Characterization of Actinobacterial Strains as Potential Biocontrol Agents against Macrophomina phaseolina and Rhizoctonia solani, the Main Soil-Borne Pathogens of Phaseolus vulgaris in Cuba
Abstract
:1. Introduction
2. Results
2.1. In Vitro Effect of Actinobacterial Strains against Macrophomina phaseolina and Rhizoctonia solani: Dual Culture Assays
2.2. Qualitative Evaluation of Enzyme Activities of Actinobacterial Strains
2.3. Phenotypic Characterization
2.4. Biochemical Characterization and Assimilation of Carbon Sources
2.5. Molecular Characterization
2.6. Effect of Actinobacterial Strains against Macrophomina phaseolina and Rhizoctonia solani Infections in Planta
2.6.1. Effect of Treatments against Macrophomina phaseolina in Planta
2.6.2. Effect of Treatments against Rhizoctonia solani in Planta
3. Discussion
4. Materials and Methods
4.1. Actinobacterial Strains and Growth Conditions
4.2. In Vitro Effect of Actinobacterial Strains against Macrophomina phaseolina and Rhizoctonia solani: Dual Culture Assays
4.3. Qualitative Evaluation of Enzyme Activities of Actinobacterial Strains
4.4. Phenotypic Characterization
4.5. Biochemical Characterization and Assimilation of Carbon Sources
4.6. Molecular Characterization
4.7. Effect of Actinobacterial Strains against Macrophomina phaseolina and Rhizoctonia solani Infections in Planta
4.7.1. Plant Material
4.7.2. Biological Control Agents and Inoculum Preparation
4.7.3. Soil Inoculation with Macrophomina phaseolina and Rhizoctonia solani
4.7.4. Seed Treatments, Growth Conditions and Experimental Design
4.7.5. Disease Severity Assessment
4.8. Data Analyses
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Actinobacterial Strain | (MGI; %) a,b | |
---|---|---|
Macrophomina phaseolina | Rhizoctonia solani | |
CBQ-CB-14 | 60.9 ± 1.63 | 69.8 ± 1.40 |
CBQ-EA-2 | 70.4 ± 1.23 | 77.4 ± 1.20 |
CBQ-EA-12 | 46.2 ± 1.32 | 78.3 ± 0.37 |
CBQ-OSS-3 | 62.8 ± 1.55 | 61.2 ± 0.53 |
CBQ-ESFe-4 | 52.0 ± 2.00 | 63.7 ± 1.19 |
CBQ-CD-24 | 64.6 ± 1.48 | 75.4 ± 1.22 |
CBQ-EBa-5 | 60.5 ± 1.65 | 45.9 ± 1.32 |
CBQ-EBa-21 | 54.0 ± 1.11 | 55.7 ± 2.01 |
CBQ-Plat-2 | 66.6 ± 0.78 | 37.3 ± 1.91 |
CBQ-WP-14 | 56.7 ± 1.81 | 37.1 ± 0.40 |
CBQ-B-8 | 63.1 ± 1.54 | 69.0 ± 1.63 |
CBQ-J-4 | 28.1 ± 1.71 | 35.4 ± 2.70 |
CBQ-CB-3 | 40.5 ± 0.91 | 40.1 ± 1.35 |
CBQ-EA-3 | 44.4 ± 0.65 | 0.0 ± 0.00 |
CBQ-EB-27 | 0.0 ± 0.00 | 0.0 ± 0.00 |
CBQ-EC-3 | 32.2 ± 0.60 | 0.0 ± 0.00 |
CBQ-EC-18 | 36.0 ± 1.30 | 54.6 ± 0.91 |
CBQ-ECa-24 | 29.9 ± 1.51 | 0.0 ± 0.00 |
