کنترل Phytophthora sojae و Macrophomina Phaseolina در سویا توسط عوامل زیستی

نوع مقاله : مقاله پژوهشی


1 گروه بیوتکنولوژی، پژوهشکده علوم محیطی، پژوهشگاه علوم و تکنولوژی پیشرفته و علوم محیطی، دانشگاه تحصیلات تکمیلی صنعتی و فناوری پیشرفته، کرمان، ایران

2 گروه تنوع زیستی، پژوهشکده علوم محیطی، پژوهشگاه علوم و تکنولوژی پیشرفته و علوم محیطی، دانشگاه تحصیلات تکمیلی صنعتی و فناوری پیشرفته، کرمان، ایران

3 دانشجوی سابق رشته بیماری شناسی گیاهی، دانشگاه زابل، زابل، ایران


سویا یکی از مهم‌ترین دانه‎‌های روغنی در جهان است که نیمی از پروتئین و روغن گیاهی مصرفی انسان را تامین می‌کند. بیماری پوسیدگی زغالی و پوسیدگی طوقه و ریشه سویا ناشی از Macrophomina phaseolina و Phytophthora sojae از مهم‌ترین بیماری‌های سویا هستند که باعث کاهش کمی و کیفی عملکرد محصول می‌شوند. راهبرد مهار زیستی با استفاده از خانواده Actinobacteria، به ویژه اعضای جنس Streptomyces و در خانواده Hypocreaceae، جنس Trichoderma، به عنوان یک روش امیدوارکننده برای مدیریت بیماری‌ها و آفات در نظر گرفته می‌شود. در این مطالعه فعالیت مهار زیستی یک جدایه استرپتومایسس و یک جدایه تریکودرما‌ی جداسازی شده از خاک باغات استان کرمان در برابر قارچ‌های بیمارگرM. phaseolina و P. sojae مورد ارزیابی قرار گرفت. آزمایش‌ها در آزمایشگاه بر پایه طرح کاملاتصادفی با سه تکرار انجام شد. تجزیه و تحلیل توالی 16s rDNA و ناحیه ITS نشان داد که  Streptomyces sp.جدایه ۲۳ وTrichoderma sp. جدایه۱ به ترتیب متعلق به S. bacillaris وT. Longibrachiatum  می‌باشند. نتایج روش کشت دوگانه و آزمون متابولیت‌های فرار نشان داد که S. bacillaris جدایه23 و T. longibrachiatum جدایه۱ بطور معنی‌داری از رشد M. phaseolina و P. sojae جلوگیری کردند. در هر دو آزمون، دو عامل بیوکنترل مورد استفاده اثر بازدارندگی بیشتری بر روی رشد میسلیومیP. sojae در مقایسه با M. phaseolina از خود نشان دادند.


عنوان مقاله [English]

Control of Phytophthora sojae and Macrophomina phaseolina in soybean by biological agents

نویسندگان [English]

  • saeid mirzaei 1
  • Masoud Ahmadi -Afzadi 1
  • Mohammadreza Lashkari 2
  • Batul Sadeghi 3
1 Department of Biotechnology, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, kerman. Iran.
2 Department of Biodiversity, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, Kerman, Iran
3 Former student of plant protection, Agricultural Faculty, Zabol University, Zabol, Iran.
چکیده [English]

Soybean is one of the most important oilseed crops, supplying half of the protein and vegetable oil by humans. Charcoal rot disease and soybean crown and root rot caused by Macrophomina phaseolina and Phytophthora sojae, respectively, are among the most important soybean pathogens that cause a reduction in crop yield. A biocontrol strategy using Actinobacteria, especially different species of Streptomyces, and Hypocreaceae especially different species of Trichoderma, is considered a method for the management of disease and pests. In this study, biological control of these pathogens was investigated using Streptomyces sp. isolate 23 and Trichoderma sp. isolates 1 and their volatile metabolites. The activity of Streptomyces isolates and a Trichoderma isolate taken from the soil of Kerman was evaluated against pathogenic fungi, M. phaseolin, and P. sojae. Experiments in the laboratory were conducted based on a completely randomized design with three replications. Sequence analysis of 16s rDNA and ITS region showed Streptomyces sp. isolate 23 and Trichoderma sp. isolate 1 belong to S. bacillaris and T. longibrachiatum, respectively. The results of the double culture method and volatile metabolites test showed that S. bacillaris isolate 23 and T. longibrachiatum isolate 1, significantly inhibited the growth of M. phaseolina and P. sojae. In both tests, the two biocontrol agents used showed more inhibitory effects on P. sojae compared to M. phaseolina. The results of the dual culture and volatile metabolites tests showed that S. bacillaris isolate 23 and T. longibrachiatum isolate 1 had a high inhibitory effect on M. phaseolina and P. sojae.

