Fungal Biocontrol Agents and Their Secondary Metabolites

Abstract

The fungus produces a large number of secondary metabolites of low molecular weight called polyketides, non-ribosomal peptides and terpenes. Although not directly involved in basic metabolic processes such as growth and energy production, secondary metabolites exhibit a range of biological activities that contribute to the survival of the producer organism in an occupied ecological niche. Studies on the use of secondary metabolites produced by fungi for biocontrol of pests, weeds and diseases due to exhibited bioactivity have been intensively concentrated in the last 10 years.

Keywords

• Fungus,Biocontrol,Secondary metabolite,Bioactivity

Fungal Biyokontrol Ajanları ve Metabolitleri

Abstract

Funguslar poliketidler, ribozomal olmayan peptitler ve terpenler olarak adlandırılan düşük moleküler ağırlıklı çok fazla sayıda sekonder metabolitler üretirler.  Büyüme ve enerji üretimi gibi temel metabolik süreçlere doğrudan dahil olmasalar da, sekonder metabolitler işgal edilen bir ekolojik niş içinde üretici organizmanın hayatta kalmasına katkıda bulunan bir dizi biyolojik aktivite sergilerler. Sergilenen biyoaktivite nedeniyle zararlı böceklerin, yabancı otların ve hastalıkların biyokontrolüne yönelik olarak fungusların ürettikleri sekonder metabolitlerin kullanımı ile ilgili çalışmalar son 10 yılda önemli ölçüde yoğunlaşmıştır.

Keywords

• Fungus,Biyokontrol,Sekonder metabolit,Biyoaktivite

References

1. Referans 1: Abbas H.K., Smeda R.J., Gerwick B.C., Shier W.T.,Fumonisin B1 from the fungus Fusarium moniliforme causes contact toxicity in plants: evidence from studies with biosynthetically labeled toxin. J Nat Toxins,8(3):405-20, (1999).
2. Referans 2: Akbaş B., Yaşarer A.H., Şimşek M., Biyolojik Mücadele Araştırmaları Ve Uygulamaya Yansımaları, Gıda Tarım ve Hayvancılık Bakanlığı, Tarımsal Araştırmalar ve Politikalar Genel Müdürlüğü, TÜRKTOB, http://www.turktob.org.tr/dergi/makaleler/dergi18/47-51.pdf, (2015).
3. Referans 3: An Z., Handbook of Industrial Mycology, Mycology, Marcel Dekker, New York, (2004).
4. Referans 4: Anderson K.I., Hallett S.G., Herbicidal spectrum and activity of Myrothecium verrucaria, Weed Science, 52(4): 623-627, (2003).
5. Referans 5: Atay, T., Asav, Ü., Önen, H., Kara, K., İstilacı Yabancı Otlarla Biyolojik Mücadele (Biological Control of Invasive alien plants), Türkiye İstilacı Bitkiler Kataloğu, T.C. Gıda, Tarım Ve Hayvancılık Bakanlığı Tarımsal Araştırmalar ve Politikalar Genel Müdürlüğü Bitki Sağlığı Araştırmaları Daire Başkanlığı, (2015).
6. Referans 6: Birişik N., Kütük H., Karacaoğlu M., Yarpuzlu F., İslamoğlu M., Öztemiz S., Teoriden Pratiğe Biyolojik Mücadele, T.C Gıda Tarım ve Hayvancılık Bakanlığı, Ankara, (2012).
7. Referans 7: Błaszczyk L., Siwulski M., Sobieralski K., Lisiecka J., Jędryczka M., Trichoderma spp, application and prospects for use in organic farming and industry, J. Plant Protec. Res., 54 (4), 309–317, (2014).
8. Referans 8: Boari A., Evidente A., Idris A.E., Abouzeid M.A.,Identification of phytotoxic metabolites of a new Fusarium sp. inhibiting germination of Striga hermonthica seeds, Phytopathologia Mediterranea, 42 (1): 65-70, (2003).

