Streptomyces sp. LH 4 promotes plant growth and resistance against Sclerotinia sclerotiorum in cucumber via modulation of enzymatic and defense pathways

  • Bong-Gyu Mun
  • Won-Hee Lee
  • Sang-Mo Kang
  • Sang-Uk Lee
  • Seok-Min Lee
  • Dong Yeol Lee
  • Muhammad Shahid
  • Byung-Wook YunEmail author
  • In-Jung LeeEmail author
Regular Article



In the soil ecosystem, microbial diversity exists and these diverse organisms interact with plant roots and influence the physicochemical properties of plants. Some of these diverse microorganisms can cause diseases or can provide beneficial interactions with plants. Rhizobacteria are well-known beneficial microorganism that colonize the plant root zone (rhizosphere) and are referred to as plant growth-promoting rhizobacteria (PGPR) that contribute to the promotion of plant growth either directly or indirectly. PGPRs are also known for their biocontrol abilities. Sclerotinia sclerotiorum, an Ascomycetous soil inhabiting fungus, causes white rot disease in cucumbers. This disease results in the loss of millions of dollars annually. The current study was conducted to isolate naturally occurring soil inhabiting bacteria that may promote plant growth under diseased conditions and also antagonize the pathogen.


The isolated LH4 strain was identified as Streptomyces sp. by 16S rRNA sequencing and phylogenetic analysis. The plant growth promoting effects and the antifungal antagonistic activities against Sclerotinia sclerotiorum were confirmed by measuring enzymatic activity of LH4 and demonstration in planta. In addition, Streptomyces sp. LH4 pure culture application exhibited significant growth inhibition of S. sclerotiorum in cucumber. Analysis of the major hormones related to pathogen defense; the jasmonic acid, and salicylic acid, showed that the modulation of these two hormones increased disease resistance in cucumber.


The present study suggests a possible dual role of Streptomyces sp. LH4 as functional material for bio-fertilizer and biocontrol against pathogens.


Streptomyces sp. Sclerotinia sclerotiorum. PGPR. Antifungal agents. Plant hormones. Cucumber 



Plant growth-promoting rhizobacteria


salicylic acid


jasmonic acid




abscisic acid




National Center for Biotechnology Information


Scanning Electron Microscopy


National Botanical Research Institute’s P growth


carboxymethyl cellulose


potato dextrose agar


Authors’ contributions

WHL, BGM and SMK designed the study and performed main experiments. SUL, SML, MS, WHL and DYL analyzed the data and performed supplementary experiments. BGM, WHL and MS wrote the manuscript and revised manuscript. BWY and IJL supervised the overall experiment and revised the manuscript. All authors read and approved the final manuscript.

Funding information

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2017R1D1A1B04035601) to In-Jung Lee and by a grant from the Next-Generation BioGreen 21 Program (Grant No. PJ01367901), Rural Development Administration, Republic of Korea to Bong-Gyu Mun.