کلیدواژه‌ها [English]

  • Actinobacteria
  • Charcoal rot disease
  • Soybean
  • Biocontrol

Extended Abstract


    Soybean is one of the most important oilseed crops in the world, supplying half of the protein and vegetable oil consumed by humans. It is a nitrogen-fixing legume that is usually cultivated in alternation with cereals. Charcoal rot disease and soybean crown and root rot caused by Macrophomina phaseolina and Phytophthora sojae, respectively, are among the most important soybean pathogens that cause quantitative and qualitative reduction of crop yield. The common method of using chemical fungicides to control these diseases poses negative side effects on humans and the environment.

 Biological control offers the best alternative for controlling plant diseases. Actinobacteria, especially different species of Streptomyces, and Hypocreaceae especially members of the genus Trichoderma, are considered as the promising method for the management of diseases and pests. Furthermore, Actinobacteria produce antifungal antibiotics, cell wall degrading enzymes, and plant growth promoters which protect plants from a wide range of phytopathogenic fungi. Trichoderma is of great importance in controlling plant pathogens due to its rapid growth, high ability to produce spores, and the ability of myco-parasitism against a wide range of fungal pathogens.


Materials and Methods

    In this study, the activity of Streptomyces isolates and Trichoderma isolates taken from the soil of Kerman was evaluated against pathogenic fungi, M. phaseolina, and P. sojae. Experiments in the laboratory were conducted based on a completely randomized design with three replications. To confirm the antagonistic activity of Trichoderma sp. isolate 1 and Streptomyces sp. isolate 23, a dual culture assay and Sandwiched Petri dish method were used. Streptomyces sp. isolate 23 and Trichoderma sp. isolate 1 were identified based on morphological and molecular characteristics (16s rDNA and ITS regions).


Results and Discussion

    Sequence analysis of 16s rDNA and ITS region showed Streptomyces sp. isolate 23 and Trichoderma sp. isolate 1 belong to S. bacillaris and T. longibrachiatum respectively.

Results of dual culture showed that the hyphal growth of M. phaseolina and P. sojae stopped by T. longibrachiatum with an average of 58% and 97.14%, respectively. In addition, the T. longibrachiatum was able to advance the inhibition zone and cover the pathogenic fungal colonies, and exert intense and rapid sporadic activity at various locations of hyphae, including on the pathogenic fungal colonies. This physiological feature is the most important stage in parasitic activity. Moreover, S. bacillaris significantly inhibited the hyphal growth of M. phaseolina and P. sojae in dual culture.

Streptomyces species have been identified as one of the promising sources for the biological control of plant diseases. They produce active antifungal and antibacterial substances. In this study was observed that volatile compounds of S. bacillaris have inhibitory effects on the hyphal growth of phytopathogenic fungi M. phaseolina and P. sojae. Furthermore, it was observed that volatile compounds of S. bacillaris stopped the production of microsclerotia in M. phaseolina and the radial growth of P. sojae. Also, Streptomyces generates antifungal volatile compounds. Furthermore, our results revealed that T. longibrachiatum volatile compound significantly decreased the rate of microsclerotia production in M. phaseolina and the density of the colony over passing time.



    The results of the present study showed that two biocontrol agents T. longibrachiatum and S. bacillaris and their volatile compounds are highly efficient in the biocontrol of pathogenic fungi of M. phaseolina and P. sojae in vitro. Both T. longibrachiatum and S. bacillaris could decrease the production of microsclerotium of M. phaseolina. Microsclerotia are living structures that persist in the soil for many years and play an important role in the disease cycle. Studies have shown that inhibition of germination of the fungus's survival organs can disrupt the disease cycle and protect the plant. T. longibrachiatum and S. bacillaris can be good candidates for controlling M. phaseolina and P. sojae in soybean plants. Further investigation is needed in the greenhouse and field conditions.

