The potential of using Metarhizium anisopliae and Metarhizium humberi to control the Asian soybean rust caused by Phakopsora pachyrhizi

References

• Agrofit. (2022). Sistema de Agrotóxicos Fitossanitários. Ministério da Agricultura, Pecuária e Abastecimento. https://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons
   Google Scholar
• Alves, L. (2022). Fungicides to control Asian rust generated BRL 9 billion in the 2020/2021 harvest. https://opresenterural.com.br/fungicidas-para-controle-da-ferrugem-asiatica-movimentaram-r-9-bilhoes-na-safra-2020-2021/
   Google Scholar
• Behie, S. W., Jones, S. J., & Bidochka, M. J. (2015). Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria. Fungal Ecology, 13, 112–119. https://doi.org/10.1016/j.funeco.2014.08.001
   Web of Science ®Google Scholar
• Bruck, D. J. (2010). Fungal entomopathogens in the rhizosphere. BioControl, 55(1), 103–112. https://doi.org/10.1007/s10526-009-9236-7
   Google Scholar
• Dalio, R. J. D., Máximo, H. J., Oliveira, T. S., Azevedo, T. M., Felizatti, H. L., Campos, M. A., & Machado, M. A. (2018). Molecular basis of Citrus sunki susceptibility and Poncirus trifoliata resistance upon Phytophthora parasitica attack. Molecular Plant-Microbe Interactions®, 31(3), 386–398. https://doi.org/10.1094/MPMI-05-17-0112-FI
   PubMed Web of Science ®Google Scholar
• De Paula, S., Holz, S., Souza, D. H. G., & Pascholati, S. F. (2021). Potential of resistance inducers for soybean rust management. Canadian Journal of Plant Pathology, 43(Suppl. 2), S298–S307. https://doi.org/10.1080/07060661.2021.1977999
   Google Scholar
• Dorighello, D. V., Bettiol, W., Maia, N. B., & de Campos Leite, R. M. V. B. (2015). Controlling Asian soybean rust (Phakopsora pachyrhizi) with Bacillus spp. and coffee oil. Crop Protection, 67, 59–65. https://doi.org/10.1016/j.cropro.2014.09.017
   Web of Science ®Google Scholar
• Faria, M. R., & Wraight, S. P. (2007). Mycoinsecticides and mycoacaricides: A comprehensive list with worldwide coverage and international classification of formulation types. Biological Control, 43(3), 237–256. https://doi.org/10.1016/j.biocontrol.2007.08.001
   Web of Science ®Google Scholar
• Fesel, P. H., & Zuccaro, A. (2016). β-glucan: Crucial component of the fungal cell wall and elusive MAMP in plants. Fungal Genetics and Biology, 90, 53–60. https://doi.org/10.1016/j.fgb.2015.12.004
   PubMed Web of Science ®Google Scholar
• Fontana, D. C., de Paula, S., Torres, A. G., de Souza, V. H. M., Pascholati, S. F., Schmidt, D., & Dourado Neto, D. (2021). Endophytic fungi: Biological control and induced resistance to phytopathogens and abiotic stresses. Pathogens, 10(5), 570. https://doi.org/10.3390/pathogens10050570
   PubMed Web of Science ®Google Scholar
• Freimoser, F. M., Hu, G., & Leger, R. J. S. (2005). Variation in gene expression patterns as the insect pathogen Metarhizium anisopliae adapts to different host cuticles or nutrient deprivation in vitro. Microbiology, 151(2), 361–371. https://doi.org/10.1099/mic.0.27560-0
   PubMedGoogle Scholar
• Gauthier, N. W., Maruthachalam, K., Subbarao, K. V., Brown, M., Xiao, Y., Robertson, C. L., & Schneider, R. W. (2014). Mycoparasitism of Phakopsora pachyrhizi, the soybean rust pathogen, by Simplicillium lanosoniveum. Biological Control, 76, 87–94. https://doi.org/10.1016/j.biocontrol.2014.05.008
   Web of Science ®Google Scholar
