Abstract
Damping off of tomato caused by Athelia rolfsii causes serious losses in the Benin Republic despite the use of chemical fungicides. To reduce pesticide dependency and provide better control, we evaluated the activity of soil isolate GT4041 against A. rolfsii in Japan for use in Benin. Isolate GT4041, applied in its PC1 culture broth, strongly inhibited A. rolfsii mycelial growth in dual culture and completely inhibited sclerotial germination. In growth chamber tests, sclerotia were pretreated with GT4041 or GT4041 was preincubated in soil before application or applied directly on sclerotia on the soil; GT4041was always used in its culture broth. Its direct application on the soil reduced disease incidence the most in the growth chamber and in the greenhouse. GT4041 inhibited mycelial growth of five other tomato fungal pathogens and also increased tomato root and shoot dry mass. GT4041 produced proteases and indole acetic and it grew optimally at 28 °C. Scanning electron microscopy of GT4041 showed cylindrical, smooth spores in flexuous chains. This is the first report of S. sasae as a biocontrol agent for tomato damping off caused by A. rolfsii.
Similar content being viewed by others
References
Abdullah ZK, Kihara J, Gondo Y, Ganphung R, Yokoyama Y, Ueno M (2021) Suppressive effect of secondary metabolites from Streptomyces plumbeus isolate F31D against Fusarium oxysporum f. sp. lycopercisi, the causal agent of Fusarium wilt of tomato. J Gen Plant Pathol 87:335–343. https://doi.org/10.1007/s10327-021-01020-x
Adandonon A, Aveling TAS, Tamo M (2004) Occurrence and distribution of cowpea damping-off and stem rot and associated fungi in Benin. J Agric Sci 142:561–566. https://doi.org/10.1017/S0021859604004629
Adandonon A, Aveling TAS, Labuschagne N, Tamo M (2006) Biocontrol agents in combination with Moringa oleifera extract for integrated control of Sclerotium-caused cowpea damping-off and stem rot. Eur J Plant Pathol 115:409–418. https://doi.org/10.1007/s10658-006-9031-6
Aycock R (1966) Stem rot and other diseases caused by Sclerotium rolfsii. North Carolina Agric Exp Stn Tech Bull 174
Baćmaga M, Wyszkowska J, Kucharski J (2016) The effect of the Falcon 460 EC fungicide on soil microbial communities, enzyme activities and plant growth. Ecotoxicology 25:1575–1587. https://doi.org/10.1007/s10646-016-1713-z
Baćmaga M, Wyszkowska J, Kucharski J (2019) The biochemical activity of soil contaminated with fungicides. J Environ Sci Health B 54:252–262. https://doi.org/10.1080/03601234.2018.1553908
Bérdy J (2012) Thoughts and facts about antibiotics: where we are now and where we are heading. J Antibiot 65:385–395. https://doi.org/10.1038/ja.2012.27
Bhuiyan MAH, Rahman MT, Bhuiyan KA (2012) In vitro screening of fungicides and antagonists against Sclerotium rolfsii. Afr J Biotechnol 11:14822–14827. https://doi.org/10.5897/AJB12.1693
Chen L, Wu YD, Chong XY, Xin QH, Wang DX, Bian K (2019) Seed-borne endophytic Bacillus velezensis LHSB1 mediate the biocontrol of peanut stem rot caused by Sclerotium rolfsii. J Appl Microbiol 128:803–813. https://doi.org/10.1111/jam.14508
Crowe FJ, Hall DH (1980) Soil temperature and moisture effects on sclerotium germination and infection of onion seedlings by Sclerotium cepivorum. Phytopathology 70:74–78. https://doi.org/10.1094/Phyto-70-74
Datta C, Basu PS (2000) Indole acetic acid production by a Rhizobium species from root nodules of a leguminous shrub, Cajanus cajan. Microbiol Res 155:123–127. https://doi.org/10.1016/S0944-5013(00)80047-6