9. Referans 9: Bobylev M.M., Bobyleva L.I., Strobel G.A., Synthesis and Bioactivity of Analogs of Maculosin, a Host-Specific Phytotoxin Produced by Alternaria alternata on Spotted Knapweed (Centaurea maculosa), Journal of Agricultural and Food Chemistry, 44 (12), (1996).
10. Referans 10: Boruta T., Uncovering the repertoire of fungal secondary metabolites: From Fleming’s laboratory to the International Space Station, Bioengineered, 9 (1), 12–16, (2018).
11. Referans 11: Brakhage A.A., Regulation of fungal secondary metabolism, Nature Reviews Microbiology, 11(1): 21-32, (2013).
12. Referans 12: Brakhage A.A., Schroeckh V., Fungal secondary metabolites - Strategies to activate silent gene clusters, Fungal Genetics and Biology, 48, 15–22, (2011).Referans 13: Brotman Y., Briff E., Viterbo A., Chet I., Role of swollenin, an expansin-like protein from Trichoderma, in plant root colonization, Plant Physiol., 147, 779–789, (2008).
13. Referans 14: Butt T.M., Jackson C., Magan N., Fungi as Biocontrol Agents, Progress, Problems and Potential, CABI Publishing, CAB International, (2001).
14. Referans 15: Calvo A.M., Wilson R.A., Bok J.W., Keller N.P., Relationship between Secondary Metabolism and Fungal Development, Microbiology and Molecular Biology Reviews, 66 (3):447-59. (2002).
15. Referans 16: Cantürk Z.,Aspergillus ve Penicillium cinslerine ait sekonder metabolitler ve sınıflandırılması, Elektronik Mikrobiyoloji Dergisi TR, 13 (2), 1-8, (2015).Referans 17: Chet I., Inbar J., Biological control of fungal pathogens, Appl. Biochem. Biotechnol., 48, 37–43, (1994).
16. Referans 18: Clarkson J.P., Mead A., Payne T., Whipps J.M., Effect of environmental factors and Sclerotium cepivorum isolate on sclerotial degradation and biological control of white rot by Trichoderma spp, Plant Pathol., 53, 353–362, (2004).
17. Referans 19: Compant S., van der Heijden M.G.A., Sessitsch A.,Climate change effects in beneficial plant-microorganism interactions, FEMS Microbiol. Ecol., 73, 197–214, (2010).
18. Referans 20: Cripps-Guazzone N., Jones E.E., Condron L.M., McLean K.L., Stewart A., Ridgway H.J., Rhizosphere and endophytic colonisation of ryegrass and sweet corn roots by the isolate Trichoderma atroviride LU132 at different soil pHs. New Zealand Plant Protec., 69, 78–85, (2016).
19. Referans 21: Daguerre Y., Siegel K., Edel-Hermann V., Steinberg C., Fungal proteins and genes associated with biocontrol mechanisms of soil-borne pathogens, Fungal Biol. Rev., 28, 97–125, (2014).
20. Referans 22: Domingues M.V.P.F., de Moura K.E., Salamao D., Elias L.M., Patricio F.R.A., Effect of temperature on mycelial growth of Trichoderma, Sclerotinia minor and S. sclerotiorum, as well as on mycoparasitism, Summa Phytopathol., Botucatu, 42 (3), 222-227, 2016.
21. Referans 23: Dong C.,Yu J., Zhu Y., Dong C.,Inhibition of hepatitis B virus gene expression & replication by crude destruxins from Metarhizium anisopliae var. Dcjhyium, Indian J Med Res., 138(6):969-76, (2013).
22. Referans 24: Esfahani K., Motallebi M., Zamani M.R., Sohi H.H., Jourabchi E.,Transformation of potato (Solanum tuberosum cv. Savalan) by chitinase andβ 1,3 glucanase genes of mycoparasitic fungi towards improving resistance to Rhizoctonia solani AG-3. Iranian Journal of Biotechnology, 8 (2) 73–81, (2010).