• Godoy, C. V., Koga, L. J., & Canteri, M. G. (2006). Diagrammatic scale for assessment of soybean rust severity. Fitopatologia Brasileira, 31(1), 63–68. https://doi.org/10.1590/S0100-41582006000100011
   Google Scholar
• Godoy, C. V., Seixas, C. D. S., Soares, R. M., Marcelino-Guimarães, F. C., Meyer, M. C., & Costamilan, L. M. (2016). Asian soybean rust in Brazil: Past, present, and future. Pesquisa Agropecuária Brasileira, 51(5), 407–421. https://doi.org/10.1590/S0100-204X2016000500002
   Web of Science ®Google Scholar
• Goellner, K., Loehrer, M., Langenbach, C., Conrath, U., Koch, E., & Schaffrath, U. (2010). Phakopsora pachyrhizi, the causal agent of Asian soybean rust. Molecular Plant Pathology, 11(2), 169–177. https://doi.org/10.1111/j.1364-3703.2009.00589.x
   PubMed Web of Science ®Google Scholar
• Gozzo, F., & Faoro, F. (2013). Systemic acquired resistance (50 years after discovery): Moving from the lab to the field. Journal of Agricultural and Food Chemistry, 61(51), 12473–12491. https://doi.org/10.1021/jf404156x
   PubMed Web of Science ®Google Scholar
• Hao, Q., Albaghdady, D. M. D., Xiao, Y., Xiao, X., Mo, C., Tian, T., & Wang, G. (2021). Endophytic Metarhizium anisopliae is a potential biocontrol agent against wheat Fusarium head blight caused by Fusarium graminearum. Journal of Plant Pathology, 103(3), 875–885. https://doi.org/10.1007/s42161-021-00866-6
   Google Scholar
• Hartley, S. E., Eschen, R., Horwood, J. M., Gange, A. C., & Hill, E. M. (2015). Infection by a foliar endophyte elicits novel arabidopside-based plant defence reactions in its host, C irsium arvense. New Phytologist, 205(2), 816–827. https://doi.org/10.1111/nph.13067
   PubMedGoogle Scholar
• Hartman, G. L., Hill, C. B., Twizeyimana, M., Miles, M. R., & Bandyopadhyay, R. (2011). Interaction of soybean and Phakopsora pachyrhizi, the cause of soybean rust. CABI Reviews, 2011, 1–13. https://doi.org/10.1079/PAVSNNR20116025
   Google Scholar
• Hu, D., Chen, Z., Zhang, C., & Ganiger, M. (2020). Reduction of Phakopsora pachyrhizi infection on soybean through host- and spray-induced gene silencing. Molecular Plant Pathology, 21(6), 794–807. https://doi.org/10.1111/mpp.12931
   PubMed Web of Science ®Google Scholar
• Jaber, L. R., & Enkerli, J. (2017). Fungal entomopathogens as endophytes: Can they promote plant growth? Biocontrol Science and Technology, 27(1), 28–41. https://doi.org/10.1080/09583157.2016.1243227
   Web of Science ®Google Scholar
• Jaber, L. R., & Ownley, B. H. (2018). Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biological Control, 116, 36–45. https://doi.org/10.1016/j.biocontrol.2017.01.018
   Web of Science ®Google Scholar
• Khan, A. L., Hamayun, M., Khan, S. A., Kang, S.-M., Shinwari, Z. K., Kamran, M., Rehman, S., Kim, J.-G., & Lee, I.-J. (2012). Pure culture of Metarhizium anisopliae LHL07 reprograms soybean to higher growth and mitigates salt stress. World Journal of Microbiology and Biotechnology, 28(4), 1483–1494. https://doi.org/10.1007/s11274-011-0950-9
   PubMed Web of Science ®Google Scholar
• Klosowski, A. C., May De Mio, L. L., Miessner, S., Rodrigues, R., Stammler, G. (2016). Detection of the F129L mutation in the cytochrome b gene in Phakopsora pachyrhizi. Pest Management Science, 72(6), 1211–1215. https://doi.org/10.1002/ps.4099
   PubMed Web of Science ®Google Scholar
• Koiri, R., Naik, R., Rawat, D., Chlonker, S., & Ahi, J. (2017). Bioecological perspective of entomopathogenic fungi with respect to biological control. Journal of Applied Microbiological Research, 1(1), 7–14.