Compliance with ethical standards

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Supplementary material

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ESM 1 Supplementary Fig. 1 Phylogenetic tree analysis of Streptomyces sp. strain LH4. 16S rRNA sequences were used from related taxa for phylogenetic tree analysis using MEGA (v7.01) (JPG 1092 kb)
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  1. Abd El Rahman T, El Oirdi M, Gonzalez-Lamothe R, Bouarab K (2012) Necrotrophic pathogens use the salicylic acid signaling pathway to promote disease development in tomato. Mol Plant-Microbe Interact 25(12):1584–1593. CrossRefGoogle Scholar
  2. Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. Journal of King Saud University-Science 26(1):1–20CrossRefGoogle Scholar
  3. Al-Askar A (2012) Microbiological studies on the in vitro inhibitory effect of Streptomyces collinus albescens against some phytopathogenic fungi. Afr J Microbiol Res 6(13):3277–3283Google Scholar
  4. Aleandri MP, Chilosi G, Bruni N, Tomassini A, Vettraino AM, Vannini A (2015) Use of nursery potting mixes amended with local Trichoderma strains with multiple complementary mechanisms to control soil-borne diseases. Crop Prot 67:269–278CrossRefGoogle Scholar
  5. Alkooranee JT, Aledan TR, Ali AK, Lu GY, Zhang XK, Wu JS et al (2017) Detecting the hormonal pathways in oilseed rape behind induced systemic resistance by Trichoderma harzianum TH12 to Sclerotinia sclerotiorum. PLoS One 12(1). PubMedPubMedCentralCrossRefGoogle Scholar
  6. Ansary WR, Prince FRK, Haque E, Sultana F, West HM, Rahman M et al (2018) Endophytic Bacillus spp. from medicinal plants inhibit mycelial growth of Sclerotinia sclerotiorum and promote plant growth. Zeitschrift für Naturforschung C 73(5–6):247–256CrossRefGoogle Scholar
  7. Baniasadi F, Bonjar GS, Baghizadeh A, Nik AK, Jorjandi M, Aghighi S, Farokhi PR (2009) Biological control of Sclerotinia sclerotiorum, causal agent of sunflower head and stem rot disease, by use of soil borne actinomycetes isolates. Am J Agric Biol Sci 4(2):146–151CrossRefGoogle Scholar
  8. Beneduzi A, Ambrosini A, Passaglia LMP (2012) Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genetics and Molecular Biology 35(4):1044–1051. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bertrand H, Nalin R, Bally R, Cleyet-Marel JC (2001) Isolation and identification of the most efficient plant growth-promoting bacteria associated with canola (Brassica napus). Biology and Fertility of Soils 33(2):152–156. CrossRefGoogle Scholar
  10. Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World Journal of Microbiology & Biotechnology 28(4):1327–1350. CrossRefGoogle Scholar
  11. Bitsadze N, Siebold M, Koopmann B, von Tiedemann A (2015) Single and combined colonization of Sclerotinia sclerotiorum sclerotia by the fungal mycoparasites Coniothyrium minitans and Microsphaeropsis ochracea. Plant Pathol 64(3):690–700CrossRefGoogle Scholar
  12. Bolton MD, Thomma BPHJ, Nelson BD (2006) Sclerotinia sclerotiorum (lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Mol Plant Pathol 7(1):1–16. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Cao L, Qiu Z, You J, Tan H, Zhou S (2004) Isolation and characterization of endophytic Streptomyces strains from surface-sterilized tomato (Lycopersicon esculentum) roots. Lett Appl Microbiol 39(5):425–430PubMedCrossRefPubMedCentralGoogle Scholar
  14. Cecagno R, Fritsch TE, Schrank IS (2015) The plant growth-promoting Bacteria Azospirillum amazonense: genomic versatility and Phytohormone pathway. Biomed Research International. CrossRefGoogle Scholar
  15. Cheng G, Huang Y, Yang H, Liu F (2014) Streptomyces felleus YJ1: potential biocontrol agents against the sclerotinia stem rot (Sclerotinia sclerotiorum) of oilseed rape. Journal of Agricultural Science (Toronto) 6(4):91–98CrossRefGoogle Scholar
  16. Chitrampalam P, Figuli P, Matheron ME, Subbarao K, Pryor BM (2008) Biocontrol of lettuce drop caused by Sclerotinia sclerotiorum and S. minor in desert agroecosystems. Plant Dis 92(12):1625–1634PubMedCrossRefPubMedCentralGoogle Scholar
