis S, Shafrir H, Epstein E, Lichter A, Barash I (1994) Biosynthesis of indole-3-acetic acid via the indole-3-acetamide pathway in Streptomyces spp. Microbiology 140(5):1045–1050
Meschke H, Walter S, Schrempf H (2012) Characterization and localization of prodiginines from Streptomyces lividans suppressing Verticillium dahliae in the absence or presence of Arabidopsis thaliana. Environ Microbiol 14(4):940–592
Moore-Landecker E, Stotzky G (1973) Morphological abnormalities of fungi induced by volatile microbial metabolites. Mycologia 65:519–530
Mugnier J, Mosse B (1987) Spore germination and viability of a vesicular arbuscular mycorrhizal fungus, Glomus mosseae. Trans Brit Mycol Soc 88:411–413
Muller G, Raymond KN (1984) Specificity and mechanism of ferrioxamine-mediated iron transport in Streptomyces pilosus. J Bacteriol 160(1):304–312
Muller G, Matzanke BF, Raymond KN (1984) Iron transport in Streptomyces pilosus mediated by ferrichrome siderophores, rhodotorulic acid, and enantio-rhodotorulic acid. J Bacteriol 160(1):313–318
Nair MG, Chandra A, Thorogood DL (1994) Gopalamicin, an antifungal macrolide produced by soil actinomycete. J Agric Food Chem 42:2308–2310
Neeno-Eckwall EC, Kinkel LL, Schottel JL (2001) Competition and antibiosis in the biological control of potato scab. Can J Microbiol 47:332–340
Nihorimbere V, Ongena M, Smargiassi M, Thonart P (2011) Beneficial effect of the rhizosphere microbial community for plant growth and health. Biotechnol Agron Soc Environ 15(2):327–337
Ntalli NG, Menkissoglu-Spiroudi U (eds)(2011) Pesticides of botanical origin: A promising tool in plant protection. InTech
Oliveira CA, Alves VMC, Marriel IE, Gomes EA, Scotti MR, Carneiro NP, Guimaraes CT, Schaffert RE, Sa NMH (2009) Phosphate solubilizing microorganisms isolated from rhizosphere of maize cultivated in an oxisol of the Brazilian Cerrado Biome. Soil Biol Biochem 41:1782–1787
Ortíz-Castro R, Valencia-Cantero E, López-Bucio J (2008) Plant growth promotion by Bacillus megaterium involves cytokinin signaling. Plant Signal Behav 3:263–265
Pal KK, Gardener BM (2006) Biological control of plant pathogens. Plant Health Instructor. doi:10.1094/PHI-A-2006-1117-02
Palaniyandi SA, Yang SH, Cheng JH, Meng L, Suh JW (2011) Biological control of anthracnose (Colletotrichum gloeosporioides) in yam by Streptomyces sp. MJM5763. J Appl Microbiol 111(2):443–455
Palaniyandi SA, Yang SH, Damodharan K, Suh JW (2013a) Genetic and functional characterization of culturable plant-beneficial actinobacteria associated with yam rhizosphere. J Basic Microbiol. doi:10.1002/jobm.201200531
Palaniyandi SA, Yang SH, Suh JW (2013b) Extracellular proteases from Streptomyces phaeopurpureus ExPro138 inhibit spore adhesion, germination and appressorium formation in Colletotrichum coccodes. J Appl Microbiol 115:207–217
Patten CL, Glick BR (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68(8):3795–3801
Pengnoo A, Kusongwiriyawong C, Nilratana L, Kanjanamaneesathian M (2000) Greenhouse and field trials of the bacterial antagonists in pellet formulations to suppress sheath blight of rice caused by Rhizoctonia solani. BioControl 45(2):245–256
Poole EJ, Bending GD, Whipps JM, Read DJ (2001) Bacteria associated with Pinus sylvestris–Lactarius rufus ectomycorrhizas and their effects on mycorrhiza formation in vitro. New Phytol 151:743–751
Postma J, Clematis F, Nijhuis EH, Someus E (2013) Efficacy of four phosphate-mobilizing bacteria applied with an animal bone charcoal formulation in controlling Pythium aphanidermatum and Fusarium oxysporum f.sp. radicis-lycopersici in tomato. Biol Control. doi:10.1016/j.biocontrol.2013.07.002
Prévost K, Couture G, Shipley B, Brzezinski R, Beaulieu C (2006) Effect of chitosan and a biocontrol streptomycete on field and potato tuber bacterial communities. Biocontrol 51(4):533–546
