The Potential of Rhizoctonia-Like Fungi for the Biological Protection of Cereals against Fungal Pathogens

. 2021 Feb 12 ; 10 (2) : . [epub] 20210212

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33673058

Grantová podpora
MZE-RO1118 Ministerstvo Zemědělství
QK1910197 Ministerstvo Zemědělství
MUNI/A/1378/2019 Masarykova Univerzita
IGA-Prf-2021-001 Univerzita Palackého v Olomouci

The use of biological control is becoming a common practice in plant production. One overlooked group of organisms potentially suitable for biological control are Rhizoctonia-like (Rh-like) fungi. Some of them are capable of forming endophytic associations with a large group of higher plants as well as mycorrhizal symbioses. Various benefits of endophytic associations were proved, including amelioration of devastating effects of pathogens such as Fusarium culmorum. The advantage of Rh-like endophytes over strictly biotrophic mycorrhizal organisms is the possibility of their cultivation on organic substrates, which makes their use more suitable for production. We focused on abilities of five Rh-like fungi isolated from orchid mycorrhizas, endophytic fungi Serendipita indica, Microdochium bolleyi and pathogenic Ceratobasidium cereale to inhibit the growth of pathogenic F. culmorum or Pyrenophora teres in vitro. We also analysed their suppressive effect on wheat infection by F. culmorum in a growth chamber, as well as an effect on barley under field conditions. Some of the Rh-like fungi affected the growth of plant pathogens in vitro, then the interaction with plants was tested. Beneficial effect was especially noted in the pot experiments, where wheat plants were negatively influenced by F. culmorum. Inoculation with S. indica caused higher dry shoot biomass in comparison to plants treated with fungicide. Prospective for future work are the effects of these endophytes on plant signalling pathways, factors affecting the level of colonization and surviving of infectious particles.

Zobrazit více v PubMed

Williams P.G. Orchidaceous Rhizoctonias in Pot Cultures of Vesicular–Arbuscular Mycorrhizal Fungi. Can. J. Bot. 1985;63:1329–1333. doi: 10.1139/b85-186. DOI

Bokati D. The Cryptic Sebacinales: An Obscure but Ubiquitous Group of Root Symbionts Comes to Light. Fungal Ecol. 2016;2:115–119. doi: 10.1016/j.funeco.2016.01.010. DOI

Weiß M., Waller F., Zuccaro A., Selosse M. Sebacinales—One Thousand and One Interactions with Land Plants. New Phytol. 2016;211:20–40. doi: 10.1111/nph.13977. PubMed DOI

Dearnaley J.D.W., Martos F., Selosse M.-A. 12 Orchid Mycorrhizas: Molecular Ecology, Physiology, Evolution and Conservation Aspects. In: Hock B., editor. Fungal Associations. Springer; Berlin/Heidelberg, Germany: 2012. pp. 207–230.

Moore R. The Genera of Rhizoctonia-like Fungi: Ascorhizoctonia, Ceratorhiza Gen. Nov., Epulorhiza Gen. Nov., Moniliopsis, and Rhizoctonia. Mycotaxon. 1987;29:91–99.

Oberwinkler F., Riess K., Bauer R., Selosse M.-A., Weiß M., Garnica S., Zuccaro A. Enigmatic Sebacinales. Mycol. Prog. 2013;12:1–27. doi: 10.1007/s11557-012-0880-4. DOI

Weiß M., Sýkorová Z., Garnica S., Riess K., Martos F., Krause C., Oberwinkler F., Bauer R., Redecker D. Sebacinales Everywhere: Previously Overlooked Ubiquitous Fungal Endophytes. PLoS ONE. 2011;6:e16793. doi: 10.1371/journal.pone.0016793. PubMed DOI PMC

Gónzalez D., Rodriguez-Carres M., Boekhout T., Stalpers J., Kuramae E.E., Nakatani A.K., Vilgalys R., Cubeta M.A. Phylogenetic Relationships of Rhizoctonia Fungi within the Cantharellales. Fungal Biol. 2016;120:603–619. doi: 10.1016/j.funbio.2016.01.012. PubMed DOI PMC

Warcup J.H. Mycorrhizal Associations of Isolates of Sebacina Vermifera. New Phytol. 1988;110:227–231. doi: 10.1111/j.1469-8137.1988.tb00256.x. DOI

Oberwinkler F., Riess K., Bauer R., Garnica S. Morphology and Molecules: The Sebacinales, a Case Study. Mycol. Prog. 2014;13:445–470. doi: 10.1007/s11557-014-0983-1. DOI

