Ascochyta blight (Ascochyta fabae) of faba bean (Vicia faba L.): phenotypic and molecular characterization, pathogenicity and in vitro biological control by Bacillus spp. and Pseudomonas spp.

Authors

  • Bouchra Oguiba Laboratory of Applied Microbiology, Department of Biology, Faculty of Natural and Life Sciences, University of Oran 1 Ahmed Ben Bella, BP1524, El M’naouer-31000 Oran, Algeria https://orcid.org/0000-0001-7252-3183
  • Noureddine Karkachi Laboratory of Applied Microbiology, Department of Biology, Faculty of Natural and Life Sciences, University of Oran 1 Ahmed Ben Bella, BP1524, El M’naouer-31000 Oran, Algeria https://orcid.org/0000-0002-3162-5279
  • Francisca Suárez-Estrella Department of Biology and Geology, University of Almería, Agrifood Campus of International Excellence (ceiA3), Center for Research in Mediterranean Intensive Agrosystems and Agri-Food Biotechnology (CIAIMBITAL), 04120 Almería, Spain https://orcid.org/0000-0003-2549-947X
  • Sadika Haouhach Department of Biotechnology, University of Science and Technology of Oran Mohamed Boudiaf, 31000 Oran, Algeria https://orcid.org/0000-0001-6419-0737
  • Mebrouk Kihal Laboratory of Applied Microbiology, Department of Biology, Faculty of Natural and Life Sciences, University of Oran 1 Ahmed Ben Bella, BP1524, El M’naouer-31000 Oran, Algeria https://orcid.org/0000-0003-2901-373X
  • María J. López Department of Biology and Geology, University of Almería, Agrifood Campus of International Excellence (ceiA3), Center for Research in Mediterranean Intensive Agrosystems and Agri-Food Biotechnology (CIAIMBITAL), 04120 Almería, Spain https://orcid.org/0000-0002-3153-3227

DOI:

https://doi.org/10.2298/ABS230203009O

Keywords:

Ascochyta blight, Ascochyta fabae, biological control, faba bean, pathogenicity, Vicia faba L.

Abstract

Paper description:

  • Ascochyta blight (Ascochyta fabae) is a major biotic constraint for faba bean (Vicia faba ) production worldwide. No information is available in the literature on local isolates from Algeria, and no studies on its biological control exist.
  • 14 strains of fabae were isolated and identified by morpho-molecular characterization and the pathogenicity assay. Isolates were separated into three groups according to their level of aggressiveness.
  • Bacillus siamensis B8 and Bacillus mojavensis B31 were the most effective against all isolates. fabae aggressiveness was negatively correlated with susceptibility to biocontrol strains.
  • These findings have important implications for epidemiological studies and disease management.

Abstract: Ascochyta blight is a major biotic constraint of faba bean (Vicia faba L.) production and productivity worldwide caused by Ascochyta fabae. No studies have been performed in Algeria to identify A. fabae isolates or to assess their pathogenicity, and therefore information on local isolates is insufficient. Herein, 14 isolates of A. fabae were obtained from faba bean samples and identified based on morphological traits and phylogenetic analysis of internal transcribed spacer sequences. All generated sequences have been deposited in GenBank and assigned accession numbers. Pathogenicity tests on faba bean plants revealed that all isolates produced necrotic lesions on aerial parts with variable intensity, classifying them as weakly, moderately, and highly aggressive. The in vitro antifungal activity of Bacillus and Pseudomonas strains against A. fabae isolates showed that Bacillus siamensis B8 and Bacillus mojavensis B31 had the highest suppressive potential against all isolates. Moreover, a negative correlation was found between the aggressiveness of A. fabae isolates and their susceptibility to biocontrol strains. This is the first report on the identification, pathogenicity and in vitro biological control of A. fabae isolates in Algeria. B8 and B31 could be further developed as promising biocontrol agents for the control of the ascochyta blight of faba bean.