CBQ-ESFe-5 | 31.6 ± 1.31 | 0.0 ± 0.00 |
CBQ-ESFe-10 | 35.8 ± 1.25 | 0.0 ± 0.00 |
CBQ-ESFe-11 | 3.24 ± 1.01 | 0.0 ± 0.00 |
CBQ-ESFe-12 | 38.9 ± 1.32 | 43.5 ± 1.92 |
CBQ-Mg-6 | 8.7 ± 0.42 | 0.0 ± 0.00 |
CBQ-Ni-24 | 21.2 ± 0.58 | 0.0 ± 0.00 |
CBQ-Ni-32 | 5.9 ± 0.34 | 0.0 ± 0.00 |
CBQ-OSS-4 | 8.9 ± 0.30 | 14.3 ± 2.38 |
CBQ-Plat-3 | 20.4 ± 1.52 | 0.0 ± 0.00 |
CBQ-Plat-4 | 24.2 ± 1.43 | 0.0 ± 0.00 |
CBQ-SFe-5 | 4.0 ± 0.11 | 0.0 ± 0.00 |
CBQ-Wni-21 | 28.3 ± 1.55 | 0.0 ± 0.00 |
CBQ-RS-3 | 4.7 ± 0.19 | 0.0 ± 0.00 |
CBQ-A-2 | 0.0 ± 0.00 | 0.0 ± 0.00 |
CBQ-A-9 | 0.0 ± 0.00 | 52.7 ± 2.98 |
CBQ-A-17 | 9.7 ± 0.33 | 32.6 ± 2.30 |
CBQ-Amb-3 | 0.0 ± 0.00 | 0.0 ± 0.00 |
CBQ-B-1 | 0.0 ± 0.00 | 35.0 ± 1.73 |
CBQ-B-41 | 0.0 ± 0.00 | 21.5 ± 0.63 |
CBQ-B-44 | 0.0 ± 0.00 | 41.5 ± 0.43 |
CBQ-Be-29 | 0.0 ± 0.00 | 0.0 ± 0.00 |
CBQ-Be-36 | 0.0 ± 0.00 | 0.0 ± 0.00 |
CBQ-C-5 | 0.0 ± 0.00 | 5.6 ± 0.47 |
CBQ-C-7 | 0.0 ± 0.00 | 17.8 ± 1.04 |
CBQ-CB-6 | 17.8 ± 1.78 | 0.0 ± 0.00 |
CBQ-CD-12 | 0.0 ± 0.00 | 0.0 ± 0.00 |
CBQ-CD-19 | 3.4 ± 0.32 | 0.0 ± 0.00 |
CBQ-CD-21 | 38.2 ± 1.26 | 0.0 ± 0.00 |
CBQ-CD-23 | 26.6 ± 1.56 | 0.0 ± 0.00 |
CBQ-CD-25 | 3.5 ± 0.36 | 0.0 ± 0.00 |
CBQ-Cy-5 | 0.0 ± 0.00 | 0.0 ± 0.00 |
CBQ-CYM-2 | 0.0 ± 0.00 | 0.0 ± 0.00 |
CBQ-E-5 | 0.0 ± 0.00 | 0.0 ± 0.00 |
CBQ-EA-29 | 17.7 ± 0.31 | 0.0 ± 0.00 |
CBQ-EBa-1 | 0.0 ± 0.00 | 0.0 ± 0.00 |
CBQ-EB-5 | 0.0 ± 0.00 | 0.0 ± 0.00 |
CBQ-EBa-22 | 0.0 ± 0.00 | 44.3 ± 1.40 |
CBQ-EBe-3 | 15.0 ± 0.12 | 0.0 ± 0.00 |
CBQ-EBe-15 | 0.0 ± 0.00 | 0.0 ± 0.00 |
CBQ-EBe-16 | 0.0 ± 0.00 | 0.0 ± 0.00 |
CBQ-EBe-19 | 16.1 ± 0.49 | 0.0 ± 0.00 |
CBQ-EBe-20 | 0.0 ± 0.00 | 0.0 ± 0.00 |
CBQ-EC-5 | 20.0 ± 0.78 | 53.2 ± 0.98 |
HSD0.05 | 6.7 | 8.5 |
Actinobacterial Strain | Chitinolytic Halo (mm) a | Cellulolytic Halo (mm) b | Proteolytic Halo (mm) c |
---|---|---|---|
CBQ-B-8 | 32.8 ± 0.96 ab | 90.0 ± 0.41 a | 41.3 ± 0.48 abcd |
CBQ-CB-3 | 0.0 ± 0.0 c | 49.3 ± 0.48 ab | 0.0 ± 0.0 e |
CBQ-CB-14 | 32.5 ± 2.65 ab | 90.0 ± 0.41 a | 50.8 ± 2.53 abc |
CBQ-CD-24 | 25.3 ± 0.96 b | 63.0 ± 2.38 ab | 34.5 ± 0.50 abcd |
CBQ-EA-2 | 34.0 ± 1.41 a | 86.3 ± 0.48 ab | 44.8 ± 1.65 abcd |
CBQ-EA-3 | 31.3 ± 0.96 ab | 36.3 ± 0.75 b | 31.8 ± 0.75 bcd |
CBQ-CB-4 | 0.0 ± 0.0 c | 86.3 ± 0.48 ab | 0.0 ± 0.0 e |
CBQ-EA-12 | 31.3 ± 3.20 ab | 80.0 ± 0.71 ab | 51.5 ± 1.50 a |
CBQ-EBa-5 | 33.5 ± 1.91 a | 85.3 ± 1.18 ab | 42.3 ± 0.25 abcd |
CBQ-EB-27 | 0.0 ± 0.0 c | 0.0 ± 0.0 c | 0.0 ± 0.0 e |
CBQ-EBa-21 | 29.8 ± 1.26 ab | 68.5 ± 1.19 ab | 47.8 ± 1.4 abc |
