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Bacillus sp. FSQ1: a Promising Biological Control Agent Against Sclerotinia sclerotiorum, the Causal Agent of white Mold in Common Bean (Phaseolus vulgaris L.)

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Abstract

Phytopathogenic fungi cause several diseases in the common bean (Phaseolus vulgaris), diminishing its productivity, i.e. white mold. This work aimed to isolate and characterize the causal agent of the white mold disease observed in a common bean commercial field, in Northern Mexico; as well as to identify a promising native biological control agent against this phytopathogen. Based on macro/microscopic traits (white-cottony mycelium, and sclerotia formation) and molecular identification [sequencing of the internal transcribed spacer 1 (ITS1) gene], a fungal isolate (FRM18) obtained from symptomatic common bean plants, was identified as Sclerotinia sclerotiorum. In addition, a bacterial strain (FSQ1) isolated from the common bean rhizosphere showed in vitro antagonism against S. sclerotiorum FRM18, inhibiting 2.4 ± 0.2 cm of the studied phytopathogen growth. Based on macro/microscopic traits (gram-positive bacteria, bacillary morphology, and endospore production) and molecular identification (sequencing of the 16S rRNA gene), strain FSQ1 was affiliated to the genus Bacillus. Common bean plants inoculated with S. sclerotiorum FRM18 showed a height reduction of 25% at day: 60 and white mold disease was observed (compared to un-inoculated plants), validating the Koch’s postulates, which confirm that strain FRM18 is the causal agent of this disease in the field. However, common bean plants co-inoculated with S. sclerotiorum FRM18 and Bacillus sp. FSQ1 (compared to un-inoculated plants) were not affected in their development, and symptoms of the disease were not observed. Even when lipopeptides are the potential action mode of Bacillus sp. FSQ1 to inhibit S. sclerotiorum FRM18, further researches are necessary to determine the main antimicrobial compounds produced by strain FSQ1.

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REFERENCES

  1. Aguado-Santacruz, G.A., Moreno-Gómez, B., Jiménez-Francisco, B., García-Moya, E., and Preciado-Ortiz, R.E., Impact of themicrobial siderophores and phytosiderophoresontheironassimilationbyplants: a synthesis, Revfitotecmex., 2012, vol. 35, pp. 9–21. http://www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S018773802012000100004.

    Article  Google Scholar 

  2. Aleti, G., Lehner, S., Bacher, M., Compant, S., Nikolic, B., Plesko, M., Schuhmacher, R., Sessitsh, A., and Brader, G., Surfactin variants mediate species-specific biofilm formation and root colonization in Bacillus, Environ. Microbiol., 2016, vol 18, pp. 2634-2645. https://doi.org/10.1111/1462-2920.13405

    Article  CAS  PubMed  Google Scholar 

  3. Allard-Massicotte, R., Tessier, L., Lécuyer, F., Lakshmanan, V., Lucier, J., Garneau, D., Caudwell, L., Vlamakis, H., Bais, H.P., and Beauregard, P.B., Bacillus subtilis early colonization of Arabidopsis thaliana roots involves multiple chemotaxis receptors, mBio, 2016, vol. 7, e01664-16.https://doi.org/10.1128/mBio.01664-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Allori, S.E., Yasem, R.M.G., and Ploper, L.D., In vitro evaluation of temperature influence on native Sclerotinia sclerotiorum carpogenic germination of Northwest Argentina [Evaluación in vitro de la influencia de la temperaturaen la germinación carpogénica de Sclerotinia sclerotiorum nativo del Noroeste Argentino], Rev Agronnoroeste Arg, vol. 36, pp. 51–56. http://www.scielo.org.ar/scielo.php?script=sci_arttext&pid= S2314369X2016000100007&lng=es&tlng=es.