Pusey PL, Curry EA (2004) Temperature and pomaceous flower age related to colonization by Erwinia amylovora and antagonists. Phytopathology 94(8):901–911
Quecine MC, Araujo WL, Marcon J, Gai CS, Azevedo JL, Pizzirani-Kleiner AA (2008) Chitinolytic activity of endophytic Streptomyces and potential for biocontrol. Lett Appl Microbiol 47(6):486–491
Rai MK, Kalia RK, Singh R, Gangola MP, Dhawan AK (2011) Developing stress tolerant plants through in vitro selection—an overview of the recent progress. Environ Exp Bot 71(1):89–98
Rezzonico F, Stockwell VO, Duffy B (2009) Plant agricultural streptomycin formulations do not carry antibiotic resistance genes. Antimicrob Agents Chemother 53(7):3173–3177
Riedlinger J, Schrey SD, Tarkka MT, Hampp R, Kapur M, Fiedler HP (2006) Auxofuran, a novel metabolite that stimulates the growth of Fly Agaric, is produced by the mycorrhiza helper bacterium Streptomyces strain AcH 505. Appl Environ Microbiol 72:3550–3557
Rodríguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339
Rothrock CS, Gottlieb D (1984) Role of antibiosis in antagonism of Streptomyces hygroscopicus var. geldanus to Rhizoctonia solani in soil. Can J Microbiol 30:1440–1447
Rungin S, Indananda C, Suttiviriya P, Kruasuwan W, Jaemsaeng R, Thamchaipenet A (2012) Plant growth enhancing effects by a siderophore-producing endophytic streptomycete isolated from a Thai jasmine rice plant (Oryza sativa L. cv. KDML105). Antonie Leeuw 102(3):463–472
Sabaou N, Bounaga N, Bounaga D (1983) Actions antibiotique, mycolytique et parsitaire de deux actinomyce’ tes envers Fusarium oxysporum f.sp. albedinis et autres formae speciales. Can J Microbiol 29:194–199
Sabaratnam S, Traquair JA (2002) Formulation of a Streptomyces biocontrol agent for the suppression of Rhizoctonia damping-off in tomato transplants. Biol Control 23(3):245–253
Sadeghi A, Karimi E, Dahaji PA, Javid MG, Dalvand Y, Askari H (2012) Plant growth promoting activity of an auxin and siderophore producing isolate of Streptomyces under saline soil conditions. World J Microbiol Biotechnol 28(4):1503–1509
Samaca DA, Willertc AM, McBrideb MJ, Kinkel LL (2003) Effects of antibiotic-producing Streptomyces on nodulation and leaf spot in alfalfa. Appl Soil Ecol 22:55–66
Schisler DA, Slininger PJ, Behle RW, Jackson MA (2004) Formulation of Bacillus spp. for biological control of plant diseases. Phytopathology 94:1267–1271
Schrey SD, Tarkka MT (2008) Friends and foes: Streptomycetes as modulators of plant disease and symbiosis. Antonie Leeuwenhoek 94:11–19
Schrey SD, Erkenbrack E, Früh E, Fengler S, Hommel K, Horlacher N, Schulz D, Ecke M, Kulik A, Fiedler H-P, Hampp R, Tarkka MT (2012) Production of fungal and bacterial growth modulating secondary metabolites is widespread among mycorrhiza-associated streptomycetes. BMC Microbiol 12:164
Schuhegger R, Ihring A, Gantner S, Bahnweg G, Knappe C, Vogg G, Hutzler P, Schmid M, Breusegem FV, Eberl L, Hartmann A, Langebartels C (2006) Induction of systemic resistance in tomato by N-acyl-l-homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ 29:909–918
Sellstedt A, Richau KH (2013) Aspects of nitrogen-fixing Actinobacteria, in particular free-living and symbiotic Frankia. FEMS Microbiol Lett 342(2):179–186
Shekhar N, Bhattacharya D, Kumar D, Gupta RK (2006) Biocontrol of wood-rotting fungi with Streptomyces violaceusniger XL-2. Can J Microbiol 52(9):805–808
Shih HD, Liu YC, Hsu FL, Mulabagal V, Dodda R, Huang JW (2003) Fungichromin: a substance from Streptomyces padanus with inhibitory effects on Rhizoctonia solani. J Agric Food Chem 51:95–99