CBQ-EC-3 | 0.0 ± 0.0 c | 40.0 ± 0.71 ab | 0.0 ± 0.0 e |
CBQ-EC-18 | 29.3 ± 0.96 ab | 0.0 ± 0.0 c | 0.0 ± 0.0 e |
CBQ-ECa-24 | 0.0 ± 0.0 c | 90.0 ± 0.41 a | 27.0 ± 0.71 d |
CBQ-ESFe-4 | 24.8 ± 0.50 b | 82.3 ± 2.59 ab | 0.0 ± 0.0 e |
CBQ-ESFe-5 | 0.0 ± 0.0 c | 88.8 ± 0.75 ab | 41.3 ± 2.39 abcd |
CBQ-ESFe-10 | 31.3 ± 0.96 ab | 81.8 ± 1.80 ab | 0.0 ± 0.0 e |
CBQ-ESFe-11 | 32.3 ±2.90 ab | 84.5 ± 1.55 ab | 0.0 ± 0.0 e |
CBQ-ESFe-12 | 29.0 ± 1.41 ab | 90.0 ± 0.41 a | 49.0 ± 0.71 ab |
CBQ-J-4 | 27.0 ± 1.41 ab | 45.0 ± 1.41 ab | 27.3 ± 0.48 d |
CBQ-Mg-6 | 0.0 ± 0.0 c | 62.0 ± 0.71 ab | 44.8 ± 0.48 abcd |
CBQ-Ni-24 | 27.3 ± 0.96 ab | 88.8 ± 0.75 ab | 31.8 ± 025 cd |
CBQ-Ni-32 | 29.8 ± 0.50 ab | 90.0 ± 0.41 a | 37.3 ± 0.48 abcd |
CBQ-OSS-3 | 33.0 ± 4.8 ab | 67.0 ± 0.71 ab | 39.3 ± 0.48 abcd |
CBQ-OSS-4 | 0.0 ± 0.0 c | 0.0 ± 0.0 c | 44.0 ± 0.71 abcd |
CBQ-Plat-2 | 29.8 ± 0.50 ab | 90.0 ± 0.41 a | 44.3 ± 0.75 abcd |
CBQ-Plat-3 | 0.0 ± 0.0 c | 90.0 ± 0.41 a | 32.8 ± 0.25 abcd |
CBQ-Plat-4 | 31.3 ± 0.96 ab | 90.0 ± 0.41 a | 33.5 ± 0.50 abcd |
CBQ-SFe-5 | 28.3 ± 3.36 ab | 47.3 ± 0.75 ab | 0.0 ± 0.0 e |
CBQ-Wni-21 | 0.0 ± 0.0 c | 42.3 ± 0.48 ab | 36.5 ± 0.95 abcd |
CBQ-WP-14 | 29.8 ± 0.50 ab | 90.0 ± 0.41 a | 44.0 ± 0.71 abc |
Actinobacterial Strain Code | Gram Stain a | Aerial Mycelium b | Color | Shape | Elevation | Edge | Consistency | Pigment |
---|---|---|---|---|---|---|---|---|
CBQ-B-8 | + | + | White | Circular | Convex | Full | Hard | Yellow |
CBQ-CB-14 | + | + | White | Circular | Convex | Full | Hard | Yellow |
CBQ-CD-24 | + | + | White | Irregular | Convex | Whole | Hard | Beige |
CBQ-EA-2 | + | + | White | Circular | Convex | Lobed | Hard | Yellow |
CBQ-EA-12 | + | + | White | Circular | Pulvini | Whole | Hard | Brown |
CBQ-EBa-5 | + | + | Yellow | Irregular | Convex | Lobular | Hard | Yellow |
CBQ-EBa-21 | + | + | White | Irregular | Pulvini | Whole | Hard | Orange |
CBQ-ESFe-4 | + | + | Yellow | Circular | Convex | Lobed | Hard | Beige |
CBQ-J-4 | + | + | White | Circular | Convex | Whole | Hard | Beige |
CBQ-OSS-3 | + | + | Yellow | Irregular | Convex | Lobular | Hard | Yellow |
CBQ-Plat-2 | + | + | White | Circular | Convex | Whole | Hard | Yellow |
Biochemical Parameters * | Actinobacterial Strain Code | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
CBQ-B-8 | CBQ-CB-14 | CBQ-CD-24 | CBQ-EA-2 | CBQ-EA-12 | CBQ-EBa-5 | CBQ-EBa-21 | CBQ-ESFe-4 | CBQ-J-4 | CBQ-OSS-3 | CBQ-Plat-2 | |
Catalase production | + | + | + | + | + | + | + | + | + | + | + |