  5. Ansary, W.R., Khan, F.R., Haque, E., Sultana, F., West, H.M., Rahman, M., Mondol, A.M., Akanda, A.M., Rahman, M., Clarke, M., and Islam, T., Endophytic Bacillus spp. from medicinal plants inhibit mycelial growth of Sclerotinia sclerotiorum and promote plant growth. Z Naturforsch C, 2018, vol. 73, pp. 247–256. https://doi.org/10.1515/znc-2018-0002

    Article  CAS  PubMed  Google Scholar 

  6. Apodaca-Sánchez, M.A., Maininfectiousdiseases of commonbean in Sinaloa and theirmanagement [Principales enfermedades infecciosas del frijol en Sinaloa y su manejo], Jornada de transferencia de tecnología del cultivo de frijol, 2010, pp. 7–26. https://www.fps.org.mx/portal/index.php/component/phocadownload/category/30-granos-y-flores%3Fdownload%3D105:jornada-de-transferencia-de-tecnologia-del-cultivo-del-frijol-2+&cd=1&hl= es&ct=clnk&gl=mx&lr=lang_en%7Clang_es#. Accessed July 29, 2018.

  7. Aranda, F.J., Teruel, J.A., and Ortiz, A., Further aspects on the hemolytic activity of the antibiotic lipopeptide iturin A, Biochim Biophys Acta, 2005, vol. 1713, pp. 51–57. https://doi.org/10.1016/j.bbamem.2005.05.003

    Article  CAS  PubMed  Google Scholar 

  8. Ayala, Q.A., Cortez, E., Apodaca, M.A., Leal, V.M., Valenzuela, F.A., and Palacios, C.A., Bio-rational and conventionalfungicideseffectivenesson in vitro Sclerotinia sclerotiorum, REMEXCA, 2015, vol. 11, pp. 2149–2156. https://doi.org/10.29312/remexca.v0i11.784

    Article  Google Scholar 

  9. Banerjee, G., Nandi, A., and Kumar, A., Assessment of hemolytic activity, enzyme production and bacteriocin characterization of Bacillus subtilis LR1 isolated from the gastrointestinal tract of fish, Arch. Microbiol., 2016, vol. 199, pp. 115–124. https://doi.org/10.1007/s00203-016-1283-8

    Article  CAS  PubMed  Google Scholar 

  10. Billon, G., Pussereau, N., and Fevre, M., The extracellular proteases secreted in vitro and “in planta” by phytopathogenic fungus Sclerotinia sclerotiorum, J. Phytopathol., 2002, vol. 150, pp. 507–511. https://doi.org/10.1046/j.1439-0434.2002.00782.x

    Article  Google Scholar 

  11. Botelho, L.S., Zacan, W.L., Machado, J.C., and Barrocas, E.N., Performance of common bean seeds infected by the fungus Sclerotinia sclerotiorum, J. Seed Sci., 2013, vol. 35, pp. 153–160. https://doi.org/10.1590/S2317-15372013000200003

    Article  Google Scholar 

  12. Calvo, P. and Zúñiga, D., Physiological characterization of Bacillus spp. strains from potato (Solanum tuberosum) rhizosphere, Ecolapl, 2010, vol. 9, pp. 31–39. https://doi.org/10.21704/rea.v9i1-2.393

    Article  Google Scholar 

  13. Chowdhury, S.P., Hartmann, A., Gao, X., and Borriss, R., Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42 – a review, Front Microbiol., 2015, vol. 6, pp. 1–11. https://doi.org/10.3389/fmicb.2015.00780

    Article  Google Scholar 

  14. de los Santos, S., Robles, R.I., Parra, F.I., Larsen, J., Lozano, P., and Tiedje, J.M., Bacillus cabrialesii sp. nov., an endophytic plant growth promoting bacterium isolated from wheat (Triticum turgidum subsp. durum) in the Yaqui Valley, Mexico, Int. J. Syst. Evol. Microbiol., 2019, vol. 69, pp. 3939–3945. https://doi.org/10.1099/ijsem.0.003711

    Article  CAS  Google Scholar 

  15. de los Santos-Villalobos, S., Barrera-Galicia, G., Miranda-Salcedo, M., and Peña-Cabriales, J., Burkholderiacepacia XXVI siderophore with biocontrol capacity against Colletotrichum gloeosporioides, World J. Microbiol. Biotechnol., 2012, vol. 28, pp. 2615–2623. https://doi.org/10.1007/s11274-012-1071-9