23. Referans 25: Fan J.Q., Chen X.R., Hu Q.B.,Effects of Destruxin A on Hemocytes Morphology of Bombyx mori, Journal of Integrative Agriculture, 12(6): 1042-1048, (2013).
24. Referans 26: Fox E.M., Howlett B.J.,Secondary metabolism: regulation and role in fungal biology, Current Opinion in Microbiology, 11:481–487, (2008).
25. Referans 27: Gajera H., Domadiya R., Patel S., Kapopara M., Golakiya B.,Molecular mechanism of Trichoderma as bio-control agents against phytopathogen system, Curr. Res. Microbiol. Biotechnol., 1, 133–142, (2013).
26. Referans 28: Geraldine A.M., Cardoso Lopes F.A., Costa Carvalho D.D., Barbosa E.T., Rodrigues A.R., Brandão R.S., Ulhoa C.J., Junior M.L.,Cell wall-degrading enzymes and parasitism of sclerotia are key factors onfield biocontrol of white mold by Trichoderma spp, Biol. Control, 67, 308–316, (2013).
27. Referans 29: Ghabrial S.A., Suzuki N.,Viruses of plant pathogenic fungi, Annu. Rev. Phytopathol., 47, 353–384, (2009).
28. Referans 30: Ghorbanpour M., Omidvari M., Abbaszadeh-Dahaji P., Omidvar R., Kariman K., Mechanisms underlying the protective effects of beneficial fungi against plant diseases, Biological Control, 117 147-157, (2017).
29. Referans 31: Gilbert L.I., Gill S.S.,Insect Control Biological And Synthetic Agents, Chapter 11, Academic Press, Elsevier 2010, (2010).
30. Referans 32: Gupta V.K.,Mach R.L.,Sreenivasaprasad S.,Fungal Biomolecules: Sources, Applications and Recent Developments, ISBN: 978-1-118-95829-2, Apr 2015, Wiley-Blackwell, (2015).
31. Referans 33: Guzmán-Guzmán P., Alemán-Duarte M.I., Delaye L., Herrera-Estrella A., OlmedoMonfi V., Identification of effector-like proteins in Trichoderma spp. and role of a hydrophobin in the plant-fungus interaction and mycoparasitism, BMC, Genetics, 18, 16, (2017).
32. Referans 34: Harman G.E., Howell C.R., Viterbo A., Chet I., Lorito M.,Trichoderma species opportunistic, avirulent plant symbionts, Nat. Rev. Microbiol., 2, 43–56, (2004).
33. Referans 35: Hermosa R., Cardoza M.B., Rubio M.E., Gutiérrez S., Monte E., Secondary metabolism and antimicrobial metabolites of Trichoderma, In: Gupta, V.K., Schmoll, M., Herrera-Estrella, A., Upadhyay, R.S., Druzhinina, i., Tuohy, M. (Eds.), Biotechnology and Biology of Trichoderma, Elsevier, The Netherlands, pp. 125–137, (2014).
34. Referans 36: Hermosa R., Rubio M.E., Cardoza M.B., Nicolás E., Monte E., Gutiérrez S.,The contribution of Trichoderma to balancing the costs of plant growth and defense, Int. Microbiol., 16, 69–80, (2013).
35. Referans 37: Hoagland R.E.,Boyette C.D., Weaver M.A., Abbas H.K., Bioherbicides: Research And Risks, Toxin Reviews, 26:4, 313-342, (2008).
36. Referans 38: Hoitink H.A.J., Maden L.V., Dorrance A.E.,Systemic resistance induced by Trichoderma spp.: interactions between the host, the pathogen, the biocontrol agent, and soil organic matter quality, Phytopathology, 96, 196–1189, (2006).
37. Referans 39: Jayawardena R.S., Li X.H., Liu M., Zhang W., Yan J.Y., Mycosphere Essay 16: Colletotrichum: Biological control, biocatalyst, secondary metabolites and toxins,Mycosphere, 7(8), 1164-1176, (2016).