Shomura T, Nishizawa N, Iwata M, Yoshida J, Ito M, Amano S, Koyama M, Kojima M, Inouye S (1983) Studies on a new nucleoside antibiotic, dapiramicin. I. Producing organism, assay method and fermentation. J Antibiot 36:1300–1304
Shrivastava S, D’Souza SF, Desai PD (2008) Production of indole-3-acetic acid by immobilized actinomycete (Kitasatospora sp.) for soil applications. Curr Sci 94:1595–1604
Siddikee MA, Chauhan PS, Anandham R, Han GH, Sa T (2010) Isolation, characterization, and use for plant growth promotion under salt stress, of ACC deaminase-producing halotolerant bacteria derived from coastal soil. J Microbiol Biotechnol 20(11):1577–1584
Singh AK, Chhatpar HS (2011) Purification, characterization and thermodynamics of antifungal protease from Streptomyces sp. A6. J Basic Microbiol 51:424–432
Smith J, Putnam A, Nair M (1990) In vitro control of Fusarium diseases of Asparagus officinalis L. with a Streptomyces or its polyene antibiotic, Faeriefungin. J Agric Food Chem 38:1729–1733
Solans M (2007) Discaria trinervis—Frankia symbiosis promotion by saprophytic actinomycetes. J Basic Microbiol 47:243–250
Solans M, Vobis G, Wall LG (2009) Saprophytic actinomycetes promote nodulation in Medicago sativa–Sinorhizobium meliloti symbiosis in the presence of high N. J Plant Growth Regul 28:106–114
Sontag B, Gerlitz M, Paululat T, Rasser HF, Grun-Wollny I, Hansske FG (2006) Oxachelin, a novel iron chelator and antifungal agent from Streptomyces sp. GW9/1258. J Antibiot 59(10):659–663
Srinivasan K, Mathivanan N (2009) Biological control of sunflower necrosis virus disease with powder and liquid formulations of plant growth promoting microbial consortia under field conditions. Biol Control 51(3):395–402
Sturtevant DB, Taller BJ (1989) Cytokinin production by Bradyrhizobium japonicum. Plant Physiol 89:1247–1252
Suleman P, Al-Musallam A, Menezes CA (2002) The effect of biofungicide Mycostop on Ceratocystis radicicola, the causal agent of black scorch on date palm. BioControl 47:207–216
Sutherland ED, Papavizas GC (1991) Evaluation of oospore hyperparasites for the control of Phytophthora crown rot of pepper. J Phytopathol 131:33–39
Sutherland ED, Baker KK, Lockwood JL (1984) Ultrastructure of Phytophthora megasperma f.sp. glycinea oospores parasitised by Actinoplanes missouriensis and Humicola fuscoatra. Trans Brit Mycol Soc 82:726–728
Sziderics A, Rasche F, Trognitz F, Sessitsch A, Wilhelm E (2007) Bacterial endophytes contribute to abiotic stress adaptation in pepper plants (Capsicum annuum L.). Can J Microbiol 53(11):1195–1202
Taechowisan T, Lu C, Shen Y, Lumyong S (2005) Secondary metabolites from endophytic Streptomyces aureofaciens CMUAc130 and their antifungal activity. Microbiology 151:1691–1695
Tapio E, Pohto-Lahdenperä A (1991) Scanning electron microscopy of hyphal interaction between Streptomyces griseoviridis and some plant pathogenic fungi. J Agric Sci Finl 63:435–441
Timmusk S, Nicander B, Granhall U, Tillberg E (1999) Cytokinin production by Paenibacillus polymyxa. Soil Biol Biochem 31:1847–1852
Tokala RK, Strap JL, Jung CM, Crawford DL, Salove MH, Deobald LA, Bailey JF, Morra MJ (2002) Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum). Appl Environ Microbiol 68(5):2161–2171
Trejo-Estrada SR, Paszczynski A, Crawford DL (1998a) Antibiotics and enzymes produced by the biocontrol agent Streptomyces violaceusniger YCED-9. J Ind Microbiol Biotechnol 21:81–85
Trejo-Estrada SR, Sepulveda I, Crawford DL (1998b) In vitro and in vivo antagonism of Streptomyces violaceusniger YCED9 against fungal pathogens of turfgrass. World J Microbiol Biotechnol 14:865–872
Tu JC (1988) Antibiosis of Streptomyces griseus against Colletotrichum lindemuthianum. J Phytopathol 121:97–102
Tylka GL, Hussey RS, Roncadori RW (1991) Axenic germination of vesicular-arbuscular mycorrhizal fungi: effects of selected Streptomyces species. Phytopathology 81:754–759