  17. Compant S, Duffy B, Nowak J, Clement C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71(9):4951–4959. CrossRefPubMedPubMedCentralGoogle Scholar
  18. Conn V, Walker A, Franco C (2008) Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana. Mol Plant-Microbe Interact 21(2):208–218PubMedCrossRefPubMedCentralGoogle Scholar
  19. Dalili A, Bakhtiari S, Barari H, Aldaghi M (2015) Effect of some fungicides against the growth inhibition of Sclerotinia sclerotiorum mycelial compatibility groups. Journal of plant protection research 55(4):354–361CrossRefGoogle Scholar
  20. de Vasconcellos RLF, Cardoso EJBN (2009) Rhizospheric streptomycetes as potential biocontrol agents of Fusarium and Armillaria pine rot and as PGPR for Pinus taeda. Biocontrol 54(6):807–816. CrossRefGoogle Scholar
  21. Dinesh R, Anandaraj M, Kumar A, Bini YK, Subila KP, Aravind R (2015) Isolation, characterization, and evaluation of multi-trait plant growth promoting rhizobacteria for their growth promoting and disease suppressing effects on ginger. Microbiol Res 173:34–43. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Dodd IC, Zinovkina NY, Safronova VI, Belimov AA (2010) Rhizobacterial mediation of plant hormone status. Ann Appl Biol 157(3):361–379. CrossRefGoogle Scholar
  23. El-Tarabily KA (2008) Promotion of tomato (Lycopersicon esculentum mill.) plant growth by rhizosphere competent 1-aminocyclopropane-1-carboxylic acid deaminase-producing streptomycete actinomycetes. Plant Soil 308(1–2):161–174CrossRefGoogle Scholar
  24. El-Tarabily K, Nassar A, Hardy GSJ, Sivasithamparam K (2009) Plant growth promotion and biological control of Pythium aphanidermatum, a pathogen of cucumber, by endophytic actinomycetes. J Appl Microbiol 106(1):13–26PubMedCrossRefPubMedCentralGoogle Scholar
  25. El-Tarabily K, Soliman M, Nassar A, Al-Hassani H, Sivasithamparam K, McKenna F, Hardy GSJ (2000) Biological control of Sclerotinia minor using a chitinolytic bacterium and actinomycetes. Plant Pathol 49(5):573–583CrossRefGoogle Scholar
  26. Errakhi R, Bouteau F, Lebrihi A, Barakate M (2007) Evidences of biological control capacities of Streptomyces spp. against Sclerotium rolfsii responsible for damping-off disease in sugar beet (Beta vulgaris L.). World J Microbiol Biotechnol 23(11):1503–1509CrossRefGoogle Scholar
  27. Evangelista-Martínez Z (2014) Isolation and characterization of soil Streptomyces species as potential biological control agents against fungal plant pathogens. World J Microbiol Biotechnol 30(5):1639–1647PubMedCrossRefPubMedCentralGoogle Scholar
  28. Fernando W, Nakkeeran S, Zhang Y, Savchuk S (2007) Biological control of Sclerotinia sclerotiorum (lib.) de Bary by Pseudomonas and Bacillus species on canola petals. Crop Prot 26(2):100–107CrossRefGoogle Scholar
  29. Franco-Correa M, Quintana A, Duque C, Suarez C, Rodríguez MX, Barea J-M (2010) Evaluation of actinomycete strains for key traits related with plant growth promotion and mycorrhiza helping activities. Appl Soil Ecol 45(3):209–217CrossRefGoogle Scholar
  30. Gerlagh M, Goossen-van de Geijn HM, Fokkema NJ, Vereijken PFG (1999) Long-term biosanitation by application of Coniothyrium minitans on Sclerotinia sclerotiorum infected crops. Phytopathology 89(2):141–147. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Getha K, Vikineswary S (2002) Antagonistic effects of Streptomyces violaceusniger strain G10 on Fusarium oxysporum f. sp. cubense race 4: indirect evidence for the role of antibiosis in the antagonistic process. J Ind Microbiol Biotechnol 28(6):303–310PubMedCrossRefPubMedCentralGoogle Scholar
  32. González-Franco AC, Robles-Hernandez R (2009) Actinomycetes as biological control agents of phytopathogenic fungi. Tecnociencia Chihuahua 3(2):64–73Google Scholar
  33. Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Gowda CLL, Krishnamurthy L (2015a) Plant growth promoting rhizobia: challenges and opportunities. 3. Biotech 5(4):355–377. CrossRefGoogle Scholar
  34. Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Rathore A, Varshney RK (2015b). The extent of grain yield and plant growth enhancement by plant growth-promoting broad-spectrum Streptomyces sp in chickpea. Springerplus, 4. Doi: 10.1186/s40064-015-0811-3Google Scholar