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References

Stagnari F, Maggio A, Galieni A, Pisante M. Multiple benefits of legumes for agriculture sustainability: an overview. Chem Biol Technol Agric. 2017;4(1):1-13. https://doi.org/10.1186/s40538-016-0085-1

De Ron AM. Grain legumes. Springer; 2015. https://doi.org/10.1007/978-1-4939-2797-5

Bessada SMF, Barreira JCM, Oliveira MBPP. Trends in Food Science & Technology Pulses and food security : Dietary protein, digestibility, bioactive and functional properties. Trends Food Sci Technol. 2019;93(228):53–68. https://doi.org/10.1016/j.tifs.2019.08.022

Boeck T, Sahin AW, Zannini E, Arendt EK. Nutritional properties and health aspects of pulses and their use in plant-based yogurt alternatives. Compr Rev Food Sci Food Saf. 2021;20:3858–80. https://doi.org/10.1111/1541-4337.12778

FAOSTAT. World Statistics on faba bean. Food Agric Organ United Nations, Rome [Internet]. 2020 [cited 2022 Aug 08]. Available from: http://faostat.fao.org/

Alharbi NH, Adhikari KN. Factors of yield determination in faba bean (Vicia faba). Crop Pasture Sci. 2020;71(4):305–21. https://doi.org/10.1071/cp19103

Mínguez MI, Rubiales D. Faba bean. In: Crop physiology case histories for major crops. Elsevier; 2021. p. 452–81.

O’Sullivan DM, Angra D. Advances in faba bean genetics and genomics. Front Genet. 2016;7:150. https://doi.org/10.3389/fgene.2016.00150

Ahmed S, Abang MM, Maalouf F. Integrated management of Ascochyta blight (Didymella fabae) on faba bean under Mediterranean conditions. Crop Prot. 2016;(81):65–9. http://dx.doi.org/10.1016/j.cropro.2015.12.013

Stoddard FL, Nicholas AH, Rubiales D, Thomas J, Villegas-Fernández AM. Integrated pest management in faba bean. F Crop Res. 2010;115(3):308–18. https://doi.org/10.1016/j.fcr.2009.07.002

Hernandez-Bello MA, Chilvers MI, Akamatsu H, Peever TL. Host specificity of Ascochyta spp. infecting legumes of the viciae and cicerae tribes and pathogenicity of an interspecific hybrid. Phytopathology. 2006;96(10):1148–56. https://doi.org/10.1094/PHYTO-96-1148

Kaiser WJ, Wang BC, Rogers JD. Ascochyta fabae and A. lentis: Host specificity, teleomorphs (Didymella), hybrid analysis, and taxonomic status. Plant Dis. 1997;81(7):809–16. https://doi.org/10.1094/PDIS.1997.81.7.809

Tivoli B, Baranger A, Avila CM, Banniza S, Barbetti M, Chen W, Davidson J, Lindeck K, Kharrat M, Rubiales D, Sadiki M, Sillero JC, Sweetingham M, Muehlbauer FJ. Screening techniques and sources of resistance to foliar diseases caused by major necrotrophic fungi in grain legumes. Euphytica. 2006;147(1–2):223–53. https://doi.org/10.1007/s10681-006-3131-4

Muehlbauer FJ, Chen W. Resistance to ascochyta blights of cool season food legumes. Eur J Plant Pathol. 2007;119(1):135–41. https://doi.org/10.1007/s10658-007-9180-2

Omri Benyoussef N, Le May C, Mlayeh O, Kharrat M. First report of Didymella fabae, teleomorph of Ascochyta fabae, on faba bean crop debris in Tunisia. Phytopathol Mediterr. 2012;51(2):369–73.

Kaur S, Kimber RBE, Cogan NOI, Materne M, Forster JW, Paull JG. SNP discovery and high-density genetic mapping in faba bean (Vicia faba L.) permits identification of QTLs for ascochyta blight resistance. Plant Sci. 2014;47–55. http://dx.doi.org/10.1016/j.plantsci.2013.11.014

Hanounik S. Effect of chemical treatments and host genotypes on disease severity/yield relationships of Ascochyta blight in faba beans (Vicia faba). FABIS Newsl. 1980;2:50.