رضایی، ساسان و علیزاده، علی (١٣٧٧) . بوته میری فیتوفترایی سویا ناشی از قارچ  Phytophthora sojaeدر استان لرستان. نشریه بیماریهای گیاهی، 34 (4)، 122- 143.
میرزایی، سعید (1396). پروفایل ترانسکریپتوم نوک شاخه و ریشه گیاه سویا. مجله پژوهشهای سلولی و مولکولی. مجله زیست شناسی ایران، 30 (4)، 409- 421.
Ajith, P.S., &Lakshmidevi, N. (2010). Effect of volatile and non-volatile compounds from Trichoderma spp. against Colletotrichumcapsiciincitant of anthracnose on bell peppers. Nature and Science. 8(9), 265– 269.
Al-Hazmi, A.S., &TariqJaveed, M. (2016). Effects of different inoculum densities of Trichoderma harzianum and Trichoderma viride against Meloidogynejavanica on tomato. Saudi Journal of Biological Sciences, 23(2), 288-292. ‏
Altomare, C., Norvell, W.A., Bjbrkman, T., &Harman, GE, (1999). Solubilization ofphosphates and micronutrients by the plant growth promoting and biocontrol fungusTrichoderma harzianumRifai 1295–22. Applied and Environmental Microbiology. 65, 2926–2933.
Ambuse, M.G., Chatage, V.S., &Bhale, U.N., (2012). Influence of Trichoderma spp. against Alternariatenuissima inciting leaf spot of RumexAcetosa L. Bioscience Discovery. 3(2), 259–262.
Arfaoui, A., Adam, L.R., Bezzahou, A., &Daayf, F. (2018). Isolation and identification of cultivated bacteria associated with soybeans and their biocontrol activity against Phytophthorasojae.Journal of the International Organization for Biological Control, 1-11. ‏
Atta, H.M., El-Sayed, A.S., El-Desoukey, M.A., Hassan, M, &El-Gazar, M. (2015). Biochemical studies on the Natamycin antibiotic produced by Streptomyceslydicus: Fermentation, extraction and biological activities. Journal of Saudi Chemical Society, 19(4), 360-371. ‏
Baltz, R.H. (2016) Genetic manipulation of secondary metabolite biosynthesis for improved production in Streptomyces and other Actinomycetes. Journal of Industrial Microbiology and Biotechnology, 43(2-3), 343-370. ‏
Benítez, T., Rincón, A.M., Limón, M.C., &Codón, A.C. (2004). Biocontrol mechanisms of Trichoderma strains. International Journal of Microbiology. 7(4):249-60.
Bibb, M.J., Hopwood, D.A., Chater, K.F., Kieser, T., Bruton, C., Kieser, H.M., Lydiate, D.L., Smith, CP., Ward, J.M., Schremp, f. H. (1985). Genetic manipulation of Streptomyces: a laboratory manual. The John Innes Foundation, Norwich, United Kingdom.
Boukaew, S., Prasertsan, P., Troulet, C., &Bardin, M. (2017). Biological control of tomato gray mold caused by Botrytis cinerea by using Streptomyces spp. Journal of the International Organization for Biological Control, 62(6), 793-803. ‏
Brotman, Y., Lisec, J., Méret, M., Chet, I., Willmitzer, L., &Viterbo, A. (2012). Transcript and metabolite analysis of the Trichoderma-induced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana. Microbiology, 158(1), 139-146. ‏
Brunner, K., Zeilinger, S., Ciliento, R., Woo, S.L, Lorito, M., Kubicek, C.P, &Mach, R.L. (2005). Improvement of the fungal biocontrol agent Trichodermaatroviride to enhance both antagonism and induction of plant systemic disease resistance. Applied and Environmental Microbiology. 71, 3959–3965.
Chen, Y., Zhou, D., Qi, D., Gao, Z., Xie, J., &Luo, Y. (2018). Growth Promotion and Disease Suppression Ability of a Streptomyces sp. CB-75 from Banana Rhizosphere Soil. Frontiers in Microbiology, 8, 2704.
Chen, Y.Y, Chen, P.C., &Tsay, T.T. (2016). The biocontrol efficacy and antibiotic activity of Streptomyces plicatus on the oomycete Phytophthoracapsici.Journal of the International Organization for Biological Control, 98, 34-42. ‏