  35. Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Varshney R (2015c) Evaluation of Streptomyces sp. obtained from herbal vermicompost for broad spectrum of plant growth-promoting activities in chickpea. Org Agric 5(2):123–133CrossRefGoogle Scholar
  36. Gopalakrishnan S, Srinivas V, Vidya MS, Rathore A (2013) Plant growth-promoting activities of Streptomyces spp. in sorghum and rice. Springerplus (2, 1):574Google Scholar
  37. Gopalakrishnan S, Vadlamudi S, Bandikinda P, Sathya A, Vijayabharathi R, Rupela O, Kudapa H, Katta K, Varshney RK (2014) Evaluation of Streptomyces strains isolated from herbal vermicompost for their plant growth-promotion traits in rice. Microbiol Res 169(1):40–48PubMedCrossRefPubMedCentralGoogle Scholar
  38. Gouda S, Kerry RG, Das G, Paramithiotis S, Shin HS, Patra JK (2017). Revitalization of plant growth promoting rhizobacteria for sustainable development in agriculture. Microbiol ResGoogle Scholar
  39. Gracia-Garza J, Reeleder R, Paulitz T (1997) Degradation of sclerotia of Sclerotinia sclerotiorum by fungus gnats (Bradysia coprophila) and the biocontrol fungi Trichoderma spp. Soil Biol Biochem 29(2):123–129CrossRefGoogle Scholar
  40. Hamdia ABE, Shaddad MAK, Doaa MM (2004) Mechanisms of salt tolerance and interactive effects of Azospirillum brasilense inoculation on maize cultivars grown under salt stress conditions. Plant Growth Regul 44(2):165–174CrossRefGoogle Scholar
  41. Hausler RE, Ludewig F, Krueger S (2014) Amino acids - A life between metabolism and signaling. Plant Sci 229:225–237. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Heng J, Shah U, Rahman N, Shaari K, Hamzah H (2015) Streptomyces ambofaciens S2—a potential biological control agent for colletotrichumgleosporioides the causal agent for anthracnose in red chilli fruits. J Plant Pathol Microbiol S 1:2Google Scholar
  43. Hildebrandt TM, Nesi AN, Araujo WL, Braun HP (2015) Amino acid catabolism in plants. Mol Plant 8(11):1563–1579. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Igarashi Y, Iida T, Yoshida R, Furumai T (2002) Pteridic acids A and B, novel plant growth promoters with auxin-like activity from Streptomyces hygroscopicus TP-A0451. The Journal of antibiotics 55(8):764–767PubMedCrossRefPubMedCentralGoogle Scholar
  45. Inderjit, van der Putten, W. H. (2010) Impacts of soil microbial communities on exotic plant invasions. Trends Ecol Evol 25(9):512–519. CrossRefGoogle Scholar
  46. Jones EE, Rabeendran N, Stewart A (2014) Biocontrol of Sclerotinia sclerotiorum infection of cabbage by Coniothyrium minitans and Trichoderma spp. Biocontrol Sci Tech 24(12):1363–1382CrossRefGoogle Scholar
  47. Joo G-J (2005) Production of an anti-fungal substance for biological control of Phytophthora capsici causing phytophthora blight in red-peppers by Streptomyces halstedii. Biotechnol Lett 27(3):201–205PubMedCrossRefPubMedCentralGoogle Scholar
  48. Kamensky M, Ovadis M, Chet I, Chernin L (2003) Soil-borne strain IC14 of Serratia plymuthica with multiple mechanisms of antifungal activity provides biocontrol of Botrytis cinerea and Sclerotinia sclerotiorum diseases. Soil Biol Biochem 35(2):323–331CrossRefGoogle Scholar
  49. Kamilova F, Validov S, Azarova T, Mulders I, Lugtenberg B (2005) Enrichment for enhanced competitive plant root tip colonizers selects for a new class of biocontrol bacteria. Environ Microbiol 7(11):1809–1817. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Karimi E, Sadeghi A, Abbaszadeh Dahaji P, Dalvand Y, Omidvari M, Kakuei Nezhad M (2012) Biocontrol activity of salt tolerant Streptomyces isolates against phytopathogens causing root rot of sugar beet. Biocontrol Sci Tech 22(3):333–349CrossRefGoogle Scholar
  51. Karlidag H, Yildirim E, Turan M, Pehluvan M, Donmez F (2013) Plant growth-promoting Rhizobacteria mitigate deleterious effects of salt stress on strawberry plants (Fragaria xananassa). HortScience 48(5):563–567CrossRefGoogle Scholar
  52. Khair A (2011) In vitro antifungal activity of Streptomyces spororaveus RDS28 against some phytopathogenic fungi. Afr J Agric Res 6(12):2835–2842Google Scholar