Verma S., Varma A., Rexer K.-H., Hassel A., Kost G., Sarbhoy A., Bisen P., Bütehorn B., Franken P. Piriformospora Indica, Gen. et Sp. Nov., a New Root-Colonizing Fungus. Mycologia. 1998;90:896–903. doi: 10.1080/00275514.1998.12026983. DOI

Shoresh M., Harman G.E., Mastouri F. Induced Systemic Resistance and Plant Responses to Fungal Biocontrol Agents. Annu. Rev. Phytopathol. 2010;48:21–43. doi: 10.1146/annurev-phyto-073009-114450. PubMed DOI

Waller F., Achatz B., Baltruschat H., Fodor J., Becker K., Fischer M., Heier T., Huckelhoven R., Neumann C., von Wettstein D., et al. The Endophytic Fungus Piriformospora Indica Reprograms Barley to Salt-Stress Tolerance, Disease Resistance, and Higher Yield. Proc. Natl. Acad. Sci. USA. 2005;102:13386–13391. doi: 10.1073/pnas.0504423102. PubMed DOI PMC

Card S., Johnson L., Teasdale S., Caradus J. Deciphering Endophyte Behaviour: The Link between Endophyte Biology and Efficacious Biological Control Agents. FEMS Microbiol. Ecol. 2016;92:fiw114. doi: 10.1093/femsec/fiw114. PubMed DOI

Látalová K., Baláž M. Carbon Nutrition of Mature Green Orchid Serapias Strictiflora and Its Mycorrhizal Fungus Epulorhiza sp. Biol. Plant. 2010;54:97–104. doi: 10.1007/s10535-010-0014-2. DOI

Rodriguez R.J., Jr., Arnold A.E., Redman R.S. Fungal Endophytes: Diversity and Functional Roles. New Phytol. 2009;182:314–330. doi: 10.1111/j.1469-8137.2009.02773.x. PubMed DOI

Brader G., Compant S., Vescio K., Mitter B., Trognitz F., Ma L.-J., Sessitsch A. Ecology and Genomic Insights into Plant-Pathogenic and Plant-Nonpathogenic Endophytes. Annu. Rev. Phytopathol. 2017;55:61–83. doi: 10.1146/annurev-phyto-080516-035641. PubMed DOI

Jiang J.-H., Tam S.-L., Toda T., Chen L.-C. Controlling Rhizoctonia Damping-off of Chinese Mustard by Using Endomycorrhizal Rhizoctonia Spp. Isolated from Orchid Mycorrhizae. Plant Dis. 2016;100:85–91. doi: 10.1094/PDIS-06-14-0597-RE. PubMed DOI

Mosquera-Espinosa A.T., Bayman P., Prado G.A., Gómez-Carabalí A., Otero J.T. The Double Life of Ceratobasidium: Orchid Mycorrhizal Fungi and Their Potential for Biocontrol of Rhizoctonia Solani Sheath Blight of Rice. Mycologia. 2013;105:141–150. doi: 10.3852/12-079. PubMed DOI

Bungtongdee N., Sopalun K., Laosripaiboon W., Iamtham S. The Chemical Composition, Antifungal, Antioxidant and Antimutagenicity Properties of Bioactive Compounds from Fungal Endophytes Associated with Thai Orchids. J. Phytopathol. 2019;167:56–64. doi: 10.1111/jph.12773. DOI

O’Brien P.A. Biological Control of Plant Diseases. Australas. Plant Pathol. 2017;46:293–304. doi: 10.1007/s13313-017-0481-4. DOI

Gilbert J., Haber S. Overview of Some Recent Research Developments in Fusarium Head Blight of Wheat. Can. J. Plant Pathol. 2013;35:149–174. doi: 10.1080/07060661.2013.772921. DOI

Sanjay R., Ponmurugan P., Baby U.I. Evaluation of Fungicides and Biocontrol Agents against Grey Blight Disease of Tea in the Field. Crop Prot. 2008;27:689–694. doi: 10.1016/j.cropro.2007.09.014. DOI

Silva V., Mol H.G.J., Zomer P., Tienstra M., Ritsema C.J., Geissen V. Pesticide Residues in European Agricultural Soils—A Hidden Reality Unfolded. Sci. Total Environ. 2019;653:1532–1545. doi: 10.1016/j.scitotenv.2018.10.441. PubMed DOI

Harman G.E. Multifunctional Fungal Plant Symbionts: New Tools to Enhance Plant Growth and Productivity: Commentary. New Phytol. 2011;189:647–649. doi: 10.1111/j.1469-8137.2010.03614.x. PubMed DOI