Lactose Fermentation | + | + | + | + | - | - | - | + | - | + | - |
Glucose Fermentation | + | + | + | + | + | D | - | - | + | D | + |
Mannitol Fermentation | + | + | - | + | - | + | - | + | - | - | - |
Dextrose Fermentation | - | - | + | + | D | - | D | + | - | - | + |
Fructose Fermentation | + | + | + | + | + | + | + | + | - | - | + |
Maltose Fermentation | + | + | + | + | + | + | + | D | + | + | - |
Sucrose Fermentation | + | + | + | + | + | + | + | D | + | - | - |
Xylose Fermentation | + | + | - | + | + | - | + | + | - | + | + |
Raffinose Fermentation | + | + | + | D | - | - | + | + | + | + | D |
Casein Hydrolysis | - | - | - | + | - | + | - | - | + | + | - |
Citrate Utilization | + | + | + | + | + | + | + | + | + | + | + |
Urea Hydrolysis | + | + | + | + | + | + | + | + | + | + | + |
Nitrate reduction | + | + | + | + | + | + | + | + | + | + | + |
Indole production | - | - | - | - | - | - | - | - | - | - | - |
Methyl red | + | + | - | + | - | + | + | - | - | - | + |
Voges Proskauer | - | - | - | - | - | - | - | - | - | - | - |
Gelatin hydrolysis | + | + | + | + | - | + | + | - | + | + | + |
Starch hydrolysis | + | + | + | + | + | + | + | + | + | - | - |
Species | Isolate | Genbank Accession a | Blast Accession b | Query Length | Gaps c | Identities d | Maximum Identity (%) |
---|---|---|---|---|---|---|---|
Streptomyces sp. | CBQ-EA-2 | OM417233 | MT540570 | 1437 | 3/1390 | 1386/1390 | 99.71 |
Streptomices sp. | CBQ-B-8 | OM417234 | EU263063 | 1491 | 1/1491 | 1490/1491 | 99.93 |
Strain * | Isolation Substrate | Origin (Location, State) | Year of Collection |
---|---|---|---|
CBQ-RS-3 | Sediment | River Seibabo, Villa Clara | 2007 |
CBQ-A-2 | Rhizosphere | Arco Iris, V. Clara | 2007 |
CBQ-EA-2 a–c | Endophytic, stem of Mosiera bullata | Arco Iris, V. Clara | 2008 |
CBQ-B-8 a–c | Rhizosphere, Carbonated brown | Botanical Garden UCLV, V. Clara | 2008 |
CBQ-J-4 b,c | Rhizosphere Ferrallitic red | River Seco, Jibacoa, Manicarargua. V. Clara | 2008 |
CBQ-A-9 | Rhizosphere | Arco Iris, V. Clara | 2008 |
CBQ-A-17 | Rhizosphere | Arco Iris, V. Clara | 2008 |
CBQ-C-5 | Rhizosphere | Cienfuegos | 2008 |
CBQ-C-7 | Rhizosphere | Cienfuegos | 2008 |
CBQ-B-1 | Rhizosphere | Botanical GardenUCLV, V. Clara | 2008 |
CBQ-E-5 | ‘Fangos de Elguea’ | Corralillo, V. Clara | 2009 |
CBQ-B-41 | Rhizosphere | Botanical Garden UCLV, V. Clara | 2009 |
CBQ-B-44 | Rhizosphere | Botanical Garden UCLV, V. Clara | 2009 |