Choudhary, S., &Reena, M. (2012). In-vitro antagonism of indigenous Trichoderma isolates against phytopathogen causing wilt of lentil. International Journal of Life Science and Pharma Research. 2(3), 195–202.
Cook, G.E., Boosalis, M.G., Duncle, L.D., &Odvody GN. (1973). Survival of Macrophominaphaseolinain corn and sorghum stalk residue. Plant Disease 57: 873-875.
Dennis, C., &Webster, J. (1971). Antagonistic properties of species-groups of Trichoderma: II. Production of volatile antibiotics. Transactions of the British Mycological Society,57(1), 41-48.
Dubey, S.C., Tripathi, A., Dureja, P., &Grover, A. (2011). Characterization of secondary metabolites and enzymes produced by Trichoderma species and their efficacy against plant pathogenic fungi. Indian Journal of Agricultural Sciences. 81(5):455–461.
Elad, Y., Chet, I., &Henis, Y. (1981). A selective medium for improving quantitative isolation of Trichoderma spp. from soil. Phytoparasitica, 9(1), 59-67. ‏
El-Tarabily, KA &Sivasithamparam K. (2006). Non-streptomyceteactinomycetes as biocontrol agents of soil-borne fungal plant pathogens and as plant growth promoters, Soil Biology and Biochemistry, 38(7): 1505-1520.
El-Tarabily, K.A., Nassar, A.H., Hardy, G.E.S.J., &Sivasithamparam, K. (2009). Plant growth promotion and biological control of Pythium aphanidermatum, a pathogen of cucumber, by endophytic actinomycetes. Journal of Appl Microbiology, 106(1):13–26.
El-Tarabily, K.A., Sykes, M.L., Kurtboke, I.D., Hardy, G.E.S.J., Barbosa, A.M. (1996). Synergistic effects of a cellulase-producing Micromonosporacarbonacea and an antibiotic- producing Streptomyces violascens on the suppression of Phytophthoracinnamomi root-rot of Banksia grandis. Canadian Journal of Botany 74, 618–624.
Erwin, D.C., &Ribeiro, O. K. (1996). PhytophthoraDiseases Worldwide. APS Press, St. Paul, M N.
EYE, L.L., Sneh, R., Lockwood, J.L. (1978) Factors affecting zoospore production by Phytophthoramegasperma var. sojae. Phytopathology68: 1766-68.
FAO. (2019). The State of Food and Agriculture.FAO, Rome.https://creativecommons.org/licenses/by-nc-sa/3.0/igo).
Feng, J., Hwang, R., Chang, K.F, Hwang, S.F., Strelkov, S.E., Gossen, B.D., &Zhou Q. (2010). An inexpensive method for extraction of genomic DNA from fungal mycelia. Canadian Journal of Plant Pathology, 32(3), 396-401.
Gams, W., &Bissett, J. (1998). Morphology and Identification of Trichoderma. In: Kubicek CP, Harman GE (Eds) Trichoderma and Gliocladium. Vol. 1. Basic Biology, Taxonomy and Genetics. Taylor and Francis Ltd, London, 3–34.
Gujar, C.P., Jain, S.C., &Mali, B.L. (2014). Pathogenic effects of root rot fungi on seed germination of soybean. Journal of Plant Disease Sciences, 9(1), 20-23. ‏
Gupta, G.K., Sharma, S.K., &Ramteke, R. (2012). Biology, epidemiology and management of the pathogenic fungus Macrophominaphaseolina (Tassi) Goid with special reference to charcoal rot of soybean (Glycine max (L.) Merrill). Journal of Phytopathology, 160(4), 167-80.
Gveroska, B., &Ziberoski, J. (2011). Trichoderma harzianum as a biocontrol against Alternariaalternata on tobacco. Environmental Technology & Innovation. 7(2):67–76.
Hajieghrari, B, Torabi-Giglou, M., Momammadi, M., &Davari, M. (2008). Biological potantial of some Iranian Trichoderma isolates in the control of soil borne plant pathogenic fungi. African Journal of Biotechnology (7): 967-972.
He, D.C., He, M.H., Amalin, D.M., Liu, W., Alvindia, D.G, &Zhan, J. (2021). Biological Control of Plant Diseases: An Evolutionary and Eco-Economic Consideration.Pathogens, 10(10), 1311.