  53. Kim AY, Shahzad R, Kang SM, Khan AL, Lee SM, Park YG et al (2017) Paenibacillus terrae AY-38 resistance against Botrytis cinerea in Solanum lycopersicum L.plants through defence hormones regulation. J Plant Interact 12(1):244–253. CrossRefGoogle Scholar
  54. Kohler J, Hernandez JA, Caravaca F, Roldan A (2008) Plant-growth-promoting rhizobacteria and arbuscular mycorrhizal fungi modify alleviation biochemical mechanisms in water-stressed plants. Funct Plant Biol 35(2):141–151. CrossRefGoogle Scholar
  55. Kokalis-Burelle N, Kloepper JW, Reddy MS (2006) Plant growth-promoting rhizobacteria as transplant amendments and their effects on indigenous rhizosphere microorganisms. Appl Soil Ecol 31(1–2):91–100. CrossRefGoogle Scholar
  56. Kumar P, Dubey RC, Maheshwari DK (2012) Bacillus strains isolated from rhizosphere showed plant growth promoting and antagonistic activity against phytopathogens. Microbiol Res 167(8):493–499. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Lavakush, Yadav, J., Verma, J.P, Jaiswal, D. K., & Kumar, A. (2014). Evaluation of PGPR and different concentration of phosphorus level on plant growth, yield and nutrient content of rice (Oryza sativa). Ecol Eng, 62, 123–128. doi: CrossRefGoogle Scholar
  58. Li GQ, Huang HC, Acharya S (2003) Antagonism and biocontrol potential of Ulocladium atrum on Sclerotinia sclerotiorum. Biol Control 28(1):11–18CrossRefGoogle Scholar
  59. Liang J, Xue Q, Niu X, Li Z (2005) Root colonization and effects of seven strains of actinomycetes on leaf PAL and PPO activities of capsicum. Acta Botan Boreali-Occiden Sin 25(10):2118–2123Google Scholar
  60. Lim JH, Kim SD (2013) Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper. Plant Pathol J 29(2):201–208. CrossRefPubMedPubMedCentralGoogle Scholar
  61. Lobo Júnior M, Abreu M d (2000) Inibição do crescimento micelial de Sclerotinia sclerotiorum por metabólitos voláteis produzidos por alguns antagonistas em diferentes temperaturas e pH's. Ciência e Agrotecnologia, Lavras 24(2):521–526Google Scholar
  62. Lucy M, Reed E, Glick BR (2004) Applications of free living plant growth-promoting rhizobacteria. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology 86(1):1–25. CrossRefGoogle Scholar
  63. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting Rhizobacteria. Annu Rev Microbiol 63:541–556. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Ma Y, Oliveira RS, Nai F, Rajkumar M, Luo Y, Rocha I, Freitas H (2015) The hyperaccumulator sedum plumbizincicola harbors metal-resistant endophytic bacteria that improve its phytoextraction capacity in multi-metal contaminated soil. J Environ Manag 156:62–69CrossRefGoogle Scholar
  65. Mahadevan B, Crawford DL (1997) Properties of the chitinase of the antifungal biocontrol agent Streptomyces lydicus WYEC108. Enzym Microb Technol 20(7):489–493CrossRefGoogle Scholar
  66. Majeed A, Abbasi MK, Hameed S, Imran A, Rahim N (2015) Isolation and characterization of plant growth-promoting rhizobacteria from wheat rhizosphere and their effect on plant growth promotion. Frontiers in Microbiology 6.
  67. Maldonado MC, Orosco CEF, Gordillo M, Navarro AR (2010). In vivo and in vitro antagonism of Streptomyces sp. RO3 against Penicillium digitatum and Geotrichum candidumGoogle Scholar
  68. Matroudi S, Zamani M (2009). Antagonistic effects of three species of Trichoderma sp. on Sclerotinia sclerotiorum, the causal agent of canola stem rot. Egyptian Journal of Biology, 11(1)Google Scholar
  69. McCloud ES, Baldwin IT (1997) Herbivory and caterpillar regurgitants amplify the wound-induced increases in jasmonic acid but not nicotine in Nicotiana sylvestris. Planta 203(4):430–435. CrossRefGoogle Scholar
  70. Meena H, Ahmed MA, Prakash P (2015) Amelioration of heat stress in wheat, Triticum aestivum by PGPR (Pseudomonas aeruginosa strain 2CpS1). Bioscience Biotechnology Research Communications 8(2):171–174Google Scholar
  71. Meguro A, Ohmura Y, Hasegawa S, Shimizu M, Nishimura T, Kunoh H (2006) An endophytic actinomycete, Streptomyces sp. MBR-52, that accelerates emergence and elongation of plant adventitious roots. Actinomycetologica 20(1):1–9CrossRefGoogle Scholar