Faridi R, Koopman B, Schierholt A, Ali MB, Apel S, Link W. Genetic study of the resistance of faba bean (Vicia faba) against the fungus Ascochyta fabae through a genome-wide association analysis. Plant Breed. 2021;140(3):442–52. https://onlinelibrary.wiley.com/doi/full/10.1111/pbr.12918

Abdulkareem MK, Kimber RBE, Scott ES. Interactions between Ascochyta fabae and Cercospora zonata, fungal pathogens of faba bean. Australas Plant Pathol. 2019;48(3):271–80. https://doi.org/10.1007/s13313-019-00627-1

Sillero JC, Rubiales D. Response of Vicia Species to Ascochyta fabae and Uromyces viciae-fabae. Czech J Genet Plant Breed. 2014;50(2):109–115. https://doi.org/10.17221/132/2013-CJGPB

Rubiales D, Khazaei H. Advances in disease and pest resistance in faba bean. Theor Appl Genet. 2022;135:3735-56. https://doi.org/10.1007/s00122-021-04022-7

Chang KF, Ahmed HU, Hwang SF, Gossen BD, Strelkov SE, Blade SF, Turnbull GD. Sensitivity of field populations of Ascochyta rabiei to chlorothalonil, mancozeb and pyraclostrobin fungicides and effect of strobilurin fungicides on the progress of ascochyta blight of chickpea. Can J Plant Sci. 2007;87(4):937–44. https://doi.org/10.4141/CJPS07019

Gikas GD, Parlakidis P, Mavropoulos T, Vryzas Z. Particularities of Fungicides and Factors Affecting Their Fate and Removal Efficacy: A Review. Sustain. 2022;14(7):1–23. https://doi.org/10.3390/su14074056

De Vrieze M, Gloor R, Codina JM, Torriani S, Gindro K, L’Haridon F, Bailly A, Weisskopf L. Biocontrol activity of three pseudomonas in a newly assembled collection of phytophthora infestans isolates. Phytopathology. 2019;109(9):1555–65. https://doi.org/10.1094/PHYTO-12-18-0487-R

Al-Fadhal FA, AL-Abedy AN, Alkhafije DA. Isolation and molecular identification of Rhizoctonia solani and Fusarium solani isolated from cucumber (Cucumis sativus L.) and their control feasibility by Pseudomonas fluorescens and Bacillus subtilis. Egypt J Biol Pest Control. 2019;29(1):1–11. https://doi.org/10.1186/s41938-019-0145-5

Sharma M, Tarafdar A, Pandey A, Ahmed S, Pandey V, Chobe DR, Ghosh R, Nair RM, Pandey S, Reddy MSP, Maalouf F, Kumari SG. Biotic Stresses in Food Legumes: An Update and Future Prospects. In: Saxena KB, Saxena RK, Varshney RK, editors. Genetic Enhancement in Major Food Legumes. Cham: Springer; 2021. p. 149–96. https://doi.org/10.1007/978-3-030-64500-7_6

Weisskopf L. The potential of bacterial volatiles for crop protection against phytophathogenic fungi. Microb Pathog Strateg Combat them Sci Technol Educ. 2013;(January):1352–63.

Dimkić I, Janakiev T, Petrović M, Degrassi G, Fira D. Plant-associated Bacillus and Pseudomonas antimicrobial activities in plant disease suppression via biological control mechanisms - A review. Physiol Mol Plant Pathol. 2022;117:101754. https://doi.org/10.1016/j.pmpp.2021.101754

Sánchez San Fulgencio N, Suárez-Estrella F, López MJ, Jurado MM, López-González JA, Moreno J. Biotic aspects involved in the control of damping-off producing agents: The role of the thermotolerant microbiota isolated from composting of plant waste. Biol Control. 2018;124:82–91. https://doi.org/10.1016/j.biocontrol.2018.04.015