Jaber L.R. Seed Inoculation with Endophytic Fungal Entomopathogens Promotes Plant Growth and Reduces Crown and Root Rot (CRR) Caused by Fusarium Culmorum in Wheat. Planta. 2018;248:1525–1535. doi: 10.1007/s00425-018-2991-x. PubMed DOI

Kuga Y., Sakamoto N., Yurimoto H. Stable Isotope Cellular Imaging Reveals That Both Live and Degenerating Fungal Pelotons Transfer Carbon and Nitrogen to Orchid Protocorms. New Phytol. 2014;202:594–605. doi: 10.1111/nph.12700. PubMed DOI

Scherm B., Balmas V., Spanu F., Pani G., Delogu G., Pasquali M., Migheli Q. Fusarium Culmorum: Causal Agent of Foot and Root Rot and Head Blight on Wheat: The Wheat Pathogen. Fusarium Culmorum. Mol. Plant Pathol. 2013;14:323–341. doi: 10.1111/mpp.12011. PubMed DOI PMC

Tóth B., Kászonyi G., Bartók T., Varga J., Mesterházy Á. Common Resistance of Wheat to Members of the Fusarium Graminearum Species Complex and F. Culmorum: Common Wheat Resistance to Fusarium Graminearum Species Complex. Plant Breed. 2008;127:1–8. doi: 10.1111/j.1439-0523.2008.01412.x. DOI

Hogg A.C., Johnston R.H., Johnston J.A., Klouser L., Kephart K.D., Dyer A.T. Monitoring Fusarium Crown Rot Populations in Spring Wheat Residues Using Quantitative Real-Time Polymerase Chain Reaction. Phytopathology. 2010;100:49–57. doi: 10.1094/PHYTO-100-1-0049. PubMed DOI

McMullen M., Bergstrom G., De Wolf E., Dill-Macky R., Hershman D., Shaner G., Van Sanford D. A Unified Effort to Fight an Enemy of Wheat and Barley: Fusarium Head Blight. Plant Dis. 2012;96:1712–1728. doi: 10.1094/PDIS-03-12-0291-FE. PubMed DOI

McCormick S.P., Stanley A.M., Stover N.A., Alexander N.J. Trichothecenes: From Simple to Complex Mycotoxins. Toxins. 2011;3:802. doi: 10.3390/toxins3070802. PubMed DOI PMC

Walter S., Nicholson P., Doohan F.M. Action and Reaction of Host and Pathogen during Fusarium Head Blight Disease. New Phytol. 2010;185:54–66. doi: 10.1111/j.1469-8137.2009.03041.x. PubMed DOI

Pestka J.J. Deoxynivalenol: Mechanisms of Action, Human Exposure, and Toxicological Relevance. Arch. Toxicol. 2010;84:663–679. doi: 10.1007/s00204-010-0579-8. PubMed DOI

Lee H.J., Ryu D. Worldwide Occurrence of Mycotoxins in Cereals and Cereal-Derived Food Products: Public Health Perspectives of Their Co-Occurrence. J. Agric. Food Chem. 2017;18:7034–7051. doi: 10.1021/acs.jafc.6b04847. PubMed DOI

Al-Hatmi A.M.S. Current Antifungal Treatment of Fusariosis. Int. J. Antimicrob. Agents. 2018;7:326–332. doi: 10.1016/j.ijantimicag.2017.06.017. PubMed DOI

Czembor E., Stępień Ł., Waśkiewicz A. Effect of Environmental Factors on Fusarium Species and Associated Mycotoxins in Maize Grain Grown in Poland. PLoS ONE. 2015;10:e0133644. doi: 10.1371/journal.pone.0133644. PubMed DOI PMC

Dweba C.C. Fusarium Head Blight of Wheat: Pathogenesis and Control Strategies. Crop Prot. 2017;9:114–122. doi: 10.1016/j.cropro.2016.10.002. DOI

Antalová Z., Bleša D., Martinek P., Matušinsky P. Transcriptional Analysis of Wheat Seedlings Inoculated with Fusarium Culmorum under Continual Exposure to Disease Defence Inductors. PLoS ONE. 2020;15:e0224413. doi: 10.1371/journal.pone.0224413. PubMed DOI PMC

Cao Y., Zhang Z., Ling N., Yuan Y., Zheng X., Shen B., Shen Q. Bacillus Subtilis SQR 9 Can Control Fusarium Wilt in Cucumber by Colonizing Plant Roots. Biol. Fertil. Soils. 2011;12:495–506. doi: 10.1007/s00374-011-0556-2. DOI

Lemańczyk G., Kwaśna H. Effects of Sharp Eyespot (Rhizoctonia cerealis) on Yield and Grain Quality of Winter Wheat. Eur. J. Plant Pathol. 2013;135:187–200. doi: 10.1007/s10658-012-0077-3. DOI