    Article  PubMed  Google Scholar 

  16. de los Santos-Villalobos, S., Kremer, J.M., Parra-Cota, F.I., Hayano-Kanashiro, A.C., García-Ortega, L.F., Gunturu, S.K., He, S.Y., and Peña-Cabriales, J.J., Draft genome of the fungicidal biological control agent Burkholderia anthina strain XXVI, Arch. Microbiol., 2018a, vol. 200, pp. 803–810. https://doi.org/10.1007/s00203-018-1490-6

    Article  CAS  PubMed  Google Scholar 

  17. de los Santos-Villalobos, S., Parra, F.I., Herrera, A., Valenzuela, B., and Estrada, J.C., Collection of edaphicmicroorganisms and nativeendophytes to contribute to nationalfoodsecurity, REMEXCA, 2018b, vol. 9, pp. 191–202. https://doi.org/10.29312/remexca.v9i1.858

    Article  Google Scholar 

  18. Díaz, A.M., Parra, F.I., Santoyo, G., and de los Santos, S., Chlorothalonil tolerance of indole producing bacteria associated to wheat (Triticum turgidum L.) rhizosphere in the Yaqui Valley, Mexico, Ecotoxicology, 2019, vol. 28, pp. 569–577. https://doi.org/10.1007/s10646-019-02053-x

    Article  CAS  Google Scholar 

  19. Elsheshtawi, M., Elkhaky, M.T., Sayed, S.R., Bahkali, A.H., Mohammed, A.A., Gambhir, D., Mansour, A.S., and Elgorban, A.M., Integrated control of white rot disease on beans caused by Sclerotinia sclerotiorum using Contans® and reduced fungicides application, Saudi J. Biol. Sci., 2017, vol. 24, pp. 405–409. https://doi.org/10.1016/j.sjbs.2016.01.038

    Article  CAS  PubMed  Google Scholar 

  20. Falardeau, J., Wise, C., Novitsky, L., and Avis, T.J., Ecological and mechanistic insights into the direct and indirect antimicrobial properties of Bacillus subtilis lipopeptides on plant pathogens, J. Chem. Ecol., 2013, vol. 39, art. 869878. https://doi.org/10.1007/s10886-013-0319-7

    Article  CAS  Google Scholar 

  21. Foley, M.E., Doğramacı, M., West, M., and Underwood, W.R., Environmental factors for germination of Sclerotinia sclerotiorum sclerotia, J. Plant Pathol. Microbiol., 2016, vol. 7, p. 379. https://doi.org/10.4172/2157-7471.1000379

    Article  Google Scholar 

  22. From, C., Hormazabal, V., Hardy, S.P., and Granum, P.E., Cytotoxicity in Bacillus mojavensis is abolished following loss of surfactin synthesis: Implications for assessment of toxicity and food poisoning potential, Int. J. Food Microbiol., 2007, vol. 117, pp. 43–49. https://doi.org/10.1016/j.ijfoodmicro.2007.01.013

    Article  CAS  PubMed  Google Scholar 

  23. Gálvez, G.T., Sánchez, M.R., Parra, F., García, J., Aviña, G.N., and de los Santos, S., Pesticides in Mexican Agriculture and promissory alternatives for their replacement, Biol. Agrop. Tuxpan, 2018, vol. 7, pp. 1977–1991. ISSN: 2007-6940.

  24. Gomashe, A.V., Gulhane, P.A., and Bezakwar, P.M., Isolation and screening of cellulose degrading. Microbes from Nagpur region soil, Int. J. Life Sci., 2013, pp. 291–293. http://files.cluster2.hostgator.co.in/hostgator84521/file/9.ijlsci_0172.pdf. Accessed July 29, 2018.

