Suppressive Effects of Volatile Compounds from Bacillus spp. on Magnaporthe oryzae Triticum (MoT) Pathotype, Causal Agent of Wheat Blast

The Magnaporthe oryzae Triticum (MoT) pathotype is the causal agent of wheat blast, which has caused significant economic losses and threatens wheat production in South America, Asia, and Africa. Three bacterial strains from rice and wheat seeds (B. subtilis BTS-3, B. velezensis BTS-4, and B. velezensis BTLK6A) were used to explore the antifungal effects of volatile organic compounds (VOCs) of Bacillus spp. as a potential biocontrol mechanism against MoT. All bacterial treatments significantly inhibited both the mycelial growth and sporulation of MoT in vitro. We found that this inhibition was caused by Bacillus VOCs in a dose-dependent manner. In addition, biocontrol assays using detached wheat leaves infected with MoT showed reduced leaf lesions and sporulation compared to the untreated control. VOCs from B. velezensis BTS-4 alone or a consortium (mixture of B. subtilis BTS-3, B. velezensis BTS-4, and B. velezensis BTLK6A) of treatments consistently suppressed MoT in vitro and in vivo. Compared to the untreated control, VOCs from BTS-4 and the Bacillus consortium reduced MoT lesions in vivo by 85% and 81.25%, respectively. A total of thirty-nine VOCs (from nine different VOC groups) from four Bacillus treatments were identified by gas chromatography–mass spectrometry (GC–MS), of which 11 were produced in all Bacillus treatments. Alcohols, fatty acids, ketones, aldehydes, and S-containing compounds were detected in all four bacterial treatments. In vitro assays using pure VOCs revealed that hexanoic acid, 2-methylbutanoic acid, and phenylethyl alcohol are potential VOCs emitted by Bacillus spp. that are suppressive for MoT. The minimum inhibitory concentrations for MoT sporulation were 250 mM for phenylethyl alcohol and 500 mM for 2-methylbutanoic acid and hexanoic acid. Therefore, our results indicate that VOCs from Bacillus spp. are effective compounds to suppress the growth and sporulation of MoT. Understanding the MoT sporulation reduction mechanisms exerted by Bacillus VOCs may provide novel options to manage the further spread of wheat blast by spores.

[1]  Lauren S. Ryder,et al.  Genomic surveillance uncovers a pandemic clonal lineage of the wheat blast fungus , 2023, PLoS biology.

[2]  M. Z. Surovy,et al.  Role of seed infection for the near and far distance dissemination of wheat blast caused by Magnaporthe oryzae pathotype Triticum , 2023, Frontiers in Microbiology.

[3]  S. Rahman,et al.  Dormancy and germination of microsclerotia of Verticillium longisporum are regulated by soil bacteria and soil moisture levels but not by nutrients , 2022, Frontiers in Microbiology.

[4]  H. Burbano,et al.  Wild grass isolates of Magnaporthe (Syn. Pyricularia) spp. from Germany can cause blast disease on cereal crops , 2022, bioRxiv.

[5]  C. Kaur,et al.  Fumigation by bacterial volatile 2, 5-dimethylpyrazine enhances anthracnose resistance and shelf life of mango , 2022, European Journal of Plant Pathology.

[6]  Vantha Choub,et al.  Antifungal Activity of Volatile Organic Compounds from Bacillus velezensis CE 100 against Colletotrichum gloeosporioides , 2022, Horticulturae.

[7]  D. R. Gupta,et al.  Natural Protein Kinase Inhibitors, Staurosporine, and Chelerythrine Suppress Wheat Blast Disease Caused by Magnaporthe oryzae Triticum , 2022, Microorganisms.

[8]  D. R. Gupta,et al.  Marine Natural Product Antimycin A Suppresses Wheat Blast Disease Caused by Magnaporthe oryzae Triticum , 2022, Journal of fungi.

[9]  A. Venâncio,et al.  The Potential of Fatty Acids and Their Derivatives as Antifungal Agents: A Review , 2022, Toxins.

[10]  Jing Zhao,et al.  Mechanism of a Volatile Organic Compound (6-Methyl-2-Heptanone) Emitted From Bacillus subtilis ZD01 Against Alternaria solani in Potato , 2022, Frontiers in Microbiology.