CBQ-Be-29 | Rhizosphere | Escambray, Bernal | 2010 |
CBQ-EC-3 b | Endophytic | Coge Finca, Camajuaní, V. Clara | 2010 |
CBQ-EC-5 | Endophytic, stem of Petiveria alliacea. | V. Clara | 2010 |
CBQ-Be-36 | Rhizosphere | Escambray, Bernal | 2010 |
CBQ-EBe-3 | Endophytic, root of Hibiscus elatus | Bernal, Herradura, Manicarargua, V. Clara | 2010 |
CBQ-Cy-5 | Rhizosphere | Key I, V. Clara | 2010 |
CBQ-CYM-2 | Rhizosphere | Salinas, V. Clara | 2010 |
CBQ-EA-29 | Endophytic, stem | Arco Iris, V. Clara | 2011 |
CBQ-EBa-1 | Endophytic, root | Banao, S. Spíritus | 2011 |
CBQ-EB-5 | Endophytic | Botanical Garden UCLV, V. Clara | 2011 |
CBQ-EBa-22 | Endophytic, stem | Banao, S. Spíritus | 2011 |
CBQ-EBe-15 | Endophytic, root | Planta Escambray, Bernal | 2011 |
CBQ-EBe-16 | Endophytic, root | Planta Escambray, Bernal | 2011 |
CBQ-EBe-20 | Endophytic, root | Planta Escambray, Bernal | 2011 |
CBQ-EA-3 b | Endophytic | Arco Iris. V. Clara | 2011 |
CBQ-EB-27 b | Endophytic, Stem | Jandín Botánico UCLV, V. Clara | 2011 |
CBQ-EA-12 a,b | Endophytic, leaf of Mosiera bullata, | Arco Iris. V. Clara | 2011 |
CBQ-EC-18 b | Endophytic, stem of Petiveria alliacea. | Coge Finca, Camajuaní, V. Clara | 2011 |
CBQ-ECa-24 b | Endophytic, root | Caguanes, S. Spíritus | 2011 |
CBQ-EBa-5 a,b | Endophytic, root | Banao. S. Spíritus | 2011 |
CBQ-EBa-21 a,b | Endophytic, root of Piper aducum | Banao. S. Spíritus | 2011 |
CBQ-Ni-24 b | Endophytic, stem | Nicho, V. Clara | 2011 |
CBQ-Ni-32 b | Endophytic, stem | Nicho, V. Clara | 2011 |
CBQ-ESFe-12 b | Endophytic, stem of Fleurya cuneata, | Loma Sta Fé, V. Clara | 2012 |
CBQ-ESFe-5 b | Endophytic, stem of Fleurya cuneata, | Loma Sta Fé, V Clara | 2012 |
CBQ-ESFe-10 b | Endophytic, stem of Fleurya cuneata, | Loma Sta Fé, V. Clara | 2012 |
CBQ-ESFe-11 b | Endophytic, stem of Fleurya cuneata, | Loma Sta Fé, V. Clara | 2012 |
CBQ-WP-14 b | Sediment, Clarias batrachus, | V. Clara | 2012 |
CBQ-ESFe-4 a,b | Endophytic, leaf of Piper aduncum | Loma Santa Fé. V. Clara | 2012 |
CBQ-Wni-21 b | Sediment | River Nicho, V. Clara | 2012 |
CBQ-Amb-3 | Endophytic, Stem of Cecropia adenopu, | V. Clara | 2013 |
CBQ-CB-14 a,b | Sediment | Caves de Bellamar, Matanzas | 2013 |
CBQ-OSS-4 b | Endophytic | Topes de Collantes, S. Spíritus | 2013 |
CBQ-Plat-3 b | Endophytic, Stem of Comocladia platyphylla. | V. Clara | 2013 |
CBQ-Plat-4 b | Endophytic, Root of Comocladia platyphylla, | V. Clara | 2013 |
CBQ-CB-3 b | Sediment | Caves de Bellamar, Matanzas | 2013 |