38. Referans 40: Jelen H., Blaszczyk L., Chelkowski J., Rogowicz K., Strakowska J.,Formation of 6-n-pentyl-2H-pyran-2-one (6-PAP) and other volatiles by different Trichoderma species,Mycol. Progress, 13 (3), 589–600, (2013).
39. Referans 41: Kredics L., Antal Z., Manczinger L., Szekeres A., Kevei F., Nagy E.,Influence of environmental parameters on Trichoderma strains with biocontrol potential, Food Technol., Biotechnol, 41, 37–42, (2003).
40. Referans 42: Kubicek C.P., Herrera-Estrella A., Seidl-Seiboth V., Martinez D.A., Druzhinina I.S., Thon M., Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma, Genome Biol., 12 (R40), 1-15, (2011).
41. Referans 43: Kumar S.,Trichoderma; a biological weapon for managing plant diseases and promoting sustainability, Int. J. Agric. Sci. Vet. Med., 1 (3), 1–16, (2013).
42. Referans 44: Liu M., Sun Z.X., Zhu J., Xu T., Harman G.E., Lorito M.,Enhancing rice resistance to fungal pathogens by transformation with cell wall degrading enzymegenes from Trichoderma atroviride, J. Zhejiang Univ. Sci. 5, 133–136, (2004).
43. Referans 45: Lopes F.A., Steindorff A.S., Geraldine A.M., Brandao R.S., Monteiro V.N., Lobo Jr. M., Coelho A.S., Ulhoa C.J., Silva R.N.,Biochemical and metabolic profiles of Trichoderma isolates isolated from common bean crops in the Brazilian Cerrado, and potential antagonism against Sclerotinia sclerotiorum, Fung. Biol., 116, 815–824, (2012).
44. Referans 46: Maimala S.,Tartar A., Boucias D., Chandrapatya A., Detection of the toxin Hirsutellin A from Hirsutella thompsonii, Journal of Invertebrate Pathology, 80 (2):112-26, (2002).
45. Referans 47: Malik R.J., Dixon M.H., Bever J.D.,Mycorrhizal composition can predict foliar pathogen colonization in soybean, Biol. Control, 103, 46–53, (2016).
46. Referans 48: Massart S., Perazzolli M., Hofte M., Pertot I., Jijakli M.H.,Impact of the omic technologies for understanding the modes of action of biological control agents against plant pathogens, Biocontrol 60, 725, (2015).
47. Referans 49: Mohan V., Nivea R., Menon S., Evaluation of ectomycorrhizal fungi as potential bio-control agents against selected plant pathogenic fungi, JAIR, 3, 408–412, (2015).
48. Referans 50: Mokhtar H., Aid D.,Contribution in isolation and identification of some pathogenic Fungi from wheat seeds, and evaluation of antagonistic capability of Trichoderma harzianum against those isolated Fungi in vitro, Agric. Biol. J. N. Am, 4(2), 145–154, (2013).
49. Referans 51: Morán-DiezE., Hermosa R., Ambrosino P., Cardoza R.E., Gutiérrez S., Lorito M., Monte E., The ThPG1 endopolygalacturonase is required for the Trichoderma harzianum–plant beneficial interaction, Mol. Plant Microbe Interact, 22, 1021–1031, (2009).
50. Referans 52: Mukherjee P.K., Horwitz B.A., Kenerley C.M.,Secondary metabolism in Trichoderma - genomic perspective, Microbiology, 158(Pt 1): 35-45, (2012).
51. Referans 53: Mukherjee P.K., Horwitz B.A., Singh U.S., Mukherjee M., Schmoll M.,Trichoderma in Agriculture, Industry and Medicine: An Overview, Trichoderma: Biology and Applications, CABI, Oxford, 1-10, (2013).