  25. Gong, M., Wang, J.D., Zhang, J., Yang, H., Lu, X.F., Pei, Y., and Cheng, J.Q., Study of the antifungal ability of Bacillus subtilis strain PY-1 in vitro and identification of its antifungal substance (Iturin A), Acta Biochim Biophys Sin., 2006, vol. 38, pp. 233–240. https://doi.org/10.1111/j.17457270.2006.00157.x

    Article  CAS  PubMed  Google Scholar 

  26. Grahovac, J.A., Roncevic, Z.Z., Tadijan, I.Z., Jokic, A.I., and Dodic, J.M., Optimization of media for antimicrobial compounds production by Bacillus subtilis, Acta Aliment., 2015 vol. 44, pp. 427–435. https://doi.org/10.1556/066.2015.44.0014

    Article  CAS  Google Scholar 

  27. Huang, H.C., Huang, J.W., Saidon, G., and Erickson, R.S., Effect of allyl alcohol and fermented agricultural wastes on carpogenic germination of sclerotia of Sclerotinia sclerotiorum and colonization by Trichoderma spp., Can. J. Plant Pathol., 1997, vol. 19, pp. 43–44. https://doi.org/10.1080/07060669709500570

    Article  CAS  Google Scholar 

  28. Instituto Nacional de Ecología y Cambio Climático (INECC), Fluazinam, 2016, http://www2.inecc.gob.mx/sistemas/plaguicidas/pdf/fluazinam.pdf. Accessed July 29, 2018.

  29. Jadhav, H.P., Shaikh, S.S., and Sayved, R.Z., Role of hydrolytic enzymes of rhizoflora in biocontrol of fungal phytopathogens: an overview, in Rhizotrophs: Plant Growth Promotion to Bioremediation. Microorganisms for Sustainability, Mehnaz, S., Ed., Springer, 2017, vol. 2. https://doi.org/10.1007/978-981-10-4862-3_9

  30. Kumar, A., Prakash, A., and Johri, B.N., Bacillus as PGPR in crop ecosystem, in Bacteria in Agrobiology: Crop Ecosystems, Maheshwari, D., Ed., Berlin: Springer, 2011, pp. 37–59. https://doi.org/10.1007/978-3-642-18357-7_2

  31. Layton, C., Maldonado, E., Monroy, L., Constanza, L., and Sánchez, L.C., Bacillus spp.; perspective biocontrol through antibiosis effect on crops affected by phytopathogenics, NOVA, 2011, vol. 9. https://doi.org/10.22490/24629448.501

  32. Lehner, M.S., Paula, T.J., Silva, R.A., Vieira, R.F., Carneiro, J.E.S., Schnabel, and G., Mizubuti, E.S.G., Fungicide sensitivity of Sclerotinia sclerotiorum: a thorough assessment using discriminatory dose, EC50, high-resolution melting analysis, and description of new point mutation associated with thiophanate-methyl resistance, Plant Dis., 2015, vol. 99, pp. 1537–1543. https://doi.org/10.1094/PDIS-11-14-1231-RE

    Article  CAS  PubMed  Google Scholar 

  33. Mazu, T.K., Flores-Rozas, H., and Ablordeppey, S.Y., The mechanistic target of antifungal agents: an overview, Mini Rev. Med. Chem., 2016, vol. 16, pp. 555–578. PMCID: PMC5215921.

    Article  CAS  Google Scholar 

  34. Mikkola, R., Kolari, M., Andersson, M.A., Helin, J., and Salkinoja-Salonen, M.S., Toxic lactonic lipopeptide from food poisoning isolates of Bacillus licheniformis, Eur. J. Biochem., 2000, vol. 267, pp. 4068–4074. https://doi.org/10.1046/j.1432-1033.2000.01467.x

    Article  CAS  PubMed  Google Scholar 

  35. Mora-Romero, G.A., López-Meyer, M., Ramírez-Douriet, C.M., Martínez-Valenzuela, M.C., Romero-Urías, C.A., Herrera-Rodríguez, G., and Félix-Gastelum, R., Evaluation of the susceptibility to Sclerotinia sclerotiorum in four micorryzed bean (Phaseolus vulgaris l.) genotypes, Interciencia, 2016, vol. 41, pp. 127–132. http://www.redalyc.org/articulo.oa?id=33944255009. Accessed July 29, 2018.