Rothen C., Miranda V., Fracchia S., Godeas A., Rodríguez A. Microdochium bolleyi (Ascomycota: Xylariales): Physiological Characterization and Structural Features of Its Association with Wheat. Bol. Soc. Argent. Bot. 2018;53:169–182. doi: 10.31055/1851.2372.v53.n2.20574. DOI

Perotto S., Rodda M., Benetti A., Sillo F., Ercole E., Rodda M., Girlanda M., Murat C., Balestrini R. Gene Expression in Mycorrhizal Orchid Protocorms Suggests a Friendly Plant–Fungus Relationship. Planta. 2014;239:1337–1349. doi: 10.1007/s00425-014-2062-x. PubMed DOI

Adholeya A., Tiwari P., Singh R. Large-Scale Inoculum Production of Arbuscular Mycorrhizal Fungi on Root Organs and Inoculation Strategies. In: Declerck S., Fortin J.A., Strullu D.-G., editors. In Vitro Culture of Mycorrhizas. Volume 4. Springer; Berlin/Heidelberg, Germany: 2005. pp. 315–338. Soil Biology.

Dehne H.-W., Backhaus G.F. The Use of Vesicular-Arbuscular Mycorrhizal Fungi in Plant Production. I. Inoculum Production/Zur Nutzung Vesikulär-Arbuskulärer Mykorrhizapilze in Der Pflanzenproduktion I. Inokulumgewinnung. Z. Pflanz. Pflanzenschutz J. Plant Dis. Prot. 1986;93:415–424.

Dsouza J. Advances in Biological Science Research. Elsevier; Amsterdam, The Netherlands: 2019. Techniques for the mass production of Arbuscular Mycorrhizal fungal species; pp. 445–451.

IJdo M., Cranenbrouck S., Declerck S. Methods for Large-Scale Production of AM Fungi: Past, Present, and Future. Mycorrhiza. 2011;21:1–16. doi: 10.1007/s00572-010-0337-z. PubMed DOI

Compant S., Duffy B., Nowak J., Clément C., Barka E.A. Use of Plant Growth-Promoting Bacteria for Biocontrol of Plant Diseases: Principles, Mechanisms of Action, and Future Prospects. AEM. 2005;71:4951–4959. doi: 10.1128/AEM.71.9.4951-4959.2005. PubMed DOI PMC

Ownley B., Weller D., Thomashow L. Influence of in Situ and in Vitro PH on Suppression of Gaeumannomyces graminis Var. Tritici by Pseudomonas fluorescens 2-79. Phytopathology. 1992;82:178–184. doi: 10.1094/Phyto-82-178. DOI

Nicholson P., Parry D.W. Development and Use of a PCR Assay to Detect Rhizoctonia Cerealis, the Cause of Sharp Eyespot in Wheat. Plant Pathol. 1996;45:872–883. doi: 10.1111/j.1365-3059.1996.tb02898.x. DOI

Zhu X., Qi L., Liu X., Cai S., Xu H., Huang R., Li J., Wei X., Zhang Z. The Wheat Ethylene Response Factor Transcription Factor PATHOGEN-INDUCED ERF1 Mediates Host Responses to Both the Necrotrophic Pathogen Rhizoctonia cerealis and Freezing Stresses. Plant Physiol. 2014;164:1499–1514. doi: 10.1104/pp.113.229575. PubMed DOI PMC

Neate S.M., Cruickshank R.H. Pectic Enzyme Patterns of Ceratobasidium and Rhizoctonia Spp. Associated with Sharp Eyespot-like Lesions on Cereals in South Australia. Trans. Br. Mycol. Soc. 1988;91:267–272. doi: 10.1016/S0007-1536(88)80214-6. DOI

Sticher L., Mauch-Mani B. Systemic acquired resistance. Annu. Rev. Phytopathol. 1997;35:235–270. doi: 10.1146/annurev.phyto.35.1.235. PubMed DOI

Adamo M., Chialva M., Calevo J., De Rose S., Girlanda M., Perotto S., Balestrini R. The Dark Side of Orchid Symbiosis: Can Tulasnella Calospora Decompose Host Tissues? IJMS. 2020;21:3139. doi: 10.3390/ijms21093139. PubMed DOI PMC

Blanco R., Aveling T.A.S. Acta Horticulturae. International Society for Horticultural Science (ISHS); Leuven, Belgium: 2018. Seed-Borne Fusarium Pathogens in Agricultural Crops; pp. 161–170.