   Google Scholar
• Lopez, A. (1991). Controle alternativo da antracnose causada por Colletrotrichum graminicola (Ces.) Wils. em sorgo (Sorgum bicolor L. (Moench.). [Dissertation]. UNESP.
   Google Scholar
• López, G., Muñoz Castellanos, C., Flores Ortiz, N. A., & González González, J. A. (2019). Control of powdery mildew (Leveillula taurica) using Trichoderma asperellum and Metarhizium anisopliae in different pepper types. BioControl, 64(1), 77–89. https://doi.org/10.1007/s10526-018-09916-y
   Google Scholar
• Luz, C., Rocha, L. F. N., Montalva, C., Souza, D. A., Botelho, A. B. R. Z., Lopes, R. B., Faria, M., & Delalibera Júnior, I. (2019). Metarhizium humberi sp. nov. Hypocreales: Clavicipitaceae), a new member of the PARB clade in the Metarhizium anisopliae complex from Latin America. Journal of Invertebrate Pathology, 166, 107216. https://doi.org/10.1016/j.jip.2019.107216
   PubMed Web of Science ®Google Scholar
• Maximo, H. J., Dalio, R. J. D., Dias, R. O., Litholdo, C. G., Felizatti, H. L., & Machado, M. A. (2019). PpCRN7 and PpCRN20 of Phythophthora parasitica regulate plant cell death leading to enhancement of host susceptibility. BMC Plant Biology, 19(1), 544. https://doi.org/10.1186/s12870-019-2129-8
   PubMedGoogle Scholar
• McCullagh, P., & Nelder, J. (1989). Generalized linear models. Chapman & Hall.
   Google Scholar
• Medeiros, F., Silva, J., & Pascholati, S. (2018). Controle biológico de doenças de plantas. In L. Amorim, J. Rezende, & A. Bergamin-Filho (Eds.), Manual de fitopatologia. Princípios e conceitos (pp. 261–272). Agr. Ceres.
   Google Scholar
• Oliveira, M. D. M., Varanda, C. M. R., & Félix, M. R. F. (2016). Induced resistance during the interaction pathogen x plant and the use of resistance inducers. Phytochemistry Letters, 15, 152–158. https://doi.org/10.1016/j.phytol.2015.12.011
   Web of Science ®Google Scholar
• Ownley, B. H., Gwinn, K. D., & Vega, F. E. (2010). Endophytic fungal entomopathogens with activity against plant pathogens: Ecology and evolution. BioControl, 55(1), 113–128. https://doi.org/10.1007/s10526-009-9241-x
   Web of Science ®Google Scholar
• Pal, S., St. Leger, R. J., & Wu, L. P. (2007). Fungal peptide destruxin A plays a specific role in suppressing the innate immune response in Drosophila melanogaster. Journal of Biological Chemistry, 282(12), 8969–8977. https://doi.org/10.1074/jbc.M605927200
   PubMed Web of Science ®Google Scholar
• Parsa, S., Ortiz, V., & Vega, F. E. (2013). Establishing fungal entomopathogens as endophytes: Towards endophytic biological control. Journal of Visualized Experiments, 74, 50360. https://doi.org/10.3791/50360
   Google Scholar
• Pascholati, S. F., & Dalio, R. J. D. (2018). Fisiologia do parasitismo: Como as plantas se defendem dos patógenos. In L. Amorim, J. A. M. Rezendo, & A. Bergamim Filho (Eds.), Manual de Fitopatologia: Princípios e Conceitos (5o ed., Vol. 1, pp. 424–450). Agronômica Ceres Ltda.
   Google Scholar
• Ravindran, K., Chitra, S., Wilson, A., & Sivaramakrishnan, S. (2014). Evaluation of antifungal activity of Metarhizium anisopliae against plant phytopathogenic fungi. In R. N. Kharwar, R. S. Upadhyay, N. K. Dubey, & R. Raghuwanshi (Eds.), Microbial diversity and biotechnology in food security (pp. 251–255). Springer India. https://doi.org/10.1007/978-81-322-1801-2_22
   Google Scholar
• R Core Team. (2018). R: A Language and environment for statistical computing. R Foundation for Statistical Computing.