  72. Mendis HC, Thomas VP, Schwientek P, Salamzade R, Chien JT, Waidyarathne P et al (2018) Strain-specific quantification of root colonization by plant growth promoting rhizobacteria Bacillus firmus I-1582 and Bacillus amyloliquefaciens QST713 in non-sterile soil and field conditions. PLoS One 13(2):e0193119. CrossRefPubMedPubMedCentralGoogle Scholar
  73. Moe LA (2013) Amino acids in the Rhizosphere: from plants to microbes. Am J Bot 100(9):1692–1705. CrossRefPubMedPubMedCentralGoogle Scholar
  74. Nimnoi P, Pongsilp N, Lumyong S (2014) Co-inoculation of soybean (Glycine max) with actinomycetes and Bradyrhizobium japonicum enhances plant growth, nitrogenase activity and plant nutrition. J Plant Nutr 37(3):432–446CrossRefGoogle Scholar
  75. Ningthoujam S, Sanasam S, Tamreihao K, Nimaich S (2009) Antagonistic activities of local actinomycete isolates against rice fungal pathogens. Afr J Microbiol Res 3(11):737–742Google Scholar
  76. Novakova M, Sasek V, Dobrev PI, Valentova O, Burketova L (2014) Plant hormones in defense response of Brassica napus to Sclerotinia sclerotiorum - reassessing the role of salicylic acid in the interaction with a necrotroph. Plant Physiol Biochem 80:308–317. CrossRefPubMedPubMedCentralGoogle Scholar
  77. Onaran A, Yanar Y (2011) Screening bacterial species for antagonistic activities against the Sclerotinia sclerotiorum (lib.) De Bary causal agent of cucumber white mold disease. Afr J Biotechnol 10(12):2223–2229Google Scholar
  78. Palaniyandi SA, Yang SH, Zhang L, Suh J-W (2013) Effects of actinobacteria on plant disease suppression and growth promotion. Appl Microbiol Biotechnol 97(22):9621–9636PubMedCrossRefPubMedCentralGoogle Scholar
  79. Pandey C, Bajpai VK, Negi YK, Rather IA, Maheshwari D (2018a). Effect of plant growth promoting Bacillus spp. on nutritional properties of Amaranthus hypochondriacus grains. Saudi Journal of Biological Sciences Google Scholar
  80. Pandey C, Bajpai VK, Negi YK, Rather IA, Maheshwari DK (2018b) Effect of plant growth promoting Bacillus spp. on nutritional properties of Amaranthus hypochondriacus grains. Saudi J Biol Sci 25(6):1066–1071. CrossRefPubMedPubMedCentralGoogle Scholar
  81. Patil HJ, Srivastava AK, Singh DP, Chaudhari BL, Arora DK (2011) Actinomycetes mediated biochemical responses in tomato (Solanum lycopersicum) enhances bioprotection against Rhizoctonia solani. Crop Prot 30(10):1269–1273CrossRefGoogle Scholar
  82. Pereira JCR, Chaves G, Zambolim L, Matsuoka K, Silva-acuña R (1996). Controle integrado de Sclerotinia sclerotiorum. Embrapa Amazônia Ocidental-Artigo em periódico indexado (ALICE)Google Scholar
  83. Perez-Montano F, Alias-Villegas C, Bellogin RA, del Cerro P, Espuny MR, Jimenez-Guerrero I et al (2014) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Res 169(5–6):325–336. CrossRefPubMedPubMedCentralGoogle Scholar
  84. Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM (2012) Hormonal modulation of plant immunity. Annual Review of Cell and Developmental Biology, Vol 28(28):489–521. CrossRefGoogle Scholar
  85. Porcel R, Zamarreno AM, Garcia-Mina JM, Aroca R (2014). Involvement of plant endogenous ABA in Bacillus megaterium PGPR activity in tomato plants. Bmc Plant Biology, 14. Doi:Artn 36 10.1186/1471-2229-14-36Google Scholar
  86. Prapagdee B, Kuekulvong C, Mongkolsuk S (2008) Antifungal potential of extracellular metabolites produced by Streptomyces hygroscopicus against phytopathogenic fungi. Int J Biol Sci 4(5):330–337PubMedPubMedCentralCrossRefGoogle Scholar
  87. Pratelli R, Pilot G (2014) Regulation of amino acid metabolic enzymes and transporters in plants. J Exp Bot 65(19):5535–5556. CrossRefPubMedPubMedCentralGoogle Scholar
  88. Rhee K-H (2003) Purification and identification of an antifungal agent from Streptomyces sp. KH-614 antagonistic to rice blast fungus, Pyricularia oryzae. Journal of Microbiology and Biotechnology 13(6):984–988Google Scholar
  89. Rothrock CS, Gottlieb D (1984) Role of antibiosis in antagonism of Streptomyces hygroscopicus var. geldanus to Rhizoctonia solani in soil. Can J Microbiol 30(12):1440–1447CrossRefGoogle Scholar