Herath, H.H.M.A.U., Wijesundera, R.L.C, Chandrasekharan, N.V., Wijesundera, W.S.S., &Kathriarachchi, H.S. (2015). Isolation and characterization ofTrichoderma erinaceum for antagonistic activity against plant pathogenic fungi. Applied and Environmental Microbiology. (5), 120-127.
Hermosa, R., Cardoza, R.E., Rubio, M.B., Gutiérrez, S., &Monte, E. (2014). Secondary metabolism and antimicrobial metabolites of Trichoderma. Biotechnology and biology of trichoderma, 125-137.
Hermosa, R., Viterbo, A., Chet, I., &Monte, E. (2012). Plant-beneficial effects of Trichoderma and of its genes. Microbiology. 158, 17–25.
Howell, C.R. (2003). Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Disease, 87(1), 4-10. ‏
Jabnoun-Khiareddine, H., Daami-Ramadi, M., Ayed, F., &Mahjoub, M.E. (2009). Biological control of tomato Verticillium wilt by using indigenous Trichoderma spp. The African Journal of Plant Science and Biotechnology. 3, 26–36.
Kaewchai, S., Soytong, K., &Hyde, K.D. (2010). Mycofungicides and fungal biofertilizers. Fungal Diversity, 38, 25-50.
Kaufmann, M.J., &Gerdemann, W. (1958). Root and stem rot of soybean caused by Phytophthorasojaen.sp. Phytopathology, 48,201-208.
Kreuze, J.F., Suomalainen, S., Paulin, L., &Valkonen, J.P. (1999). Phylogenetic analysis of 16S rRNA genes and PCR analysis of the nec1 gene from Streptomyces spp. causing common scab, pitted scab, and netted scab in Finland. Phytopathology, 89(6), 462-469. ‏
Lane, D.J. (1991) 16S/23S rRNA Sequencing. In: Stackebrandt, E. and Goodfellow, M., Eds., Nucleic Acid Techniques in Bacterial Systematic, John Wiley and Sons, New York, 115-175.
Li, Q., Ning, P., Zheng, L., &Huang, J. (2012). Effects of volatile substances of Streptomyces globisporus JK-1 on control of Botrytis cinerea on tomato fruit. Biological Control. 61, 113–120.
Manhas, R.K., &Kaur, T. (2016). Biocontrol potential of Streptomyces hydrogenans strain DH16 toward Alternariabrassicicola to control damping off and black leaf spot of Raphanussativus. Frontiers in Plant Science, 7, 1- 13. ‏
Markovich, N.A., &Kononova, G.L. (2003). Lytic enzymes of Trichoderma and their role in plant defense from fungal diseases: a review. Applied of Biochemistry of Microbiology. 39, 341-351.
Martínez-Medina, A., Roldán, A., Pascual, J.A. (2011). Interaction between arbuscular mycorrhizal fungi and Trichoderma harzianum under conventional and low input fertilization field condition in melon crops: growth response and Fusarium wilt biocontrol. Applied Soil Ecology. 47, 98–105.
Matroudi, S., Zamani, M.R., &Motallebi, M. (2009). Antagonistic effects of three species of Trichoderma sp. on Sclerotiniasclerotiorum, the causal agent of canola stem rot. Egyptian Journal of Biology, 11, 37-44.
Mendoza, J.L.H., Pérez, M.I.S., Prieto, J.M.G., Velásquez, J.D.Q, Olivares, J.G.G &Langarica, H.R.G. (2015). Antibiosis of Trichodermaspp strains native to northeastern Mexico against the pathogenic fungus Macrophominaphaseolina. Brazilian Journal of Microbiology, 46(4), 1093-1101.‏
Mirzaei, S. (2018). Transcriptome profiling of shoot and root tip of soybean, Molecular and Cellular Researches, 30(4), 409-421 (In Persian).
Mohammadi, A., Alizadeh, A., MIrabolfathy, M., &Safaie, N. (2007). Change in Racial Composition of Phytophthorasojae in Iran between 1998 and 2005. Journal of Plant Protection Research. 47 (1), 30-34.
Monteiro, V., Silva, R.N., Steindorff, A., Costa, F., &Noronha, E. (2010). New insightsin; Trichoderma harzianum antagonism of fungal plant pathogens bysecreted protein analysis. Current Microbiology. 61, 298–305.
Mukhopadhyay, R., &Kumar, D. (2020). Trichoderma: a beneficial antifungal agent and insights into its mechanism of biocontrol potential. Egyptian Journal of Biological Pest Control.30, 133.