[11]  L. Cruz‐López,et al.  Volatile Organic Compounds Produced by Cacao Endophytic Bacteria and Their Inhibitory Activity on Moniliophthora roreri , 2022, Current microbiology.

[12]  M. S. Malik,et al.  Biological control of fungal pathogens of tomato (Lycopersicon esculentum) by chitinolytic bacterial strains , 2021, Journal of basic microbiology.

[13]  A. Smolinska,et al.  Identification of Volatile Organic Compounds in Extremophilic Bacteria and Their Effective Use in Biocontrol of Postharvest Fungal Phytopathogens , 2021, Frontiers in Microbiology.

[14]  W. Shim,et al.  Streptomyces and Bacillus species utilize volatile organic compounds to impact Fusarium oxysporum f.sp. vasinfectum race 4 (Fov4) virulence and suppress Fusarium wilt in Pima cotton , 2021 .

[15]  V. P. Campos,et al.  The combination of two Bacillus strains suppresses Meloidogyne incognita and fungal pathogens, but does not enhance plant growth. , 2021, Pest management science.

[16]  A. Kundu,et al.  Rice leaf associated Chryseobacterium species: An untapped antagonistic flavobacterium displays volatile mediated suppression of rice blast disease , 2021 .

[17]  N. Hawkins,et al.  Fungicide resistance management: Maximizing the effective life of plant protection products , 2021, Plant Pathology.

[18]  S. Coughlan,et al.  Volatile Compounds From Bacillus, Serratia, and Pseudomonas Promote Growth and Alter the Transcriptional Landscape of Solanum tuberosum in a Passively Ventilated Growth System , 2021, Frontiers in Microbiology.

[19]  B. L. Manjunatha,et al.  Commercialization, Diffusion and Adoption of Bioformulations for Sustainable Disease Management in Indian Arid Agriculture: Prospects and Challenges , 2021, Circular Economy and Sustainability.

[20]  C. Ullah,et al.  Biological and biorational management of blast diseases in cereals caused by Magnaporthe oryzae , 2021, Critical reviews in biotechnology.

[21]  Rujikan Nasanit,et al.  Effects of temperature and relative humidity on Aflatoxin B1 reduction in corn grains and antagonistic activities against Aflatoxin-producing Aspergillus flavus by a volatile organic compound-producing yeast, Kwoniella heveanensis DMKU-CE82 , 2021, BioControl.

[22]  O. Rubilar,et al.  Current advances in plant-microbe communication via volatile organic compounds as an innovative strategy to improve plant growth. , 2021, Microbiological research.

[23]  J. Desaeger,et al.  Volatile compounds as potential bio-fumigants against plant-parasitic nematodes – a mini review , 2021, Journal of nematology.

[24]  D. Kelly,et al.  Widespread distribution of resistance to triazole fungicides in Brazilian populations of the wheat blast pathogen , 2020 .

[25]  Patrick Chiza Chikoti,et al.  Detection and characterization of fungus (Magnaporthe oryzae pathotype Triticum) causing wheat blast disease on rain-fed grown wheat (Triticum aestivum L.) in Zambia , 2020, PloS one.

[26]  Pallab Bhattacharjee,et al.  Suitable methods for isolation, culture, storage and identification of wheat blast fungus Magnaporthe oryzae Triticum pathotype , 2020 .

[27]  N. Sheoran,et al.  Antifungal and defense elicitor activities of pyrazines identified in endophytic Pseudomonas putida BP25 against fungal blast incited by Magnaporthe oryzae in rice , 2020, Journal of Plant Diseases and Protection.

[28]  N. Sheoran,et al.  Antifungal and defense elicitor activities of pyrazines identified in endophytic Pseudomonas putida BP25 against fungal blast incited by Magnaporthe oryzae in rice , 2020, Journal of Plant Diseases and Protection.

[29]  M. Kabir,et al.  Wheat blast: a new threat to food security , 2020, Phytopathology Research.

[30]  M. Perazzolli,et al.  Volatile Organic Compounds From Lysobacter capsici AZ78 as Potential Candidates for Biological Control of Soilborne Plant Pathogens , 2020, Frontiers in Microbiology.