  90. 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 Van Leeuwenhoek 102(3):463–472PubMedCrossRefPubMedCentralGoogle Scholar
  91. Ryu CM, Hu CH, Locy RD, Kloepper JW (2005) Study of mechanisms for plant growth promotion elicited by rhizobacteria in Arabidopsis thaliana. Plant Soil 268(1–2):285–292. CrossRefGoogle Scholar
  92. Sangmanee P, Bhromsiri A, Akarapisan A (2009). The potential of endophytic actinomycetes,(Streptomyces sp.) for the biocontrol of powdery mildew disease in sweet pea (Pisum sativum). As J Food Ag-Ind, 93, e8Google Scholar
  93. Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proceedings of the National Academy of Sciences of the United States of America 97(21):11655–11660. CrossRefPubMedPubMedCentralGoogle Scholar
  94. Schirmbock M, Lorito M, Wang YL, Hayes CK, Arisanatac I, Scala F et al (1994) Parallel formation and synergism of hydrolytic enzymes and Peptaibol antibiotics, molecular mechanisms involved in the antagonistic action of Trichoderma-Harzianum against Phytopathogenic Fungi. Appl Environ Microbiol 60(12):4364–4370PubMedPubMedCentralCrossRefGoogle Scholar
  95. Seskar M, Shulaev V, Raskin I (1998) Endogenous methyl salicylate in pathogen-inoculated tobacco plants. Plant Physiology 116(1):387–392. CrossRefPubMedCentralGoogle Scholar
  96. Shaharoona B, Arshad M, Zahir ZA (2006) Effect of plant growth promoting rhizobacteria containing ACC-deaminase on maize (Zea mays L.) growth under axenic conditions and on nodulation in mung bean (Vigna radiata L.). Lett Appl Microbiol 42(2):155–159. CrossRefPubMedPubMedCentralGoogle Scholar
  97. Shahzad R, Khan AL, Bilal S, Asaf S, Lee IJ (2017) Plant growth-promoting endophytic bacteria versus pathogenic infections: an example of Bacillus amyloliquefaciens RWL-1 and Fusarium oxysporum f. sp lycopersici in tomato. Peerj, 5. Doi:ARTN e310710.7717/peerj.3107Google Scholar
  98. Singh PP, Shin YC, Park CS, Chung YR (1999) Biological control of Fusarium wilt of cucumber by chitinolytic bacteria. Phytopathology 89(1):92–99PubMedCrossRefPubMedCentralGoogle Scholar
  99. Smolińska U, Kowalska B (2018) Biological control of the soil-borne fungal pathogen Sclerotinia sclerotiorum –– a review. J Plant Pathol 100(1):1–12. CrossRefGoogle Scholar
  100. Steindorff AS, Ramada MHS, Coelho ASG, Miller RNG, Pappas GJ, Ulhoa CJ, Noronha EF (2014) Identification of mycoparasitism-related genes against the phytopathogen Sclerotinia sclerotiorum through transcriptome and expression profile analysis in Trichoderma harzianum. BMC Genomics 15(1):204PubMedPubMedCentralCrossRefGoogle Scholar
  101. Tamreihao K, Ningthoujam DS, Nimaichand S, Singh ES, Reena P, Singh SH, Nongthomba U (2016) Biocontrol and plant growth promoting activities of a Streptomyces corchorusii strain UCR3-16 and preparation of powder formulation for application as biofertilizer agents for rice plant. Microbiol Res 192:260–270. CrossRefPubMedPubMedCentralGoogle Scholar
  102. Tokala RK, Strap JL, Jung CM, Crawford DL, Salove MH, Deobald LA, Bailey JF, Morra M (2002) Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum). Appl Environ Microbiol 68(5):2161–2171PubMedPubMedCentralCrossRefGoogle Scholar
  103. Tozlu E, Mohammadi P, Kotan MS, Nadaroglu H, Kotan R (2016) Biological control of Sclerotinia sclerotiorum (lib.) de Bary, the causal agent of white Mould disease in red cabbage, by some Bacteria. Plant Protection Science 52(3):188–198. CrossRefGoogle Scholar
  104. Trutmann P, Keane PJ (1990) Trichoderma koningii as a biological control agent for Sclerotinia sclerotiorum in southern Australia. Soil Biol Biochem 22(1):43–50CrossRefGoogle Scholar
  105. Tzin V, Galili G (2010) The biosynthetic pathways for Shikimate and aromatic amino acids in Arabidopsis thaliana. Arabidopsis Book 8:e0132. CrossRefPubMedPubMedCentralGoogle Scholar
  106. Ullah A, Heng S, Munis MFH, Fahad S, Yang XY (2015) Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: A review. Environ Exp Bot 117:28–40. CrossRefGoogle Scholar
  107. van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annual Review of Phytopathology 36:453–483. CrossRefPubMedPubMedCentralGoogle Scholar
