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Entoleuca sp. infected by mycoviruses as potential biocontrol agents of avocado white root rot

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Abstract

Rosellinia necatrix Prill. the causal agent of white root rot diseases causes major losses in avocado crops in Spain. To study the biocontrol of this disease, 31 antagonistic isolates were collected from the avocado rhizosphere and identified as Entoleuca sp. Studies were carried out in mycovirus detection, in vitro optimal growth temperature, mycelial compatibility groups of these isolates, and their inhibition of R. necatrix growth. The pathogenicity of these antagonistic isolates and their biocontrol of white root rot on avocado plants were also studied. The presence of mycoviruses was detected in all 31 Entoleuca sp. isolates studied and the optimal growth temperature for almost all the isolates (> 80%) was 25 °C. Dual culture showed different responses, with some isolates compatible and others incompatible with each other, showing inhibition halos and black lines. Twenty-five of the 31 isolates showed significant growth inhibition to a virulent R. necatrix isolate in in vitro conditions. In addition, none of the Entoleuca sp. isolates produced any symptoms on inoculated avocado plants and in 24 of them, symptoms of avocado white root rot were reduced, with significant differences among the Entoleuca sp. isolates when they were used as biocontrol agents. New virus-carrying Entoleuca sp. isolates were obtained, which are capable of controlling avocado white root rot.

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References

  • Arakawa, M., Nakamura, H., Uetake, Y., & Matsumoto, N. (2002). Presence and distribution of double-stranded RNA elements in the white root rot fungus Rosellinia necatrix. Mycoscience, 43(1), 21–26. https://doi.org/10.1007/s102670200004.

    Article  CAS  Google Scholar 

  • Arjona-Girona, I., & López-Herrera, C. J. (2018). Study of a new biocontrol fungal agent for avocado white root rot. Biological Control, 117, 6–12. https://doi.org/10.1016/j.biocontrol.2017.08.018.

    Article  Google Scholar 

  • Arjona-Lopez, J. M., Telengech, P., Jamal, A., Hisano, S., Kondo, H., Yelin, M. D., Arjona-Girona, I., Kanematsu, S., Lopez-Herrera, C. J., & Suzuki, N. (2018). Novel, diverse RNA viruses from Mediterranean isolates of the phytopathogenic fungus, Rosellinia necatrix: Insights into evolutionary biology of fungal viruses. Environmental Microbiology, 20(4), 1464–1483. https://doi.org/10.1111/1462-2920.14065.

    Article  CAS  PubMed  Google Scholar 

  • Arjona-López, J. M., Capote, N., & López-Herrera, C. J. (2019). Improved real-time PCR protocol for the accurate detection and quantification of Rosellinia necatrix in avocado orchards. Plant and Soil, 443, 605–612. https://doi.org/10.1007/s11104-019-04215-6.

    Article  CAS  Google Scholar 

  • Arjona-López, J. M., Telengech, P., Suzuki, N., & López-Herrera, C. J. (2020). A moderate level of hypovirulence conferred by a hypovirus in the avocado white root rot fungus, Rosellinia necatrix. Fungal Biology. https://doi.org/10.1016/j.funbio.2020.10.007.

  • Bhardwaj, L., Nag, N., & Sharma, S. (2000). Effect of green amendments and VAM fungi on the management of white root rot of apple. Plant Disease Research, 15(1), 53–59.

    Google Scholar 

  • CABI. (2019). https://www.cabi.org/isc/datasheet/47860#toDistributionMaps. Accessed 8 July 2019.

  • Campbell, C. L., & Madden, L. V. (1990). Temporal analysis of epidemics I: Descriptions and comparisons of disease progress curve. In C. L. Campbell & L. V. Madden (Eds.), Introduction to plant disease epidemiology (pp. 161–202). New York: Wiley.

    Google Scholar 

  • Çeliker, N., & Nemli, T. (1994). Investigation on biocontrol of white root rot [Rosellinia necatrix (Hartig)] Berlese. Türkiye III. Biyolojik Mücadele Kongresi, 25–28.

  • Chiba, S., Salaipeth, L., Lin, Y.-H., Sasaki, A., Kanematsu, S., & Suzuki, N. (2009). A novel bipartite double-stranded RNA mycovirus from the white root rot fungus Rosellinia necatrix: Molecular and biological characterization, taxonomic considerations, and potential for biological control. Journal of Virology, 83(24), 12801–12812. https://doi.org/10.1128/JVI.01830-09.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dafny-Yelin, M., Mairesse, O., Moy, J., Dor, S., & Malkinson, D. (2018). Genetic diversity and infection sources of Rosellinia necatrix in northern Israel. Phytopathologia Mediterranea, 57(1), 37–47. https://doi.org/10.14601/Phytopathol_Mediterr-22478.