[31]  Shuǐqìng Yú,et al.  Antifungal Effects of Volatiles Produced by Bacillus subtilis Against Alternaria solani in Potato , 2020, Frontiers in Microbiology.

[32]  Tofazzal Islam,et al.  Oligomycins inhibit Magnaporthe oryzae Triticum and suppress wheat blast disease , 2020, bioRxiv.

[33]  D. R. Gupta,et al.  Inhibitory Effects of Linear Lipopeptides From a Marine Bacillus subtilis on the Wheat Blast Fungus Magnaporthe oryzae Triticum , 2020, Frontiers in Microbiology.

[34]  J. Köhl,et al.  Mode of Action of Microbial Biological Control Agents Against Plant Diseases: Relevance Beyond Efficacy , 2019, Front. Plant Sci..

[35]  F. Loreto,et al.  Exploiting Plant Volatile Organic Compounds (VOCs) in Agriculture to Improve Sustainable Defense Strategies and Productivity of Crops , 2019, Front. Plant Sci..

[36]  Jaehyuk Choi,et al.  Wheat Blast in Bangladesh: The Current Situation and Future Impacts , 2019, The plant pathology journal.

[37]  G. Berg,et al.  Microbiota Associated with Sclerotia of Soilborne Fungal Pathogens – A Novel Source of Biocontrol Agents Producing Bioactive Volatiles , 2019, Phytobiomes Journal.

[38]  Ky Young Park,et al.  2,3-butanediol Induces Systemic Acquired Resistance in the Plant Immune Response , 2018, Journal of Plant Biology.

[39]  Ky Young Park,et al.  2,3-butanediol Induces Systemic Acquired Resistance in the Plant Immune Response , 2018, Journal of Plant Biology.

[40]  Liming Wu,et al.  Volatile Compounds of Endophytic Bacillus spp. have Biocontrol Activity Against Sclerotinia sclerotiorum. , 2018, Phytopathology.

[41]  B. McDonald,et al.  Wheat blast: from its origins in South America to its emergence as a global threat , 2018, Molecular plant pathology.

[42]  R. Borriss,et al.  Acetoin and 2,3-butanediol from Bacillus amyloliquefaciens induce stomatal closure in Arabidopsis thaliana and Nicotiana benthamiana , 2018, Journal of experimental botany.

[43]  P. Ceresini,et al.  Wheat Blast: Past, Present, and Future. , 2018, Annual review of phytopathology.

[44]  Liang Chen,et al.  A comprehensive understanding of the biocontrol potential of Bacillus velezensis LM2303 against Fusarium head blight , 2018, PloS one.

[45]  P. Garbeva,et al.  Microbial Volatiles: Small Molecules with an Important Role in Intra- and Inter-Kingdom Interactions , 2017, Front. Microbiol..

[46]  S. Doty,et al.  Bacterial Endophyte Colonization and Distribution within Plants , 2017, Microorganisms.

[47]  Jian-mei Che,et al.  Volatile organic compounds produced by Lysinibacillus sp. FJAT-4748 possess antifungal activity against Colletotrichum acutatum , 2017 .

[48]  N. Suwannarach,et al.  Applications of volatile compounds acquired from Muscodor heveae against white root rot disease in rubber trees (Hevea brasiliensis Müll. Arg.) and relevant allelopathy effects. , 2017, Fungal biology.

[49]  B. Valent,et al.  Wheat blast disease: danger on the move , 2017, Tropical Plant Pathology.

[50]  S. F. Pascholati,et al.  Potential of fumigation of orange fruits with volatile organic compounds produced by Saccharomyces cerevisiae to control citrus black spot disease at postharvest , 2017 .

[51]  N. Talbot,et al.  Emergence of wheat blast in Bangladesh was caused by a South American lineage of Magnaporthe oryzae , 2016, BMC Biology.

[52]  Shusheng Zhu,et al.  Tobacco Rotated with Rapeseed for Soil-Borne Phytophthora Pathogen Biocontrol: Mediated by Rapeseed Root Exudates , 2016, Front. Microbiol..

[53]  W. Raza,et al.  Effect of organic fertilizers prepared from organic waste materials on the production of antibacterial volatile organic compounds by two biocontrol Bacillus amyloliquefaciens strains. , 2016, Journal of biotechnology.