   Google Scholar
• Rupe, J., & Sconyers, L. (2008). Soybean rust. Plant Health Instructor. https://doi.org/10.1094/PHI-I-2008-0401-01
   Google Scholar
• Sarven, S., Hao, Q., Deng, J., Yang, F., Wang, G., Xiao, Y., & Xiao, X. (2020). Biological control of tomato gray mold caused by botrytis cinerea with the entomopathogenic fungus Metarhizium anisopliae. Pathogens, 9(3), 213. https://doi.org/10.3390/pathogens9030213
   PubMed Web of Science ®Google Scholar
• Sasan, R. K., & Bidochka, M. J. (2012). The insect-pathogenic fungus Metarhizium robertsii (Clavicipitaceae) is also an endophyte that stimulates plant root development. American Journal of Botany, 99(1), 101–107. https://doi.org/10.3732/ajb.1100136
   PubMed Web of Science ®Google Scholar
• Sasan, R. K., & Bidochka, M. J. (2013). Antagonism of the endophytic insect pathogenic fungus Metarhizium robertsii against the bean plant pathogen Fusarium solani f. sp. phaseoli. Canadian Journal of Plant Pathology, 35(3), 288–293. https://doi.org/10.1080/07060661.2013.823114
   Web of Science ®Google Scholar
• Schmitz, H. K., Medeiros, C.-A., Craig, I. R., & Stammler, G. (2014). Sensitivity of Phakopsora pachyrhizi towards quinone-outside-inhibitors and demethylation-inhibitors, and corresponding resistance mechanisms: Sensitivity and resistance mechanisms of P. pachyrhizi towards fungicides. Pest Management Science, 70(3), 378–388. https://doi.org/10.1002/ps.3562
   PubMed Web of Science ®Google Scholar
• Schrank, A., & Vainstein, M. H. (2010). Metarhizium anisopliae enzymes and toxins. Toxicon, 56(7), 1267–1274. https://doi.org/10.1016/j.toxicon.2010.03.008
   PubMed Web of Science ®Google Scholar
• Simões, K., Hawlik, A., Rehfus, A., Gava, F., & Stammler, G. (2018). First detection of a SDH variant with reduced SDHI sensitivity in Phakopsora pachyrhizi. Journal of Plant Diseases and Protection, 125(1), 21–26. https://doi.org/10.1007/s41348-017-0117-5
   Web of Science ®Google Scholar
• Soto, N., Hernández, Y., Delgado, C., Rosabal, Y., Ortiz, R., Valencia, L., Borrás-Hidalgo, O., Pujol, M., & Enríquez, G. A. (2020). Field resistance to Phakopsora pachyrhizi and Colletotrichum truncatum of transgenic soybean expressing the NmDef02 plant defensin gene. Frontiers in Plant Science, 11, 562. https://doi.org/10.3389/fpls.2020.00562
   PubMedGoogle Scholar
• St. Leger, R. J. (2008). Studies on adaptations of Metarhizium anisopliae to life in the soil. Journal of Invertebrate Pathology, 98(3), 271–276. https://doi.org/10.1016/j.jip.2008.01.007
   PubMed Web of Science ®Google Scholar
• Twizeyimana, M., & Hartman, G. L. (2019). Effect of selected biopesticides in reducing soybean rust (Phakopsora pachyrhizi) development. Plant Disease, 103(9), 2460–2466. https://doi.org/10.1094/PDIS-02-19-0384-RE
   PubMed Web of Science ®Google Scholar
• Vega, F. E., Goettel, M. S., Blackwell, M., Chandler, D., Jackson, M. A., Keller, S., Koike, M., Maniania, N. K., Monzón, A., Ownley, B. H., Pell, J. K., Rangel, D. E. N., & Roy, H. E. (2009). Fungal entomopathogens: New insights on their ecology. Fungal Ecology, 2(4), 149–159. https://doi.org/10.1016/j.funeco.2009.05.001
   Web of Science ®Google Scholar
• Yamaoka, Y., Yamanaka, N., Akamatsu, H., & Suenaga, K. (2014). Pathogenic races of soybean rust Phakopsora pachyrhizi collected in Tsukuba and vicinity in Ibaraki, Japan. Journal of General Plant Pathology, 80(2), 184–188. https://doi.org/10.1007/s10327-014-0507-5
   Google Scholar