Ng, L.C., Ngadin, A., Azhari, M., &Zahari, N.A. (2015). Potential of Trichoderma spp. as biological control agents against Bakanae pathogen (Fusarium fujikuroi) in rice. Asian Journal of Plant Pathology. 9(2):46–58.
Prasad, B.N., &Kumar, M.R. (2011). Comparative efficacy of different isolates of Trichoderma spp. against Rhizoctoniasolani, incitant of sheath blight of rice. Indian Journal of Fundamental and Applied Life Sciences. 1(3),107–111.
Qualhato, T.F., Lopes, F.A.C., Steindorff, A.S., Brandao, R.S., Jesuino, R.S.D., &Ulhoa, C.j. (2013). Mycoparasitism studies of Trichoderma species against three phytopathogenic fungi: evaluation of antagonism and hydrolytic enzyme production. Biotechnology Letters. 35(9), 1461-1468.‏
Rahman, M.A., Razvy, M.A., &Alam, M.F. (2013). Antagonistic activities of Trichoderma strains against chili anthracnose pathogen. International Journal of Microbiology and Mycology. 1(1), 7–22.
Ramezani, M., Shier, W.T., Abbas, H.K., Tonos, J.L., Baird, R.E., &Sciumbato, G.L. (2007). Soybean charcoal rot disease fungus Macrophominaphaseolina in Mississippi produces the phytotoxin (−)-botryodiplodin but no detectable phaseolinone. Journal of Natural Products, 70(1), 128-129. ‏
Rezaei, S., &Alizadeh, A. (1998). Soybean damping off due to Phytophthorasojae in Lorestan province. Journal of Plant Diseases. 34:122- 143 (In Persian).
Sadeghi-Garmaroodi, H., MIrabolfathy, M., Babai, H., &Zeinali, H. (2007). Physiological races of Phytophthorasojaein Iran and race–specific reactions of some soybean cultivars. Journal Agriculture Science Technology. 9: 243-249.
Sadeghy, B., Salari, M., ShahidiBonjar, G.H, Panjekeh, N., &Aminnaee, M. (2014). A preliminary study of biological control of citrus gummosis by soil-borne Streptomyces sp. isolates in vitro condition. Archives of Phytopathology and Plant Protection, 47(7), 774-779. ‏
Schmitthenner, A.F. (1999). Phytophthora Rot of Soybean. American Phytopathological Society Press, St. Paul, pp. 39-42.
Schmitthenner, A.F., &van doren, D.M. (1985). Integrated Control of root rot of soybean caused by Phytophthoramegaspermaf.sp. glycinea. In: A.D. Rovira, K.J. Moore, P. T. Wong, W., and J. FKollmorgen (Eds.), Ecology and Management of Soil borne Plant Pathogens. American Phytopathological Society Press, St., Paul.
Shahzad. S., Rajput, A.Q., &Khanzada, M.A. (2018). Effect of different organic substrates and carbon and nitrogen sources on growth and shelf life of trichodermaharzianum. Journal Agriculture Science and Technology. 16: 731-745.
Shariffah-Muzaimah, S.A., Idris, A.S., Madihah, A.Z., Dzolkhifli, O., Kamaruzzaman, S., &Maizatul-Suriza, M. (2018). Characterization of Streptomyces spp. isolated from the rhizosphere of oil palm and evaluation of their ability to suppress basal stem rot disease in oil palm seedlings when applied as powder formulations in a glasshouse trial. World Journal of Microbiology and Biotechnology, 34(1), 15.‏18- 34.
Sharma, S., Kour, D., Rana, K.L., Dhiman, A., &Thakur, S. (2019). Trichoderma: Biodiversity, Ecological Significances, and Industrial Applications. In Recent Advancement in White Biotechnology through Fungi. 85-120.
Sharma, M. (2014). Actinomycetes: source, identification, and their applications. International Journal of Current Microbiology and Applied Sciences. 3(2), 801-32. ‏
Shrivastava, P., Kumar, R., &Yandigeri, M.S. (2017). In vitro biocontrol activity of halotolerant Streptomyces aureofaciens K20: a potent antagonist against Macrophominaphaseolina (Tassi) Goid. Saudi Journal of Biological Sciences. 24(1), 192-199.
