Abstract
Globally, phytopathogenic fungi infections cause crop diseases, resulting in crop yield and quality loss. Extensive use of chemical fungicides leads to resistance and high costs for growers as well as environmental pollution; thus, researchers are exploring a more sustainable approach using biological control tactics. This review highlights the critical processes involved in biological control by bacteria, fungi, viruses, and archaea, i.e., the synthesis of various metabolites, enzymes, and signaling molecules, as well as competitive tactics or soil suppressiveness that can effectively control the phytopathogenic fungi. The global increase in registrations for biological products reflects the rising demand and requirement for more organic agriculture and achieving some sustainable development targets. Understanding the complicated interplay between microorganisms in this environment can aid in managing soil diversity and inhibiting phytopathogenic fungi without chemical residues. Therefore, microorganisms are recommended as a sustainable alternative biological control.
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Abbreviations
- FAO:
-
Food and Agriculture Organization of the United Nations
- DMDS:
-
dimethyl disulfide
- VOCs:
-
volatile organic compounds
- DMHDA:
-
dimethyl hexadecylamine
- PGPB:
-
plant growth–promoting bacteria
- PGPR:
-
plant growth-promoting rhizobacteria
- NRPS:
-
non-ribosomal peptide synthetases
- PKS:
-
polyketide synthetases
- SAR:
-
systemic acquired resistance
- ISR:
-
induced systemic resistance
- JA:
-
jasmonic acid
- SA:
-
salicylic acid
- ET:
-
ethylene
- PR1, 2:
-
pathogenesis-related gene
- Chit-1:
-
the plant defensive chitinase
- Glu-2:
-
1,3-glucanase
- dsRNA:
-
Double-stranded RNA
- CHV:
-
Cryphonectria hypovirulence viruses
- SsNSRV-1:
-
S. sclerotiorum negative-stranded RNA virus 1
- SsHV2:
-
S. sclerotiorum hypovirus 2
- SsPV1:
-
S. sclerotiorum partitivirus 1
References
Abdelkhalik A, El-Mageed A, Taia A, Mohamed IA, Semida WM, Al-Elwany OA, AbuQamar SF, El-Tarabily KA, Gyushi MA (2023) Soil application of effective microorganisms and nitrogen alleviates salt stress in hot pepper (Capsicum annum L.) plants. Front Plant Sci 13:1079260. https://doi.org/10.3389/fpls.2022.1079260
Adebayo C, Aderiye B (2010) Antifungal activity of bacteriocins of lactic acid bacteria from some Nigerian fermented foods. Res J Microbiol 5(11):1070–1082. https://doi.org/10.3923/jm.2010.1070.1082
Ahluwalia V, Kumar J, Rana VS, Sati OP, Walia S (2015) Comparative evaluation of two Trichoderma harzianum strains for major secondary metabolite production and antifungal activity. Nat Prod Res 29(10):914–920. https://doi.org/10.1080/14786419.2014.958739
Ahmed IH, Ali EF, Gad AA, Bardisi A, El-Tahan AM, Abd Esadek OA, El-Saadony MT, Gendy AS (2022) Impact of plant growth regulators spray on fruit quantity and quality of pepper (Capsicum annuum L.) cultivars grown under plastic tunnels. Saudi J Biol Sci 29(4):2291–2298. https://doi.org/10.1016/j.sjbs.2021.11.062
Alblooshi AA, Purayil GP, Saeed EE, Ramadan GA, Tariq S, Altaee AS, El-Tarabily KA, AbuQamar SF (2022) Biocontrol potential of endophytic actinobacteria against Fusarium solani, the causal agent of sudden decline syndrome on date palm in the UAE. J Fungi 8(1):8. https://doi.org/10.3390/jof8010008
Al Hamad BM, AlRaish SM, Ramadan GA, Alameri SSA, Al Senaani SS, AbuQamar SF, El-Tarabily KA (2021) Effectiveness of augmentative biological control of Streptomyces griseorubens UAE2 depends on 1-Aminocyclopropane-1-carboxylic acid deaminase activity against Neoscytalidium Dimidiatum. J Fungi 7(11):885. https://doi.org/10.3390/jof7110885
Alijani Z, Amini J, Ashengroph M, Bahramnejad B (2019) Antifungal activity of volatile compounds produced by Staphylococcus sciuri strain MarR44 and its potential for the biocontrol of Colletotrichum nymphaeae, causal agent strawberry anthracnose. Int J Food Microbiol 307:108276. https://doi.org/10.1016/j.ijfoodmicro.2019.108276
Ali S, Hameed S, Shahid M, Iqbal M, Lazarovits G, Imran A (2020) Functional characterization of potential PGPR exhibiting broad-spectrum antifungal activity. Microbiol Res 232:126389. https://doi.org/10.1016/j.micres.2019.126389
Al Raish SM, Saeed EE, Alyafei DM, El-Tarabily KA, AbuQamar SF (2021) Evaluation of Streptomycete Actinobacterial isolates as biocontrol agents against royal poinciana stem canker Disease caused by the fungal pathogen Neoscytalidium Dimidiatum. Biol Control 164:104783. https://doi.org/10.1016/j.biocontrol.2021.104783