Suárez-Estrella F, Jurado MM, López MJ, López-González JA, Moreno J. Biocatalysis and Agricultural Biotechnology Role of bacteria isolated from a plant waste-based compost producing bioactive substances in the control of bacterial spot syndrome caused by Xanthomonas campestris pv . vesicatoria. Biocatal Agric Biotechnol. 2019;20:101198. https://doi.org/10.1016/j.bcab.2019.101198

Kohpina S, Knight R, Stoddard FL. Variability of Ascochyta fabae in South Australia. Aust J Agric Res. 1999;(50):1475–81. https://doi.org/10.1071/AR98204

White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols: A Guide to Methods and Applications. San Diego, CA : Academic Press; 1990. p. 315–22. https://doi.org/10.1016/B978-0-12-372180-8.50042-1

Hall Thomas. BioEdit: a user-firendly biological sequence alignment editor and analysis program for Windows 95/95/NT. Nucleic Acids Symp. 1999;41:95–8.

Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22(22):4673–80. https://doi.org/10.1093/nar/22.22.4673

Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17(4):540–52. https://doi.org/10.1093/oxfordjournals.molbev.a026334

Padder BA, Kapoor V, Kaushal RP, Sharma PN. Identification and Genetic Diversity Analysis of Ascochyta Species Associated with Blight Complex of Pea in a Northwestern Hill State of India. Agric Res. 2012;1(4):325–37. https://doi.org/10.1007/s40003-012-0033-7

Peever TL, Barve MP, Stone LJ, Kaiser WJ. Evolutionary relationships among Ascochyta species infecting wild and cultivated hosts in the legume tribes Cicereae and Vicieae. Mycologia. 2007;99(1):59–77. https://doi.org/10.3852/mycologia.99.1.59

Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547–9. https://doi.org/10.1093/molbev/msy096

Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980;16(2):111–20.

Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9(8):772. https://doi.org/10.1038/nmeth.2109

Landa BB, Hervás A, Bettiol W, Jiménez-Díaz RM. Antagonistic activity of bacteria from the chickpea rhizosphere against Fusarium oxysporum f. sp. ciceris. Phytoparasitica. 1997;25(4):305–18. https://doi.org/10.1007/BF02981094

Rashid KY, Bernier CC, Conner RL. Evaluation of faba bean for resistance to Ascochyta fabae and development of host differentials for race identification. Plant Dis. 1991;75(8):852–5. https://doi.org/10.1094/PD-75-0852

Bernier CC, Hanounik SB, Hussen MM, Mohamed HA. Field manual of common bean diseases in the Nile Valley. ICARDA Inf Bull. 1984;3:40.

RStudio Team. RStudio: Integrated Development for R. RStudio, PBC, Boston, MA. 2020 [cited 2022 Jan 14]. Available from: http://www.rstudio.com/.

Lever J, Krzywinski M, Altman N. Principal component analysis. Nat Publ Gr. 2017;14(7):641–2. http://dx.doi.org/10.1038/nmeth.4346

Abdi H, Williams LJ. Principal component analysis. Comput Stat. 2010;2(4):433–59. https://doi.org/10.1002/wics.101

Peever TL. Role of host specificity in the speciation of Ascochyta pathogens of cool season food legumes. Eur J Plant Pathol. 2007;119(1):119–26. https://doi.org/10.1007/s10658-007-9148-2

Mel’nik VA, Braun U, Hagedorn G. Key to the fungi of the genus Ascochyta Lib . ( Coelomycetes ). Berlin: Parey Buchverlag; 2000. 192 p.