    Article  Google Scholar 

  • de Mendiburu, F. (2013). Statistical procedures for agricultural research. Package “Agricolae”, version 1.4-4. Comprehensive R Archive Network. Vienna: Institute for Statistics and Mathematics.

  • de Waard, M., Georgopoulos, S., Hollomon, D., Ishii, H., Leroux, P., Ragsdale, N., & Schwinn, F. (1993). Chemical control of plant diseases: Problems and prospects. Annual Review of Phytopathology, 31(1), 403–421.

    Article  Google Scholar 

  • Eguchi, N., Kondo, K., & Yamagishi, N. (2009). Bait twig method for soil detection of Rosellinia necatrix, causal agent of white root rot of Japanese pear and apple, at an early stage of tree infection. Journal of General Plant Pathology, 75(5), 325–330. https://doi.org/10.1007/s10327-009-0179-8.

    Article  Google Scholar 

  • Elad, Y., Chet, I., & Katan, J. (1980). Trichoderma harzianum: A biocontrol agent effective against Sclerotium rolfsii and Rhizoctonia solani. Phytopathology, 70(2), 119–121.

    Article  Google Scholar 

  • El-Refai, I. M., Said, A., Assawah, W., & Draz, M. S. (2013). Vegetative compatibility and strain improvement of some Egyptian Trichoderma isolates. Life Science Journal, 10, 187–197.

    Google Scholar 

  • Eusebio-Cope, A., & Suzuki, N. (2015). Mycoreovirus genome rearrangements associated with RNA silencing deficiency. Nucleic Acids Research, 43(7), 3802–3813. https://doi.org/10.1093/nar/gkv239.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freeman, S., Sztejnberg, A., & Chet, I. (1986). Evaluation of Trichoderma as a biocontrol agent for Rosellinia necatrix. Plant and Soil, 94(2), 163–170. https://doi.org/10.1007/BF02374340.

    Article  Google Scholar 

  • Garcia-Jiménez, J., Busto, J., Vicent, A., & Armengol, J. (2004). Control of Dematophora necatrix on Cyperus esculentus tubers by hot-water treatment. Crop Protection, 23(7), 619–623. https://doi.org/10.1016/j.cropro.2003.11.012.

    Article  Google Scholar 

  • Gomez, I., Chet, I., & Herrera-Estrella, A. (1997). Genetic diversity and vegetative compatibility among Trichoderma harzianum isolates. Molecular and General Genetics MGG, 256(2), 127–135. https://doi.org/10.1007/s004380050554.

    Article  CAS  PubMed  Google Scholar 

  • Gómez-Lama Cabanás, C., & Pérez-Artés, E. (2014). New evidence of intra-race diversity in Fusarium oxysporum f. sp. dianthi populations based on vegetative compatibility groups. European Journal of Plant Pathology, 139(3), 445–451. https://doi.org/10.1007/s10658-014-0412-y.

    Article  Google Scholar 

  • Gullino, M. L., & Kuijpers, L. A. (1994). Social and political implications of managing plant diseases with restricted fungicides in Europe. Annual Review of Phytopathology, 32(1), 559–581.

    Article  CAS  Google Scholar 

  • Hajieghrari, B., Torabi-Giglou, M., Mohammadi, M. R., & Davari, M. (2008). Biological potantial of some Iranian Trichoderma isolates in the control of soil borne plant pathogenic fungi. African Journal of Biotechnology, 7(8), 967–972.

    Google Scholar 

  • Harman, G. E., & Kubicek, C. P. (1998). Trichoderma and gliocladium, volume 2: Enzymes, biological control and commercial applications. Boca Raton: CRC Press.

    Book  Google Scholar 

  • Heiniger, U., & Rigling, D. (1994). Biological control of chestnut blight in Europe. Annual Review of Phytopathology, 32(1), 581–599.

    Article  Google Scholar 

  • Hillman, B. I., Annisa, A., & Suzuki, N. (2018). Chapte Five - Viruses of Plant-Interacting Fungi. In M. Kielian, T. C. Mettenleiter, & M. J. Roossinck (Eds.) Advances in Virus Research,100, 99–116. Academic Press. https://doi.org/10.1016/bs.aivir.2017.10.003.