Dutta P, Kaman PK, Kumari A, Saikia B, Deb L (2022) Management of Sclerotium rolfsii causing basal rot of Piper longum through organic approaches. Indian Phytopathol 75:267–271. https://doi.org/10.1007/s42360-021-00428-x
Elad Y, Kapat A (1999) The role of Trichoderma harzianum protease in the biocontrol of Botrytis cinerea. Eur J Plant Pathol 105:177–189. https://doi.org/10.1023/A:1008753629207
FAO (2020) Crop and livestock products. FAOSTAT. Food and Agriculture Organization of the United Nations. http://www.fao.org/faostat/en/#data/QCL
Farhaoui A, Adadi A, Tahiri A, Alami NE, Khayi S, Mentag R, Ezrari S, Radouane N, Mokrini F, Belabess Z, Lahlali R (2022) Biocontrol potential of plant growth-promoting rhizobacteria (PGPR) against Sclerotiorum rolfsii diseases on sugar beet (Beta vulgaris L). Physiol Mol Plant Pathol 119:101829. https://doi.org/10.1016/j.pmpp.2022.101829
Franke MD, Brenneman TB, Stevenson KL, Padgett GB (1998) Sensitivity of isolates of Sclerotium rolfsii from peanut in Georgia to selected fungicides. Plant Dis 82:578–583. https://doi.org/10.1094/PDIS.1998.82.5.578
Ganphung R, Kihara J, Ueno M (2019) Biological control of powdery mildew caused by Podosphaera xanthii in cucumber by Streptomyces blastmyceticus strain STS1 isolated in Shimane Prefecture. J JSATM 26:61–68
Gordon SA, Weber RP (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26:192–195. https://doi.org/10.1104/pp.26.1.192
Haidary M, Tamura T, Ueno M (2018) Inhibitory activity of Paenibacillus sp. isolated from soil in Gotsu city, Shimane Prefecture, against Xanthomas oryzae pv. Oryzae, the causal agent of rice bacterial leaf blight. J Adv Microbiol 8:197–210. https://doi.org/10.4236/aim.2018.83014
Huong NL, Itoh K, Suyama K (2007) Diversity of 2,4-diclorophenoxyacetic acid (2,4-D) and 2,4,5-trichlorophenoxyacetiacid (2,4,5-T)-degrading bacteria in vietnamese soils. Microb Environ 22:243–256. https://doi.org/10.1264/jsme2.22.243
James B, Atcha-Ahowé C, Godonou I, Baimey H, Goergen G, Sikirou R, Toko M (2010) Integrated pest management in vegetable production: a guide for extension workers in West Africa. IITA, Ibadan. https://hdl.handle.net/10568/63650
Khatri K, Kunwar S, Barocco RL, Dufault NS (2017) Monitoring fungicide sensitivity levels and mycelial compatibility groupings of Sclerotium rolfsii isolates from Florida peanut fields. Peanut Sci 44:83–92. https://doi.org/10.3146/PS17-7.1
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. https://doi.org/10.1007/BF01731581
Küçük HB, Yusufoglu A, Mataracı E, Dösler S (2011) Synthesis and biological activity of new 1,3-dioxolanes as potential antibacterial and antifungal compounds. Molecules 16:6806–6815. https://doi.org/10.3390/molecules16086806
Le CN, Mendes R, Kruijt M, Raaijmakers JM (2012) Genetic and phenotypic diversity of Sclerotium rolfsii in groundnut fields in central Vietnam. Plant Dis 96:389–397. https://doi.org/10.1094/PDIS-06-11-0468
Lee H, Whang K (2015) Streptomyces sasae sp. nov., isolated from bamboo (Sasa borealis) rhizosphere soil. Int J Syst Evol Microbiol 65:3547–3551. https://doi.org/10.1099/ijsem.0.000454
Lee J, Whang K (2016) Optimization of indole-3-acetic acid (IAA) production by Bacillus megaterium BM5. Korean J Soil Sci 49:461–468. https://doi.org/10.7745/KJSSF.2016.49.5.461
Lemtukei D, Tamura T, Nguyen TQ, Kihara J, Ueno M (2016) Antagonistic potential of isolated microorganisms from soil in Shimane Prefecture against rice blast disease caused by Magnaporthe oryzae. Bull Fac Life Environ Sci Shimane Univ 21:9–12