    Google Scholar 

  36. Nihorimbere, V. and Ongena, M., Isolation of plant growth-promoting Bacillus strains with biocontrol activity in vitro, MRJMBS, 2017, vol. 5, no. 2, pp. 13–21. ISSN: 2408-7076. http://www.meritresearchjournals.org/mbs/ content/2017/March/Nihorimbere%20and%20Ongena.pdf. Accessed July 29, 2018.

  37. Ongena, M. and Jacques, P., Bacillus lipopeptides: versatile weapons for plant disease biocontrol, Trends Microbiol., 2008, vol. 16, pp. 115–125. https://doi.org/10.1016/j.tim.2007.12.009

    Article  CAS  PubMed  Google Scholar 

  38. Pandin, C., Darsonval, M.D., Mayeur, C., Le Coq, D., Aymerich, S., Biandet, R. Biofilm formation and synthesis of antimicrobial compounds by the biocontrol agent Bacillus velezensis QST713 in an Agaricus bisporus compost micromodel, Appl. Environ. Microbiol., 2019, vol. 85. https://doi.org/10.1128/AEM.00327-19

  39. Parra-Cota, F.I., García-Pereyra, J., Aviña-Martínez, G.N., de los Santos-Villalobos, S., First report of Fusarium wilt on Citrus sinensis var. Valencia in the Yaqui Valley, Mexico, Rev. Mex. Fitopatol., 2019, vol. 37, pp. 193–201. https://doi.org/10.18781/r.mex.fit.1810-3

    Article  Google Scholar 

  40. Parte, A.C., List of prokaryotic names with standing in nomenclature (bacterio.net), 20 years on, Int. J. Syst. Evol. Microbiol., 2018, vol. 68, pp. 1825–1829. https://doi.org/10.1099/ijsem.0.002786

    Article  PubMed  Google Scholar 

  41. Perneel, M., Heyrman, J., Adiobo, A., De Maeyer, K., Raaijmakers, J.M., de Vos, P., and Hofte, M., Characterization of CMR5c and CMR12a, novel fluorescent Pseudomonas strains from the cocoyam rhizosphere with biocontrol activity, J. Appl. Microbiol., 2007, vol. 103, pp. 1007–1020. https://doi.org/10.1111/j.1365-2672.2007.03345.x

    Article  CAS  PubMed  Google Scholar 

  42. Pontón, J., The fungal cell wall and the mechanism of action of anidulafungin, Rev. Iberoam Micol., 2008, vol. 25, pp. 78–82. https://doi.org/10.1016/S1130-1406(08)70024-X

    Article  PubMed  Google Scholar 

  43. Raaijmakers, J.M., de Bruijn, I., Nybroe, O., and Ongena, M., Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics, FEMS Microbiol., 2010, vol. 34, pp. 1037–1062. https://doi.org/10.1111/j.1574-6976.2010.00221.x

    Article  CAS  Google Scholar 

  44. Sabaté, D.C., Pérez, C., Petroselli, G., Erra-Balsells, R., and Adisio, M.C., Biocontrol of Sclerotinia sclerotiorum (Lib.) de Bary on common bean by native lipopeptide-producer Bacillus strains, Microbiol. Res., 2018, vol. 211, pp. 21–30. https://doi.org/10.1016/j.micres.2018.04.003

    Article  CAS  PubMed  Google Scholar 

  45. SAGARPA, Technical Manual for Sampling Agricultural Products and Water Sources for the Determination of Microbiological Pollutants, SAGARPA, 2015. https://www.cesavejal.org.mx/divulgacion/Manual%20Digital%202014/ 17.1%20manual_MUESTREO_MICROBIOLOGICO_ CORREGIDO1%20(3)(1)%20(2).pdf. Accessed November 4, 2015.