  • Howell, C., & Stipanovic, R. (1995). Mechanisms in the biocontrol of Rhizoctonia solani-induced cotton seedling disease by Gliocladium virens: Antibiosis. Phytopathology, 85, 469.

    Article  Google Scholar 

  • Ikeda, K., Nakamura, H., Arakawa, M., & Matsumoto, N. (2004). Diversity and vertical transmission of double-stranded RNA elements in root rot pathogens of trees, Helicobasidium mompa and Rosellinia necatrix. Mycological Research, 108(6), 626–634. https://doi.org/10.1017/S0953756204000061.

    Article  CAS  PubMed  Google Scholar 

  • Ikeda, K., Inoue, K., Nakamura, H., Hamanaka, T., Ohta, T., Kitazawa, H., Kida, C., Kanematsu, S., & Park, P. (2011). Genetic analysis of barrage line formation during mycelial incompatibility in Rosellinia necatrix. Fungal Biology, 115(1), 80–86. https://doi.org/10.1016/j.funbio.2010.10.008.

    Article  PubMed  Google Scholar 

  • Jiang, Y., Zhang, T., Luo, C., Jiang, D., Li, G., Li, Q., Hsiang, T., & Huang, J. (2015). Prevalence and diversity of mycoviruses infecting the plant pathogen Ustilaginoidea virens. Virus Research, 195, 47–56. https://doi.org/10.1016/j.virusres.2014.08.022.

    Article  CAS  PubMed  Google Scholar 

  • Kanematsu, S., Arakawa, M., Oikawa, Y., Onoue, M., Osaki, H., Nakamura, H., Ikeda, K., Kuga-Uetake, Y., Nitta, H., Sasaki, A., Suzaki, K., Yoshida, K., & Matsumoto, N. (2004). A reovirus causes hypovirulence of Rosellinia necatrix. Phytopathology, 94(6), 561–568. https://doi.org/10.1094/PHYTO.2004.94.6.561.

    Article  CAS  PubMed  Google Scholar 

  • Katan, T., Zamir, D., Sarfatti, M., & Katan, J. (1991). Vegetative compatibility groups and subgroups in Fusarium oxysporum f. sp. radicis-lycopersici. Phytopathology, 81(3), 255–262.

    Article  CAS  Google Scholar 

  • Khan, A. (1959). Biology and pathogenicity of Rosellinia necatrix (Hart.) Berl. Biologia, 5, 199–245.

    Google Scholar 

  • Korolev, N., Katan, J., & Katan, T. (2000). Vegetative compatibility groups of Verticillium dahliae in Israel: Their distribution and association with pathogenicity. Phytopathology, 90(5), 529–536. https://doi.org/10.1094/PHYTO.2000.90.5.529.

    Article  CAS  PubMed  Google Scholar 

  • López-Herrera, C. (1989). Podredumbres radiculares del aguacate en la Costa del Sol. Años 1987-88. In J. Moral (Ed.), Estudios Fitopatología (pp. 172–176). Badajoz: SEFDGIEA.

    Google Scholar 

  • López-Herrera, C. J., & Zea-Bonilla, T. (2007). Effects of benomyl, carbendazim, fluazinam and thiophanate methyl on white root rot of avocado. Crop Protection, 26(8), 1186–1192. https://doi.org/10.1016/j.cropro.2006.10.015.

    Article  CAS  Google Scholar 

  • López-Herrera, C. J., Pérez-Jiménez, R. M., Zea-Bonilla, T., Basallote-Ureba, M. J., & Melero-Vara, J. M. (1998). Soil solarization in established avocado trees for control of Dematophora necatrix. Plant Disease, 82(10), 1088–1092. https://doi.org/10.1094/PDIS.1998.82.10.1088.

    Article  PubMed  Google Scholar 

  • López-Herrera, C., Pérez-Jiménez, R., Llobel, A., Monte-Vázquez, E., & Zea-Bonilla, T. (1999). Estudios in vivo de Trichoderma como agente de biocontrol contra Phytophthora cinnamomi y Rosellinia necatrix en aguacate. Revista Chapingo Serie Horticultura, 5, 261–265.

    Google Scholar 

  • MAPA. (2019). http://www.mapa.gob.es/es/. Accessed 20 Sep 2019.