Matsui T, Kato K, Namihira T, Shinzato N, Semba H (2009) Stereospecific degradation of phenylsuccinate by actinomycetes. Chemosphere 76:1278–1282. https://doi.org/10.1016/j.chemosphere.2009.06.021
Mohite B (2013) Isolation and characterization of indole acetic acid (IAA) producing bacteria from rhizospheric soil and its effect on plant growth. J Soil Sci Plant Nutr 13:638–649. https://doi.org/10.4067/S0718-95162013005000051
Mukherjee PK, Raghu K (1997) Trichoderma sp. as a microbial suppressive agent of Sclerotium rolfsii on vegetables. World J Microbiol Biotechnol 13:497–499. https://doi.org/10.1023/A:1018501006122
Muthukumar A, Venkatesh A (2014) Biological inductions of systemic resistance to collar rot of peppermint caused by Sclerotium rolfsii. Acta Physiol Plant 36:1421–1431. https://doi.org/10.1007/s11738-014-1520-1
Myo EM, Ge B, Ma J, Cui H, Liu B, Shi L, Jiang M, Zhang K (2019) Indole-3-acetic acid production by Streptomyces fradiae NKZ-259 and its formulation to enhance plant growth. BMC Microbiol 19:155. https://doi.org/10.1186/s12866-019-1528-1
Nakagawa Y, Tamura T, Kawasaki H (2001) Genetic analysis method (in japanese). (ed) Identification manual of actinomycetes. Business Center for Academic Societies Japan, Tokyo, Japan, pp 249–257. The Society for Actinomycetes Japan
Osemwegie OO, Oghenekaro AO, Owolo LO (2010) Effects of pulverized Ganoderma spp., on Sclerotium rolfsii Sacc and post-harvest tomato (Lycopersicon esculentum Mill.) Fruits preservation. J Appl Sci Res 6:1794–1800
Punja ZK (1985) The biology, ecology, and control of Sclerotium rolfsii. Annu Rev Phytopathol 23:97–127. https://doi.org/10.1146/annurev.py.23.090185.000525
Rakh RR, Raut LS, Dalvi SM, Manwar AV (2011) Biological control of Sclerotium rolfsii, causing stem rot of groundnut by Pseudomonas cf monteilii . Recent Res Sci Technol 3:26–34. https://doi.org/10.25081/rrst.2017.9.3355
Ratna Kumar PK, Shiny Niharika P, Hemanth G (2015) Impact of fungicides on the growth and distribution of soil mycoflora in agriculture fields at Narasannapeta. Int J Sci Res 6:2337–2347. https://doi.org/10.21275/ART20164650
Roman DL, Voiculescu DI, Filip M, Ostafe V, Isvoran A (2021) Effects of triazole fungicides on soil microbiota and on the activities of enzymes found in soil: a review. Agriculture 11:893. https://doi.org/10.3390/agriculture11090893
Sahu KP, Singha S, Gupta A, Singha UB, Brahmaprakash GP, Saxena AK (2019) Antagonistic potential of bacterial endophytes and induction of systemic resistance against collar rot pathogen sclerotium rolfsii in tomato. Biol Control 137:104014. https://doi.org/10.1016/j.biocontrol.2019.104014
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Santhanarajan A, Han Y, Koh S (2021) The efficacy of functional compost manufactured using spent coffee ground, rice bran, biochar, and functional microorganisms. Appl Sci 11:7703. https://doi.org/10.3390/app11167703
Sarker A, Al-Rashid J (2013) Analytical protocol for determination of indole 3 acetic acid (IAA) production by plant growth promoting bacteria (PGPB). In: Technical report of quantification of IAA by microbes, pp 1–2. https://www.researchgate.net/publication/263818523
Scinos AS (1989) Targeting fungicides for control of southern stem rot on peanut. Plant Dis 73:723–726. https://doi.org/10.1094/PD-73-0723
Sennoi S, Jogloy S, Saksirirat W, Kesmala T, Patanothai A (2013) Genotypic variation of resistance to southern stem rot of Jerusalem artichoke caused by Sclerotium rolfsii. Euphytica 190:415–424. https://doi.org/10.1007/s10681-012-0813-y