52. Referans 54: Nair A., Kolet S.P., Thulasiram H.V., Bhargava S., Systemic jasmonic acid modulation in mycorrhizal tomato plants and its role in induced resistance against Alternaria alternata, Plant Biol., 17 (3), 625–663, (2014).
53. Referans 55: Nassimi Z., Taheri P., Endophytic fungus Piriformospora indica induced systemic resistance against rice sheath blight via affecting hydrogen peroxide and antioxidants, Biocontrol Sci. Technol., 27, 1–16, (2017).
54. Referans 56: Özaslan Ö.,Diyarbakır ili buğday ve pamuk ekim alanlarında sorun olan yabancı otlar ile üzerindeki fungal etmenlerin tespiti ve bio-etkinlik potansiyellerinin araştırılması, Selçuk Üniversitesi, Fen Bilimleri Enstitüsü, Bitki Koruma Anabilim Dalı, Doktora Tezi, Konya, (2011).
55. Referans 57: Pelaez F., Biological activities of fungal metabolites, Handbook of Industrial Mycology,(ed. An, Z.), 49–92, (Marcel Dekker, New York, (2005).
56. Referans 58: Ramesha A.,Venkataramana M., Nirmaladevi D., Gupta V.K., Chandranayaka S., Srinivas C., Cytotoxic effects of oosporein isolated from endophytic fungus Cochliobolus kusanoi, Frontiers in Microbiology, 1; 1-12, (2015).
57. Referans 59: Rubio M.E, Quijada N.M, Pérez E., Dominguez S., Monte E., Hermosa R., Identifying beneficial qualities of Trichoderma parareesei for plants, Appl. Environ. Microbiol., 80, 1864–1873, (2014).
58. Referans 60: Salar R.K., Gahlawat S.K., Siwach P., Duhan J.S., Biotechnology: Prospects and Applications, Springer, (2013).
59. Referans 61: Saxena S.,Applied Microbiology, Springer India, 2015, DOI:10.1007/978-81-322 2259-0, (2015).
60. Referans 62: Scharf D.H., Brakhage A.A., Mukherjee P.K.,Gliotoxin, bane or boon?, Environ. Microbiol., 18(4), 1096–1109. (2016).
61. Referans 63: Seidl V., Huemer B., Seiboth B., Kubicek C.P.,A complete survey of Trichoderma chitinases reveals three distinct subgroups of family 18 chitinases, FEBS J., 272, 5923–5939, (2005).
62. Referans 64: Sghir F., TouatiJ., Mouria B., Selmoui K., Touhami A.O., Filali-Maltouf A., Modafar C.E., Moukhli A., Benkirane R., Douira A., Effect of Trichoderma harzianum and endomycorrhizae on growth and Fusarium wilt of tomato and eggplant, WJPLS 2 (3), 69–93, (2016).
63. Referans 65: Shoresh M., Yedidia I., Chet I.,Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203, Phytopathology, 95, 76–84, (2005).
64. Referans 66: Singh S., Pandey R.K., Goswami B.K.,Bio-control activity of Purpureocillium lilacinum strains in managing root-knot disease of tomato caused by Meloidogyne incognita, Biocontrol Sci. Technol., 23 (12), 1469–1489, (2013).
65. Referans 67: SolgiT., Moradyar M., Zamani M.R., Motallebi M.,Transformation of Canola by chit33 gene towards improving resistance to Sclerotinia sclerotiorum, Plant Protec. Sci., 51 (1), 1–5, (2015).
66. Referans 68: Sree K.S., Padmaja V., Murthy Y.L.N., Insecticidal activity of the mycotoxin, destruxin from Metarhizium anisopliae (Hypocreales) strains against Spodoptera litura (Lepidoptera: Noctuidae) larval stages, Pest Manage. Sci., 2008; 64:119-125, (2008).
67. Referans 69: Sree K.S., Varma A.,Biocontrol of Lepidopteran Pests: Use of Soil Microbes and their Metabolites, Soil Biology, Springer International, (2015).