  • McElreath, S. D., Yao, J. M., Coker, P. S., & Tainter, F. H. (1994). Double-stranded RNA in isolates of Discula destructiva from the eastern United States. Current Microbiology, 29(1), 57–60. https://doi.org/10.1007/BF01570193.

    Article  CAS  Google Scholar 

  • Mendoza García, R. A., Martijn ten Hoopen, G., Kass, D. C. J., Sánchez Garita, V. A., & Krauss, U. (2003). Evaluation of mycoparasites as biocontrol agents of Rosellinia root rot in cocoa. Biological Control, 27(2), 210–227. https://doi.org/10.1016/S1049-9644(03)00014-8.

    Article  Google Scholar 

  • Nakamura, H., Uetake, Y., Arakawa, M., Okabe, I., & Matsumoto, N. (2000). Observations on the teleornorph of the white root rot fungus, Rosellinia necatrix, and a related fungus, Rosellinia aquila. Mycoscience, 41(5), 503–507. https://doi.org/10.1007/BF02461671.

    Article  Google Scholar 

  • Naseby, D., Pascual, J., & Lynch, J. (2000). Effect of biocontrol strains of Trichoderma on plant growth, Pythium ultimum populations, soil microbial communities and soil enzyme activities. Journal of Applied Microbiology, 88(1), 161–169. https://doi.org/10.1046/j.1365-2672.2000.00939.x.

    Article  CAS  PubMed  Google Scholar 

  • Nuss, D. L. (1992). Biological control of chestnut blight: An example of virus-mediated attenuation of fungal pathogenesis. Microbiology and Molecular Biology Reviews, 56(4), 561–576.

    CAS  Google Scholar 

  • Osaki, H., Nomura, K., Matsumoto, N., & Ohtsu, Y. (2004). Characterization of double-stranded RNA elements in the violet root rot fungus Helicobasidium mompa. Mycological Research, 108(6), 635–640. https://doi.org/10.1017/S095375620400005X.

    Article  CAS  PubMed  Google Scholar 

  • Perez Jimenez, R. M., Jimenez Diaz, R. M., & Lopez Herrera, C. J. (2002). Somatic incompatibility of Rosellinia necatrix on avocado plants in southern Spain. Mycological Research, 106(2), 239–244. https://doi.org/10.1017/S0953756201005500.

    Article  Google Scholar 

  • R Development Core Team. (2017). R: A language and environment for statistical computing. Vienna: R foundation for statistical computing. ISBN 3-900051-07-0. http://www.r-project.org/.

    Google Scholar 

  • Reisenzein, H., & Tiefenbrunner, W. (1997). Wachstumshemmende Wirkung verschiedener Isolate des entomopathogenen Pilzes Beauveria bassiana (Bals.) Vuill. auf Schadpilze der Gattungen Fusarium, Armillaria und Rosellinia. Pflanzenschutzbericht, 57(1), 15–24.

    Google Scholar 

  • Rojo, F. G., Reynoso, M. M., Ferez, M., Chulze, S. N., & Torres, A. M. (2007). Biological control by Trichoderma species of Fusarium solani causing peanut brown root rot under field conditions. Crop Protection, 26(4), 549–555. https://doi.org/10.1016/j.cropro.2006.05.006.

    Article  Google Scholar 

  • Ruano-Rosa, D. (2006). Control biológico, caracterización y detección molecular de Rosellinia necatrix Prill., agente causal de la podredumbre blanca del aguacate. PhD Thesis, Universidad de Córdoba, Córdoba, Spain, 361 pp.

  • Ruano-Rosa, D., & López-Herrera, C. J. (2009). Evaluation of Trichoderma spp. as biocontrol agents against avocado white root rot. Biological Control, 51(1), 66–71. https://doi.org/10.1016/j.biocontrol.2009.05.005.

    Article  Google Scholar 

  • Ruano-Rosa, D., Del Moral-Navarrete, L., & Lopez-Herrera, C. J. (2010). Selection of Trichoderma spp. isolates antagonistic to Rosellinia necatrix. Spanish Journal of Agricultural Research, 8(4), 1084–1097. https://doi.org/10.5424/sjar/2010084-1403.

    Article  Google Scholar 

  • Schena, L., Nigro, F., & Ippolito, A. (2002). Identification and detection of Rosellinia necatrix by conventional and real-time scorpion-PCR. European Journal of Plant Pathology, 108(4), 355–366. https://doi.org/10.1023/A:1015697813352.