Jellis GJ, Punithalingam E. Discovery of Didymella fabae sp . nov ., the teleomorph of Ascochyta fabae , on faba bean straw. Plant Pathol. 1991;40(1):150-7. https://doi.org/10.1111/j.1365-3059.1991.tb02305.x

Tivoli B, Banniza S. Comparison of the epidemiology of ascochyta blights on grain legumes. Eur J Plant Pathol. 2007;119(1):59–76. https://doi.org/10.1007/s10658-007-9117-9

Saha M, Sarkar S, Sarkar B, Sharma BK, Bhattacharjee S, Tribedi P. Microbial siderophores and their potential applications: a review. Environ Sci Pollut Res. 2016;23(5):3984–99. https://doi.org/10.1007/s11356-015-4294-0

Elnahal ASM, El-Saadony MT, Saad AM, Desoky ESM, El-Tahan AM, Rady MM, AbuQamar SF, El-Tarabily KA. The use of microbial inoculants for biological control, plant growth promotion, and sustainable agriculture: A review. Eur J Plant Pathol. 2022;162(4):759–92. https://doi.org/10.1007/s10658-021-02393-7

Shen N, Li S, Li SY, Zhang H, Jiang M. The siderophore-producing bacterium, Bacillus siamensis Gxun-6, has an antifungal activity against Fusarium oxysporum and promotes the growth of banana. Egypt J Biol Pest Control. 2022;32(1):34. https://doi.org/10.1186/s41938-022-00533-7

Pal KK, Gardener BM. Biological control of plant pathogens. Plant Heal Instr. 2006. https://doi.org/10.1094/PHI-A-2006-1117-02

Hunziker L, Bönisch D, Groenhagen U, Bailly A, Schulz S, Weisskopf L. Pseudomonas strains naturally associated with potato plants produce volatiles with high potential for inhibition of Phytophthora infestans. Appl Environ Microbiol. 2015;81(3):821–30. https://doi.org/10.1128/AEM.02999-14

De Vrieze M, Germanier F, Vuille N, Weisskopf L. Combining Different Potato-Associated Pseudomonas Strains for Improved Biocontrol of Phytophthora infestans. Front Microbiol. 2018;9:02573. https://doi.org/10.3389/fmicb.2018.02573

Anand A, Chinchilla D, Tan C, Mène-Saffrané L, L’haridon F, Weisskopf L. Contribution of hydrogen cyanide to the antagonistic activity of pseudomonas strains against phytophthora infestans. Microorganisms. 2020;8(8):1144. https://doi.org/10.3390/microorganisms8081144

Heydari A, Pessarakli M. A review on biological control of fungal plant pathogens using microbial antagonists. J Biol Sci. 2010;10(4):273–90. https://doi.org/10.3923/jbs.2010.273.290

Shali A, Ghasemi S, Ahmadian G, Ranjbar G, Dehestani A, Khalesi N, Motallebi E, Vahed M. Bacillus pumilus SG2 chitinases induced and regulated by chitin, show inhibitory activity against Fusarium graminearum and Bipolaris sorokiniana. Phytoparasitica. 2010;38(2):141–7. https://doi.org/10.1007/s12600-009-0078-8

Gupta CP, Kumar B, Dubey RC, Maheshwari DK. Chitinase-mediated destructive antagonistic potential of Pseudomonas aeruginosa GRC1 against Sclerotinia sclerotiorum causing stem rot of peanut. BioControl. 2006;51(6):821–35. https://doi.org/10.1007/S10526-006-9000-1

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2023-04-03

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Oguiba B, Karkachi N, Suárez-Estrella F, Haouhach S, Kihal M, López MJ. Ascochyta blight (Ascochyta fabae) of faba bean (Vicia faba L.): phenotypic and molecular characterization, pathogenicity and in vitro biological control by Bacillus spp. and Pseudomonas spp. Arch Biol Sci [Internet]. 2023Apr.3 [cited 2024Nov.21];75(1):103-17. Available from: https://serbiosoc.org.rs/arch/index.php/abs/article/view/8375

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Vol. 75 No. 1 (2023)

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Copyright (c) 2023 Bouchra OGUIBA, Noureddine KARKACHI, Francisca SUÁREZ-ESTRELLA , Sadika HAOUHACH, Mebrouk KIHAL, María J. LÓPEZ

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