  46. Sarwar, A., Nadee, M., Imran, M., Iqbal, M., Majeed, S., Brader, G., Sessitsch, A., and Yusuf, F., Biocontrol activity of surfactin A purified from Bacillus NH-100 and NH-217 against rice bakanae disease, Microbiol. Res., 2018, vol. 209, pp. 1–13. https://doi.org/10.1016/j.micres.2018.01.006

    Article  CAS  PubMed  Google Scholar 

  47. Schwartz, H. and Singh, P., Breeding common bean for resistance to white mold, Crop Sci., 2013, vol. 53, p. 13. https://doi.org/10.2135/cropsci2013.02.0081

    Article  Google Scholar 

  48. Servicio Agrícola y Ganadero (SAG), Rutyl fungicide, Chile, ROTAM, 2017. https://www.sag.gob.cl/sites/default/files/rutyl_01-03-2017.pdf. Accessed July 29, 2018.

  49. Singh, P., Shin, Y., Park, C., and Chung, Y., Biological control of Fusarium wilt of cucumber by chitinolytic bacteria, Phytopathology, 1999, vol. 89, pp. 92–99. https://doi.org/10.1094/PHYTO.1999.89.1.92

    Article  CAS  PubMed  Google Scholar 

  50. Sivasakthi, S., Usharani, G., and Saranraj, P., Biocontrol potentially of plant growth promoting bacteria (PGPR)—Pseudomonas fluorescens and Bacillus subtilis: a review, Afr. J. Agric. Res., 2014, vol. 9, pp. 1265–1277. https://doi.org/10.5897/AJAR2013.7914

    Article  Google Scholar 

  51. Steindorff, A., Ramada, M.H., Coelho, A.S., Miller, R.N., Pappas, G., Ulhoa, C., and Noronha, E., Identification of mycoparasitism-related genes against the phytopathogen Sclerotinia sclerotiorum through transcriptome and expression profile analysis in Trichoderma harzianum, BMC Genomics, 2014, vol. 15, p. 204. https://doi.org/10.1186/1471-2164-15-204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Tejera-Hernández, B., Rojas-Badía, M.M., and Heydrich-Pérez, M., Potential of the genus Bacillus in the promotion of plant growth and biological control of phytopathogenic fungi Revista CENIC Ciencias Biológicas, 2011, vol. 42, pp. 131–138. Disponibleenlínea: http://www.redalyc.org/pdf/1812/ 181222321004.pdf

    Google Scholar 

  53. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G., The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools, Nucleic Acids Res., 1997, vol. 25, pp. 4876–4882.

    Article  CAS  Google Scholar 

  54. Torres, M.J., Pérez, C., Sabaté, D.C., Petroselli, G., Erra-Balsells, R., and Carina, M., Biological activity of the lipopeptide-producing Bacillus amyloliquefaciens PGPBacCA1 on common bean Phaseolus vulgaris L. pathogens, Biol. Control, 2017, vol. 105, pp. 93–99. https://doi.org/10.1016/j.biocontrol.2016.12.001

    Article  CAS  Google Scholar 

  55. Valenzuela-Aragon, B., Parra-Cota, F.I., Santoyo, G., Arellano-Wattenbarger, G.L., and de los Santos-Villalobos, S., Plant-assisted selection: a promising alternative for in vivo identification of wheat (Triticum turgidum L. subsp. Durum) growth promoting bacteria, Plant Soil, 2019, vol. 435, pp. 367–384. https://doi.org/10.1007/s11104-018-03901-1

    Article  CAS  Google Scholar 

  56. Valenzuela-Ruiz, V., Ayala-Zepeda, M., Arellano-Wattenbarger, L., Parra-Cota, F.I., García-Pereyra, J., Aviña-Martínez, G.N., and de los Santos-Villalobos, S., Microbial culture collections and their potential contribution to current and future food security, Rev. Lat. Ame. Rec. Nat., 2018, vol. 14, pp. 18–25. ISSN 2594-0384.