Upadhyay RS, Rai B (1987) Studies on antagonism between Fusarium udum Butler and root region microflora of pigeon-pea. Plant Soil 101:79–93
Valdés M, Pérez NO, Estrada-de Los Santos P, Caballero-Mellado J, Peña-Cabriales JJ, Normand P, Hirsch AM (2005) Non-Frankia actinomycetes isolated from surface-sterilized roots of Casuarina equisetifolia fix nitrogen. Appl Environ Microbiol 71:460–466
Valencia-Cantero E, Hernández-Calderón E, Velázquez-Becerra C, López-Meza JE, Alfaro-Cuevas R, López-Bucio J (2007) Role of dissimilatory fermentative iron-reducing bacteria in Fe uptake by common bean (Phaseolus vulgaris L.) plants grown in alkaline soil. Plant Soil 291(1–2):263–273
Valois D, Fayad K, Barasubiye T, Garon M, Dery C, Brzezinski R, Beaulieu C (1996) Glucanolytic actinomycetes antagonistic to Phytophthora fragariae var. rubi, the causal agent of Raspberry root rot. Appl Environ Microbiol 62(5):1630–1635
Vereecke D, Messens E, Klarskov K, Bruyn A, Montagu M, Goethals K (1997) Patterns of phenolic compounds in leafy galls of tobacco. Planta 201:342–348
Verma VC, Singh SK, Prakash S (2011) Bio-control and plant growth promotion potential of siderophore producing endophytic Streptomyces from Azadirachta indica A. Juss. J Basic Microbiol 51(5):550–556
Wagner SC (2012) Biological nitrogen fixation. Nature Education Knowledge 3(10):15
Wan M, Li G, Zhang J, Jiang D, Huang H-C (2008) Effect of volatile substances of Streptomyces platensis F-1 on control of plant fungal diseases. Biol Control 46(3):552–559
Wang C, Wang Z, Qiao X, Li Z, Li F, Chen M, Wang Y, Huang Y, Cui H (2013) Antifungal activity of volatile organic compounds from Streptomyces alboflavus TD-1. FEMS Microbiol Lett 341(1):45–51
Xue L, Xue Q, Chen Q, Lin C, Shen G, Zhao J (2013) Isolation and evaluation of rhizosphere actinomycetes with potential application for biocontrol of Verticillium wilt of cotton. Crop Prot 43:231–240
Yamaguchi I (1982) Fungicides for control of rice blast disease. J Pestic Sci 7:307–316
Yamanaka K, Oikawa H, Ogawa HO, Hosono K, Shinmachi F, Takano H, Sakuda S, Beppu T, Ueda K (2005) Desferrioxamine E produced by Streptomyces griseus stimulates growth and development of Streptomyces tanashiensis. Microbiology 151(9):2899–2905
Yamaura M, Uchiumi T, Higashi S, Abe M, Kucho K (2010) Identification of Frankia genes induced under nitrogen-fixing conditions by suppression subtractive hybridization. Appl Environ Microbiol 76:1692–1694
Yuan WM, Crawford DL (1995) Characterization of Streptomyces lydicus WYEC108 as a potential biocontrol agent against fungal root and seed rots. Appl Environ Microbiol 61:3119–3128
Zhao S, Du CM, Tian CY (2012) Suppression of Fusarium oxysporum and induced resistance of plants involved in the biocontrol of cucumber fusarium wilt by Streptomyces bikiniensis HD-087. World J Microbiol Biotechnol 28(9):2919–2927
Zucchi TD, Almeida LG, Dossi FCA, Cônsoli FL (2010) Secondary metabolites produced by Propionicimonas sp. (ENT-18) induce histological abnormalities in the sclerotia of Sclerotinia sclerotiorum. BioControl 55(6):811–819
Acknowledgments
A grant from the Next-Generation BioGreen 21 Program (no. PJ009007), Rural Development Administration, Republic of Korea, supported this work. LZ is an Awardee for National Distinguished Young Scholar Program in China.
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Palaniyandi, S.A., Yang, S.H., Zhang, L. et al. Effects of actinobacteria on plant disease suppression and growth promotion. Appl Microbiol Biotechnol 97, 9621–9636 (2013). https://doi.org/10.1007/s00253-013-5206-1
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DOI: https://doi.org/10.1007/s00253-013-5206-1