Leišová L., Kučera L., Chrpová J., Sýkorová S., Šíp V., Ovesná J. Quantification of Fusarium Culmorum in Wheat and Barley Tissues Using Real-Time PCR in Comparison with DON Content. J. Phytopathol. 2006;154:603–611. doi: 10.1111/j.1439-0434.2006.01154.x. DOI

Bai G., Shaner G. Management and resistance in wheat and barley to fusarium head blight. Annu. Rev. Phytopathol. 2004;42:135–161. doi: 10.1146/annurev.phyto.42.040803.140340. PubMed DOI

Clement J.A., Parry D.W. Stem-Base Disease and Fungal Colonisation of Winter Wheat Grown in Compost Inoculated with Fusarium Culmorum, F. Graminearum and Microdochium Nivale. Eur. J. Plant Pathol. 1998;104:323–330. doi: 10.1023/A:1008681618351. DOI

Beccari G., Covarelli L., Nicholson P. Infection Processes and Soft Wheat Response to Root Rot and Crown Rot Caused by Fusarium Culmorum: Root Rot and Crown Rot Caused by F. culmorum on Soft Wheat. Plant Pathol. 2011;60:671–684. doi: 10.1111/j.1365-3059.2011.02425.x. DOI

Schroeder K.L., Paulitz T.C. Root Diseases of Wheat and Barley during the Transition from Conventional Tillage to Direct Seeding. Plant Dis. 2006;90:1247–1253. doi: 10.1094/PD-90-1247. PubMed DOI

Smiley R.W., Gourlie J.A., Easley S.A., Patterson L.-M. Pathogenicity of Fungi Associated with the Wheat Crown Rot Complex in Oregon and Washington. Plant Dis. 2005;89:949–957. doi: 10.1094/PD-89-0949. PubMed DOI

Liu Z., Ellwood S.R., Oliver R.P., Friesen T.L. Pyrenophora Teres: Profile of an Increasingly Damaging Barley Pathogen: Pathogen Profile of Pyrenophora Teres. Mol. Plant Pathol. 2011;12:1–19. doi: 10.1111/j.1364-3703.2010.00649.x. PubMed DOI PMC

Murray G.M., Brennan J.P. Estimating Disease Losses to the Australian Wheat Industry. Austral. Plant Pathol. 2009;38:558. doi: 10.1071/AP09053. DOI

Leišová-Svobodová L., Minaříková V., Matušinsky P., Hudcovicová M., Ondreičková K., Gubiš J. Genetic Structure of Pyrenophora Teres Net and Spot Populations as Revealed by Microsatellite Analysis. Fungal Biol. 2014;118:180–192. doi: 10.1016/j.funbio.2013.11.008. PubMed DOI

Matusinsky P., Frei P., Mikolasova R., Svacinova I., Tvaruzek L., Spitzer T. Species-Specific Detection of Bipolaris Sorokiniana from Wheat and Barley Tissues. Crop Prot. 2010;29:1325–1330. doi: 10.1016/j.cropro.2010.07.013. DOI

Anderson R.C., Liberta A.E., Dickman L.A. Interaction of Vascular Plants and Vesicular-Arbuscular Mycorrhizal Fungi across a Soil Moisture-Nutrient Gradient. Oecologia. 1984;64:111–117. doi: 10.1007/BF00377552. PubMed DOI

Evelin H., Kapoor R., Giri B. Arbuscular Mycorrhizal Fungi in Alleviation of Salt Stress: A Review. Ann. Bot. 2009;104:1263–1280. doi: 10.1093/aob/mcp251. PubMed DOI PMC

Malinowski D.P., Belesky D.P. Adaptations of Endophyte-Infected Cool-Season Grasses to Environmental Stresses: Mechanisms of Drought and Mineral Stress Tolerance. Crop Sci. 2000;40:923–940. doi: 10.2135/cropsci2000.404923x. DOI

White T.J., Bruns T., Lee S., Taylor J. 38—Amplification and direct sequencing of fungal ribosomal rna genes for phylogenetics. In: Innis M.A., Gelfand D.H., Sninsky J.J., White T.J., editors. PCR Protocols. Academic Press; San Diego, CA, USA: 1990. pp. 315–322.

Matusinsky P., Zouhar M., Pavela R., Novy P. Antifungal Effect of Five Essential Oils against Important Pathogenic Fungi of Cereals. Ind. Crops Prod. 2015;67:208–215. doi: 10.1016/j.indcrop.2015.01.022. DOI

Koske R.E., Gemma J.N. A Modified Procedure for Staining Roots to Detect VA Mycorrhizas. Mycol. Res. 1989;92:486–488. doi: 10.1016/S0953-7562(89)80195-9. DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...