Shim MY, Starr JL, Keller NP, Woodard KE, Lee TAJr (1998) Distribution of isolates of Sclerotium rolfsii tolerant to pentachloronitrobenzene in Texas peanut fields. Plant Dis 82:103–106. https://doi.org/10.1094/PDIS.1998.82.1.103
Sikirou R, Zannou A, Gbèhounou G, Tosso F, Komlan FA (2010) Fungicide effect of banana column juice on tomato southern blight caused by Sclerotium rolfsii: Technical and economic efficiency. Afr J Agric Res 5:3230–3238. https://doi.org/10.5897/AJAR10.513
Sikirou R, Ezin V, Beed F, Etchiha afoha SAP, Tosso FD, Ouessou Idrissou F (2015) Geographical distribution and prevalence of the main tomato fungal wilt diseases in Benin. Int J Biol Chem Sci 9:603–613. https://doi.org/10.4314/ijbcs.v9i2.3
Solans M, Vobis G, Cassan F (2011) Production of phytohormones by root-associated saprophytic actinomycetes isolated from the actinorhizal plant Ochetophila trinervis. World J Microbiol Biotechnol 27:2195–2202. https://doi.org/10.1007/s11274-011-0685-7
Srivastava N, Gupta S, Sarethy IP (2021) Characterization of Streptomyces sp. UK-201 from Lachhiwala Reserve Forest, a biodiversity hot spot of the Himalayas. Nat Prod J 11:207–220. https://doi.org/10.2174/2210315509666191113152549
Sudiana IM, Putri A, Napitupulu TP, Idris, Purnaningsih I, Kanti A (2020) Growth inhibition of Fusarium solani and F oxysporum by Streptomyces sasae TG01, and its ability to solubilize insoluble phosphate. Biodivers J Biol Divers 21:429–435. https://doi.org/10.13057/biodiv/d210201
Suzuki S, Taketani H, Kusumoto K, Kashiwagi Y (2006) High-throughput genotyping of filamentous fungus aspergillus oryzae based on colony direct polymerase chain reaction. J Biosci Bioeng 102:572–574. https://doi.org/10.1263/jbb.102.572
Taechowisan T, Peberdy JF, Lumyong S (2003) Isolation of endophytic actinomycetes from selected plants and their antifungal activity. World J Microbiol Biotechnol 19:381–385. https://doi.org/10.1023/A:1023901107182
Thompson J, Higgins D, Gibson T (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties, and weight matrix choice. Nucleic Acid Res 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673
You J, Tang T, Wang F, Mao T, Yuan B, Guo J, Guo X, Duan Y, Huang J (2021) Baseline sensitivity and control efficacy of strobilurin fungicide pyraclostrobin against Sclerotium rolfsii. Plant Dis 105:3503–3509. https://doi.org/10.1094/PDIS-01-21-0176-RE
Zacky FA, Ting ASY (2013) Investigating the bioactivity of cells and cell-free extracts of Streptomyces griseus towards Fusarium oxysporum f. sp. cubense race 4. Biol Control 66:204–208. https://doi.org/10.1016/j.biocontrol.2013.06.001
Acknowledgements
The authors thank the Ministry of Education, Culture, Sports, Science, and Technology (MEXT) and the Faculty of Life and Environmental Sciences of Shimane University for their financial support in the publication of this report.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Ethical approval
Not applicable.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The nucleotide sequence presented in this paper is available in the DDBJ/EMBL/GenBank database under accession number LC720967.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Adam Dade, G.M.A., Kihara, J. & Ueno, M. Control of tomato southern blight caused by Athelia rolfsii (syn. Sclerotium rolfsii) using the soil isolate Streptomyces sasae strain GT4041. J Gen Plant Pathol 89, 159–169 (2023). https://doi.org/10.1007/s10327-023-01122-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10327-023-01122-8