68. Referans 70: Strakowska J., Błaszczyk L., Chełkowski J.,The significance of cellulolytic enzymes produced by Trichoderma in opportunistic lifestyle of this fungus, J. Basic Microb., 54, 1–12, (2014).
69. Referans 71: Szekeres A., Leitgeb B., Kredics L., Vágvölgyi C.,Peptaibols and Related Peptaibiotics of Trichoderma,Acta Microbiologica et Immunologica Hungarica,52(2):137-68, (2005).
70. Referans 72: Tahat M., Kamaruzaman S., Othman R.,Mycorrhizal fungi as a biocontrol agent, Plant Pathol. J., 9, 198–207, (2010).
71. Referans 73: Tuão Gava C.A., Pinto J.M.,Biocontrol of melon wilt caused by Fusarium oxysporum Schlect f. sp. melonis using seed treatment with Trichoderma spp. and liquid compost, Biol. Control, 97, 13–20, (2016).
72. Referans 74: Uygun N., Ulusoy M.R., Satar S., Biyolojik Mücadele, Türk. biyo. müc. derg., 2010, 1 (1): 1-14, ISSN 2146-0035, (2010).
73. Referans 75: Vagelas I., Leontopoulos S.,Cross-protection of cotton against Verticillium wilt by Verticillium nigrescens, Emir. J. Food Agric., 27 (9), 687–691, (2015).
74. Referans 76: Varejão E.V.V., Demuner A.J., Barbosa L.C.A., Barreto R.W.,Phytotoxic effects of metabolites from Alternaria euphorbiicola against its host plant Euphorbia heterophylla, Quim. Nova, Vol. 36, No. 7, 1004-1007, 2013, (2013).
75. Referans 77: Viterbo A., Chet I.,TasHyd1, a new hydrophobin gene from the biocontrol agent Trichoderma asperellum, is involved in plant root colonization, Mol. Plant Pathol., 7, 249–258, (2006).
76. Referans 78: Vos C.M., De Cremer K., Cammue B.P.A., De Coninck B.,The toolbox of Trichoderma spp. inthe biocontrol of Botrytis cinerea disease, Mol. Plant Pathol., 16, 400–412, (2015).
77. Referans 79: Vos C.M., Yang Y., De Coninck B., Cammue B.P.A.,Fungal (-like) biocontrol organisms in tomato disease control, Biol. Control, 74, 65–81, (2014).
78. Referans 80: Wang G., Liu Z., Lin R., Li E., Mao Z., Ling J., Yang Y., Yin W., Xie B.,Biosynthesis of antibiotic leucinostatins in bio-control fungus Purpureocillium lilacinum and their inhibition on phytophthora revealed by genome mining, PLoS Pathog., 12 (7), (2016).
79. Referans 81: Woo S.L., Donzelli B., Scala F., Mach R.L., Harman G.E., Kubicek C.P., Del Sorbo G., Lorito M.,Disruption of the ech42 (endochitinase-encoding) gene affects biocontrol activity in Trichoderma harzianum P1. Mol. Plant-Microbe Interact., 12, 419–429, (1999).
80. Referans 82: Xiang M., Chen S., Wang L., Dong Z., Huang J., Zhang Y., Strasser R.J.,Effect of vulculic acid produced by Nimbya alternantherae on the photosynthetic apparatus of Alternanthera philoxeroides,Plant Physiol Biochem, 65: 81-8, doi: 10.1016/j.plaphy.2013.01.013, (2013).
81. Referans 83: You J., Zhang J., Wu M., Yang L., Chen W., Li G.,Multiple criteria-based screening of Trichoderma isolates for biological control of Botrytis cinerea on tomato, Biol. Control, 101, 31–38, (2016).
82. Referans 84: Yu X., Li B., Fu Y., Xie J., Cheng J., Ghabrial S.A., Li G., Yi X., Jiang D.,Extracellular transmission of a DNA mycovirus and its use as a natural fungicide, Proc. Natl. Acad. Sci. U.S.A., 110, 1452–1457, (2013).