Sinclair, J.B., &Backman, P.A. (1989). Compendium of Soybean Disease. Third edition. APS Press, American Phytopathological Society, 106 pp.
Steindorff, A., Ramada, M.H., Coelho, A.S., Miller, R.N., &Pappas, G. (2014). Identification of mycoparasitism-related genes against the phytopathogenSclerotiniasclerotiorum through transcriptome and expression profile analysis in Trichoderma harzianum. BMC Genomics. 15, 204- 217.
Stirling, G.R. (2017). Biological control of plant-parasitic nematodes. In Diseases of nematodes. CRC Press: 103-150.
 Tapwal, A., &Pandey, H. (2016). In vitro evaluation of Trichoderma species for virulence efficacy on Botryodiplodiapalmarum. Current Life Sciences. (2), 86–91.
Tapwal, A., Singh, U., Singh, G., Garg, S., & Kumar, R. (2011). In vitro antagonism of Trichoderma viride against five phytopathogens. Pest Technology. 5(1), 59–62.
Tchameni, S.N., Sameza, M.L., O’donovan, A., Fokom, R., &MangaptcheNgonkeu, E.L. (2017). Antagonism of Trichoderma asperellum against Phytophthoramegakarya and its potential to promote cacao growth and induce biochemical defence. Mycology, 8(2), 84-92. ‏
Valois, D., Fayad, K., Barasubiye, T., Garon, M., &Brzezinski, R. (1996). GlucanolyticActinomycetes antagonistic to Phytophthorafragariae var. rubi, the causal agent of raspberry root rot. Applied and Environmental Microbiology. 62(5), 1630–1635.
VazJauri, P., Altier, N., &Kinkel, L.L. (2016). Streptomyces for sustainability. In: Castro-Sowinski S (ed) Microbial models: from environment to industrial sustainability, microorganism for sustainability (Book). 251–276.
Verma, V.C., Singh, S.K., &Prakash, S. (2011). Bio‐control and plant growth promotion potential of siderophore producing endophytic Streptomyces from Azadirachtaindica A. Juss. Journal of Basic Microbiology, 51(5), 550-556. ‏
Vieira, P.M., Coelho, AS., Steindorff, A.S., de Siqueira, S.J., &Silva, R.N. (2013). Identification of differentially expressed genes from Trichoderma harzianum during growth on cell wall of Fusarium solani as a tool for biotechnological application. BMC Genomics (14), 177e187.
Vinodkumar, S., Indumathi, T., &Nakkeeran, S. (2017). Trichoderma asperellum (NVTA2) as a potential antagonist for the management of stem rot in carnation under protected cultivation. Biological Control, (113), 58-64. ‏
Vitti, A., Pellegrini, E., Nali, C., Lovell, i S., &Sofo, A. (2016). Trichoderma harzianum T-22 induces systemic resistance in tomato infected by Cucumber mosaic virus. Frontiers in Plant Science, (7), 1520. ‏
White, T.J., Bruns, T., Lee, S., &Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. eds. by MA Innis, DH Gelfand, JJ Sninsky and TJ White, In: PCR Protocols: a guide to methods and applications. 315-322.
Woo, S.L., Ruocco, M., Vinale, F., Nigro, M., Marra, R., Lombardi, N., Pascale, A., Lanzuise, S., Manganiello, G., &Lorito, M. (2014). Trichoderma-based Products and their Widespread Use in Agriculture. The OpenMycology Journal, 8, 71-126.
Wu, Y., Yuan, J., Yaoyao, E., Raza, W., Shen, Q., &Huan, Q. (2015). Effects of volatile organic compounds from Streptomyces albulus NJZJSA2 on growth of two fungal pathogens. Journal of Basic Microbiolg. (55), 1104–1117.
Xiao, K., Kinkel, L.L., Samac, D.A. (2002). Biological control of Phytophthora root rots on alfalfa and soybean with Streptomyces. Biological Control. 23(3), 285–295.
Yuan, S., Li, M., Fang, Z., Liu, Y., Shi, W., Pan, B., &Shen, Q. (2016). Biological control of tobacco bacterial wilt using Trichoderma harzianum amended bioorganic fertilizer and the arbuscular mycorrhizal fungi Glomus mosseae. Biological Control, (92), 164-171.