    Article  CAS  Google Scholar 

  • Segarra, G., Casanova, E., Avilés, M., & Trillas, I. (2010). Trichoderma asperellum strain T34 controls Fusarium wilt disease in tomato plants in soilless culture through competition for iron. Microbial Ecology, 59(1), 141–149. https://doi.org/10.1007/s00248-009-9545-5.

    Article  PubMed  Google Scholar 

  • Shi, L.-L., Mortimer, P. E., Ferry Slik, J. W., Zou, X.-M., Xu, J., Feng, W.-T., & Qiao, L. (2014). Variation in forest soil fungal diversity along a latitudinal gradient. Fungal Diversity, 64(1), 305–315. https://doi.org/10.1007/s13225-013-0270-5.

    Article  Google Scholar 

  • Sivan, A., Elad, Y., & Chet, I. (1984). Biological control effects of a new isolate of Trichoderma harzianum on Pythium aphanidermatum. Phytopathology, 74(4), 498–501.

    Article  Google Scholar 

  • Steel, R. G. D., & Torrie, J. H. (1960). Principles and procedures of statistics: With special reference to the biological sciences. New York: Academic.

    Google Scholar 

  • Sztejnberg, A., & Madar, Z. (1980). Host range of Dematophora necatrix, the cause of white root rot disease in fruit trees. Plant Disease, 64(7), 662–664. https://doi.org/10.1094/PD-64-662.

    Article  Google Scholar 

  • Sztejnberg, A., Freeman, S., Chet, I., & Katan, J. (1987). Control of Rosellinia necatrix in soil and in apple orchard by solarization and Trichoderma harzianum. Plant Disease, 71(4), 365–369. https://doi.org/10.1094/PD-71-0365.

    Article  Google Scholar 

  • ten Hoopen, G. M., & Krauss, U. (2006). Biology and control of Rosellinia bunodes, Rosellinia necatrix and Rosellinia pepo: A review. Crop Protection, 25(2), 89–107. https://doi.org/10.1016/j.cropro.2005.03.009.

    Article  Google Scholar 

  • van den Berg, N., Hartley, J., Engelbrecht, J., Mufamadi, Z., van Rooyen, Z., & Mavuso, Z. (2018). First report of white root rot caused by Rosellinia necatrix on Persea americana in South Africa. Plant Disease, 102(9), 1850. https://doi.org/10.1094/PDIS-10-17-1637-PDN.

    Article  Google Scholar 

  • Velasco, L., Arjona-Girona, I., Ariza-Fernández, M. T., Cretazzo, E., & López-Herrera, C. (2018). A novel hypovirus species from xylariaceae fungi infecting avocado. Frontiers in Microbiology, 9, 1–14. https://doi.org/10.3389/fmicb.2018.00778.

    Article  Google Scholar 

  • Velasco, L., Arjona-Girona, I., Cretazzo, E., & López-Herrera, C. (2019). Viromes in Xylariaceae fungi infecting avocado in Spain. Virology, 532, 11–21. https://doi.org/10.1016/j.virol.2019.03.021.

    Article  CAS  PubMed  Google Scholar 

  • Watanabe, T. (1991). Evaluation of Sordaria spp. as biocontrol agents against soilborne plant diseases caused by Pythium aphanidermatum and Dematophora necatrix. Japanese Journal of Phytopathology, 57(5), 680–687. https://doi.org/10.3186/jjphytopath.57.680.

    Article  Google Scholar 

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Acknowledgements

The authors are grateful to TROPS for their technical support, especially in the location of isolates in commercial avocado orchards and to Prof. José M. Melero-Vara for his assistance in the review.

Funding

This study was partly supported by the Plan Nacional I+D+I Ministerio de Economía y Competitividad (AGL 2014-52518-C2-2-R) Spain. In addition, this research was co-financed by FEDER funds (EU).

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  1. Institute for Sustainable Agriculture, Spanish Research Council, Alameda del Obispo s/n, 14004, Córdoba, Spain

    Juan M. Arjona-López & Carlos J. López-Herrera

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  1. Juan M. Arjona-López
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Correspondence to Carlos J. López-Herrera.

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Arjona-López, J.M., López-Herrera, C.J. Entoleuca sp. infected by mycoviruses as potential biocontrol agents of avocado white root rot. Eur J Plant Pathol 159, 409–420 (2021). https://doi.org/10.1007/s10658-020-02171-x

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