[54]  K. S. Subramanian,et al.  Bacterial antagonists and hexanal-induced systemic resistance of mango fruits against Lasiodiplodia theobromae causing stem-end rot , 2016 .

[55]  B. McDonald,et al.  Resistance to QoI Fungicides Is Widespread in Brazilian Populations of the Wheat Blast Pathogen Magnaporthe oryzae. , 2015, Phytopathology.

[56]  Pu Liu,et al.  Mechanisms of action for 2-phenylethanol isolated from Kloeckera apiculata in control of Penicillium molds of citrus fruits , 2014, BMC Microbiology.

[57]  A. Café-Filho,et al.  Management of wheat blast with synthetic fungicides, partial resistance and silicate and phosphite minerals , 2014, Phytoparasitica.

[58]  E. Pérez-Rueda,et al.  Identification of volatile compounds produced by the bacterium Burkholderia tropica that inhibit the growth of fungal pathogens , 2013, Bioengineered.

[59]  D. Jiāng,et al.  Evaluation of Sporidiobolus pararoseus strain YCXT3 as biocontrol agent of Botrytis cinerea on post-harvest strawberry fruits , 2012 .

[60]  W. Raza,et al.  Antifungal Activity of Bacillus amyloliquefaciens NJN-6 Volatile Compounds against Fusarium oxysporum f. sp. cubense , 2012, Applied and Environmental Microbiology.

[61]  M. Maffei,et al.  Fusarium oxysporum and its bacterial consortium promote lettuce growth and expansin A5 gene expression through microbial volatile organic compound (MVOC) emission. , 2011, FEMS microbiology ecology.

[62]  V. Flors,et al.  Hexanoic acid-induced resistance against Botrytis cinerea in tomato plants. , 2009, Molecular plant-microbe interactions : MPMI.

[63]  H. Thormar,et al.  In Vitro Killing of Candida albicans by Fatty Acids and Monoglycerides , 2001, Antimicrobial Agents and Chemotherapy.

[64]  M. Chadeganipour,et al.  Antifungal activities of pelargonic and capric acid on Microsporum gypseum , 2001, Mycoses.

[65]  I. Chet,et al.  Biological control of fungal pathogens , 1994, Applied biochemistry and biotechnology.

[66]  Bacilli in Agrobiotechnology: Plant Stress Tolerance, Bioremediation, and Bioprospecting , 2022, Bacilli in Climate Resilient Agriculture and Bioprospecting.

[67]  Zerihun T. Dame,et al.  Discovery of Bioactive Natural Products from Bacillus Species: Chemistry, Biosynthesis and Biological Activities , 2022, Bacilli in Climate Resilient Agriculture and Bioprospecting.

[68]  S. Kamoun,et al.  Genomic analyses reveal that biocontrol of wheat blast by Bacillus spp. may be linked with production of antimicrobial compounds and induced systemic resistance in host plants , 2018 .

[69]  S. Kamoun,et al.  Plant probiotic bacteria suppress wheat blast fungus Magnaporthe oryzae Triticum pathotype , 2017 .

[70]  A. Kundu,et al.  Genotyping and identification of broad spectrum antimicrobial volatiles in black pepper root endophytic biocontrol agent, Bacillus megaterium BP17 , 2016 .

[71]  Ye Wang,et al.  Lipopeptides, a novel protein, and volatile compounds contribute to the antifungal activity of the biocontrol agent Bacillus atrophaeus CAB-1 , 2013, Applied Microbiology and Biotechnology.

[72]  L. Eberl,et al.  Production of Bioactive Volatiles by Different Burkholderia ambifaria Strains , 2013, Journal of Chemical Ecology.

[73]  A. Foroutan EVALUATION OF TRICHODERMA ISOLATES FOR BIOLOGICAL CONTROL OF WHEAT FUSARIUM FOOT AND ROOT ROT , 2013 .

[74]  M. Mazzola,et al.  Diversity and natural functions of antibiotics produced by beneficial and plant pathogenic bacteria. , 2012, Annual review of phytopathology.

[75]  Joseph M. Awika,et al.  Major Cereal Grains Production and Use around the World , 2011 .

[76]  L. Azeez,et al.  Available Online at www , 2010 .

[77]  K. K. Pal,et al.  Biological Control of Plant Pathogens , 2006 .