CBQ-Plat-2 a,b | Endophytic, stem of Comocladia platyphylla. | V. Clara | 2013 |
CBQ-OSS-3 a,b | Endophytic, leaf of Ossanum | Topes de Collantes, S. Spíritus | 2013 |
CBQ-CB-4 b | Sediment | Caves de Bellamar, Matanzas | 2013 |
CBQ-CD-12 | Rhizosphere | Key Las Dunas, V. Clara | 2014 |
CBQ-CD-19 | Rhizosphere | Key Las Dunas, V. Clara | 2014 |
CBQ-CD-21 | Rhizosphere | Key Las Dunas, V. Clara | 2014 |
CBQ-CD-23 | Rhizosphere | Key Las Dunas, V. Clara | 2014 |
CBQ-CD-25 | Rhizosphere | Key Las Dunas, V. Clara | 2014 |
CBQ-CD-24 a,b | Rhizosphere | Key Las Dunas. V. Clara | 2014 |
CBQ-Mg-6 b | Endophytic, stem of Rhizophora mangle | Mégano, La Habana | 2014 |
CBQ-SFe-5 b | Rhizosphere | Sta Fé, V. Clara | 2015 |
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Díaz-Díaz, M.; Bernal-Cabrera, A.; Trapero, A.; Medina-Marrero, R.; Sifontes-Rodríguez, S.; Cupull-Santana, R.D.; García-Bernal, M.; Agustí-Brisach, C. Characterization of Actinobacterial Strains as Potential Biocontrol Agents against Macrophomina phaseolina and Rhizoctonia solani, the Main Soil-Borne Pathogens of Phaseolus vulgaris in Cuba. Plants 2022, 11, 645. https://doi.org/10.3390/plants11050645
Díaz-Díaz M, Bernal-Cabrera A, Trapero A, Medina-Marrero R, Sifontes-Rodríguez S, Cupull-Santana RD, García-Bernal M, Agustí-Brisach C. Characterization of Actinobacterial Strains as Potential Biocontrol Agents against Macrophomina phaseolina and Rhizoctonia solani, the Main Soil-Borne Pathogens of Phaseolus vulgaris in Cuba. Plants. 2022; 11(5):645. https://doi.org/10.3390/plants11050645
Chicago/Turabian StyleDíaz-Díaz, Miriam, Alexander Bernal-Cabrera, Antonio Trapero, Ricardo Medina-Marrero, Sergio Sifontes-Rodríguez, René Dionisio Cupull-Santana, Milagro García-Bernal, and Carlos Agustí-Brisach. 2022. "Characterization of Actinobacterial Strains as Potential Biocontrol Agents against Macrophomina phaseolina and Rhizoctonia solani, the Main Soil-Borne Pathogens of Phaseolus vulgaris in Cuba" Plants 11, no. 5: 645. https://doi.org/10.3390/plants11050645
APA StyleDíaz-Díaz, M., Bernal-Cabrera, A., Trapero, A., Medina-Marrero, R., Sifontes-Rodríguez, S., Cupull-Santana, R. D., García-Bernal, M., & Agustí-Brisach, C. (2022). Characterization of Actinobacterial Strains as Potential Biocontrol Agents against Macrophomina phaseolina and Rhizoctonia solani, the Main Soil-Borne Pathogens of Phaseolus vulgaris in Cuba. Plants, 11(5), 645. https://doi.org/10.3390/plants11050645