  57. Valenzuela-Ruiz, V., Robles-Montoya, R.I., Parra-Cota, F.I., Santoyo, G., Orozco-Mosqueda, M.C., Rodríguez-Ramírez, R., and de los Santos-Villalobos, S., Draft genome sequence of Bacillus paralicheniformis TRQ65, a biological control agent and plant growth-promoting bacterium isolated from wheat (Triticum turgidum subsp. durum) rhizosphere in the Yaqui Valley, Mexico, 3 Biotech, 2019, vol. 9, p. 436. https://doi.org/10.1007/s13205-019-1972-5

  58. Villa-Rodriguez, E., Lugo-Enríquez, C., de los Santos-Villalobos, S., Parra-Cota, F.I., and Figueroa-López, P., First report of Cochliobolus sativus causing spot blotch on durum wheat (Triticum durum) in The Yaqui Valley, Mexico, Plant Dis., 2016, vol. 100, p. 2329. https://doi.org/10.1094/PDIS-05-16-0634-PDN

    Article  Google Scholar 

  59. Villa-Rodríguez, E., Parra-Cota, F., Castro-Longoria, E., López-Cervantes, J., and de los Santos-Villalobos, S., Bacillus subtilis TE3: A promising biological control agent against Bipolaris sorokiniana, the causal agent of spot blotch in wheat (Triticum turgidum L. subsp. durum), Biol. Control, 2019, vol. 132, pp. 135–143. https://doi.org/10.1016/j.biocontrol.2019.02.012

    Article  CAS  Google Scholar 

  60. Villarreal-Delgado, M.F., Villa-Rodríguez, E.D., Cira-Chávez, L.A., Estrada-Alvarado, M.I., Parra-Cota, F.I., and de los Santos-Villalobos, S. The genus Bacillus as a biological control agent and itsimplications in theagriculturalbiosecurity, Rev. Mex. Fitopatol., 2018, vol. 36, pp. 95–130. https://doi.org/10.18781/R.MEX.FIT.1706-5

    Article  Google Scholar 

  61. Weisburg, W., Barns, S., Pelletier, D., and Lane, D. 16S ribosomal DNA amplification for phylogenetic study, J. Bacteriol., 1991, vol. 173, pp. 697–703. PMCID: PMC207061.

    Article  CAS  Google Scholar 

  62. White, T., Bruns, T., Lee, S., and Taylor, J., Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, in PCR—Protocols and Applications—A Laboratory Manual, Academic, 1990, pp. 315–322.

    Google Scholar 

  63. Willetts, H., Wong, J., and Kirst, G.D., The biology of Sclerotinia sclerotiorum, S. trifoliorum and S. minor with emphasis on specific nomenclature, Bot. Rev., 1980, vol. 46, pp. 101–165. https://doi.org/10.1007/BF02860868

    Article  Google Scholar 

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Funding

This study was funded by the CONACyT Project 253663, and Instituto Tecnológico de Sonora Proyect PROFAPI_2021_0006.

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Authors and Affiliations

  1. Instituto Tecnológico de Sonora, 5 de Febrero 818 Sur, Col. Centro C. P. 85000, Ciudad Obregón, Sonora, México

    María Fernanda Villarreal-Delgado, Luis Alberto Cira-Chávez, María Isabel Estrada-Alvarado & Sergio de los Santos-Villalobos

  2. Sartorius de México, Libramiento Norte de Tepotzotlán S/N Int 5, Col. Tlacateco, CP 54605, Tepotzotan, Estado de México, México

    María Fernanda Villarreal-Delgado

  3. Campo Experimental Norman E. Borlaug-INIFAP, Norman E. Borlaugkm. 12, C. P. 85000, Cd. Obregón, Sonora, México

    Fannie Isela Parra-Cota

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  3. Luis Alberto Cira-Chávez
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  4. María Isabel Estrada-Alvarado
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  5. Sergio de los Santos-Villalobos
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Correspondence to Sergio de los Santos-Villalobos.

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The authors declare that they have no conflict of interest. This article does not contain any studies with human participants or animals performed by any of the authors.

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María Fernanda Villarreal-Delgado, Parra-Cota, F.I., Cira-Chávez, L.A. et al. Bacillus sp. FSQ1: a Promising Biological Control Agent Against Sclerotinia sclerotiorum, the Causal Agent of white Mold in Common Bean (Phaseolus vulgaris L.). Biol Bull Russ Acad Sci 48, 729–739 (2021). https://doi.org/10.1134/S1062359021060182

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