  108. Van Peer R, Niemann G, Schippers B (1991) Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS 417 r. Phytopathology 81(7):728–734CrossRefGoogle Scholar
  109. Verma SC, Ladha JK, Tripathi AK (2001) Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J Biotechnol 91(2–3):127–141PubMedCrossRefPubMedCentralGoogle Scholar
  110. Vinodkumar S, Nakkeeran S, Renukadevi P, Malathi VG (2017) Biocontrol potentials of antimicrobial peptide producing Bacillus species: multifaceted antagonists for the Management of Stem rot of carnation caused by Sclerotinia sclerotiorum. Frontiers in Microbiology, 8. Doi:ARTN 44610.3389/fmicb.2017.00446Google Scholar
  111. Viterbo A, Horwitz BA (2010). Mycoparasitism Cellular and molecular biology of filamentous fungi (pp. 676-693): American society of microbiologyGoogle Scholar
  112. Vurukonda SSKP, Giovanardi D, Stefani E (2018) Plant growth promoting and biocontrol activity of Streptomyces spp. as endophytes. International Journal of Molecular Sciences 19(4):952PubMedCentralCrossRefGoogle Scholar
  113. Wang Z, Tan XL, Zhang ZY, Gu SL, Li GY, Shi HF (2012) Defense to Sclerotinia sclerotiorum in oilseed rape is associated with the sequential activations of salicylic acid signaling and jasmonic acid signaling. Plant Sci 184:75–82. CrossRefPubMedPubMedCentralGoogle Scholar
  114. Wei G, Kloepper JW, Tuzun S (1991) Induction of systemic resistance of cucumber to Colletotrichum orbiculare by select strains of plant growth-promoting rhizobacteria. Phytopathology 81(11):1508–1512CrossRefGoogle Scholar
  115. Westfall CS, Muehler AM, Jez JM (2013) Enzyme action in the regulation of plant hormone responses. J Biol Chem 288(27):19304–19311. CrossRefPubMedPubMedCentralGoogle Scholar
  116. Whipps JM, Gerlagh M (1992) Biology of Coniothyrium-Minitans and its potential for use in disease biocontrol. Mycological Research 96:897–907. CrossRefGoogle Scholar
  117. Woo J-H, Kamei Y (2003) Antifungal mechanism of an anti-Pythium protein (SAP) from the marine bacterium Streptomyces sp. strain AP77 is specific for Pythium porphyrae, a causative agent of red rot disease in Porphyra spp. Appl Microbiol Biotechnol 62(4):407–413PubMedCrossRefPubMedCentralGoogle Scholar
  118. Wu J, Zhao Q, Yang QY, Liu H, Li QY, Yi XQ, . . . Zhou YM (2016). Comparative transcriptomic analysis uncovers the complex genetic network for resistance to Sclerotinia sclerotiorum in Brassica napus. Scientific Reports, 6. Doi:ARTN 1900710.1038/srep19007Google Scholar
  119. Xiang, N., Lawrence, K. S., Kloepper, J. W., Donald, P. A., McInroy, J. A. (2017). Biological control of Heterodera glycines by spore-forming plant growth-promoting rhizobacteria (PGPR) on soybean. PLoS One, 12(7). Doi:ARTN e018120110.1371/journal.pone.0181201Google Scholar
  120. Yandigeri MS, Malviya N, Solanki MK, Shrivastava P, Sivakumar G (2015) Chitinolytic Streptomyces vinaceusdrappus S5MW2 isolated from Chilika lake, India enhances plant growth and biocontrol efficacy through chitin supplementation against Rhizoctonia solani. World J Microbiol Biotechnol 31(8):1217–1225PubMedCrossRefPubMedCentralGoogle Scholar
  121. Zahed MJ, Purabaei AA, Behbodi K, & S, E. (2018). Biological control of Sclerotinia sclerotiorum (Lib) De Bary cause the cucumber white stem rot by rhizospheric Actinobacteria. Biological control of Pests & Plant Diseases, 7(1), 33–45. doi:10.22059/jbioc.2017.230696.191Google Scholar
  122. Zeng W, Wang D, Kirk W, Hao J (2012) Use of Coniothyrium minitans and other microorganisms for reducing Sclerotinia sclerotiorum. Biol Control 60(2):225–232CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Bong-Gyu Mun
    • 1
  • Won-Hee Lee
    • 1
  • Sang-Mo Kang
    • 1
  • Sang-Uk Lee
    • 1
  • Seok-Min Lee
    • 2
  • Dong Yeol Lee
    • 3
  • Muhammad Shahid
    • 1
  • Byung-Wook Yun
    • 1
    Email author
  • In-Jung Lee
    • 1
    Email author
  1. 1.School of Applied BiosciencesKyungpook National UniversityDaeguRepublic of Korea
  2. 2.Environment-friendly Agriculture Division, Gyeongsangnam-do Agricultural Research & Extension ServicesJinjuRepublic of Korea
  3. 3.Gyeongnam Oriental Anti-aging InstituteSancheongRepublic of Korea

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