Alwahshi KJ, Purayil GP, Saeed EE, Abufarajallah HA, Aldhaheri SJ, AbuQamar SF, El-Tarabily KA (2022) The 1-aminocyclopropane-1-carboxylic acid deaminase-producing Streptomyces violaceoruber UAE1 can provide protection from sudden decline syndrome on date palm. Front Plant Sci 13:904166. https://doi.org/10.3389/fpls.2022.904166
Anagnostakis SL (1982) Biological control of chestnut blight. Science 215:466–471
Anderson LM, Stockwell VO, Loper JE (2004) An extracellular protease of Pseudomonas fluorescens inactivates antibiotics of Pantoea agglomerans. Phytopathol 94:1228–1234. https://doi.org/10.1094/PHYTO.2004.94.11.1228
Ashry NM, Alaidaroos BA, Mohamed SA, Badr OA, El-Saadony MT, Esmael A (2022) Utilization of drought-tolerant bacterial strains isolated from harsh soils as a plant growth-promoting rhizobacteria (PGPR). Saudi J Biol Sci 29(3):1760–1769. https://doi.org/10.1016/j.sjbs.2021.10.054
Badalyan SM (2001) Higher basidiomycetes as prospective objects for mycopharmacological research. Int J Med Mushrooms 3(2–3):108. https://doi.org/10.1615/IntJMedMushr.v3.i2-3.270
Beris D, Theologidis I, Skandalis N, Vassilakos N (2018) Bacillus amyloliquefaciens strain MBI600 induces salicylic acid dependent resistance in tomato plants against tomato spotted wilt virus and potato virus Y. Sci Rep 8(1):10320. https://doi.org/10.1038/s41598-018-28677-3
Bertuzzi T, Leni G, Bulla G, Giorni P (2022) Reduction of mycotoxigenic fungi growth and their mycotoxin production by Bacillus subtilis QST 713. Toxins 14(11):797. https://doi.org/10.3390/toxins14110797
Bhat MA, Mishra AK, Jan S, Bhat MA, Kamal MA, Rahman S, Shah AA, Jan AT (2023) Plant growth promoting rhizobacteria in plant health: a perspective study of the underground interaction. Plants 12(3):629. https://doi.org/10.3390/plants12030629
Biraghi A (1953) Possible active resistance to Endothia Parasitica in Castanea crenata. Congress International Union Forest Research Organization, pp 149–157
Bird F, Elgee D (1957) A virus Disease and introduced parasites as factors controlling the European spruce sawfly, Diprion hercyniae (htg.), in Central New Brunswick1. Can Entomol 89:371–378
Black BC, Brennan LA, Dierks PM, Gard IE (1997) Commercialization of baculoviral insecticides. The baculoviruses. Springer US, Boston, MA, pp 341–387
Bonaterra A, Badosa E, Daranas N, Francés J, Roselló G, Montesinos E (2022) Bacteria as biological control agents of plant diseases. Microorganisms10(9): 1759. https://doi.org/10.3390/microorganisms10091759
Brasier CM (2001) Rapid evolution of introduced plant pathogens via interspecific hybridization: hybridization is leading to rapid evolution of Dutch elm Disease and other fungal plant pathogens. Biosci 51(2):123–133. https://doi.org/10.1641/0006-3568(2001)051[0123:REOIPP]2.0.CO;2
Brauer VS, Rezende CP, Pessoni AM, De Paula RG, Rangappa KS, Nayaka SC, Gupta VK, Almeida F (2019) Antifungal agents in agriculture: friends and foes of public health. Biomolecules 9(10):521. https://doi.org/10.3390/biom9100521
Bungtongdee N, Sopalun K, Laosripaiboon W, Iamtham S (2019) The chemical composition, antifungal, antioxidant and antimutagenicity properties of bioactive compounds from fungal endophytes associated with Thai orchids. J Phytopathol 167:56–64. https://doi.org/10.1111/jph.12773
Calderone RA, Fonzi WA (2001) Virulence factors of Candida albicans. Trends Microbiol 9:327–335. https://doi.org/10.1016/s0966-842x(01)02094-7
Cascales E, Buchanan SK, Duché D, Kleanthous C, Lloubes R, Postle K, Riley M, Slatin S, Cavard D (2007) Colicin biology. Microbiol Mol Biol Rev 71:158–229. https://doi.org/10.1128/mmbr.00036-06
Chelius M, Triplett E (2001) The diversity of archaea and bacteria in association with the roots of Zea mays L. Microb Ecol 41(3):252–263. https://doi.org/10.1007/s002480000087
Chen B, Nuss DL (1999) Infectious cDNA clone of hypovirus CHV1-Euro7: a comparative virology approach to investigate virus-mediated hypovirulence of the chestnut blight fungus Cryphonectria parasitica. J Virol 73(2):985–992. https://doi.org/10.1128/JVI.73.2.985-992.1999
Chen JH, Xiang W, Cao KX, Lu X, Yao SC, Hung D, Huang RS, Li LB (2020) Characterization of volatile organic compounds emitted from endophytic Burkholderia cenocepacia ETR-B22 by SPME-GC-MS and their inhibitory activity against various plant fungal pathogens. Molecules 25(17):3765. https://doi.org/10.3390/molecules25173765
Conrad AM (2022) Management of Sclerotinia sclerotiorum in soybean using the biofungicides Bacillus amyloliquefaciens and Coniothyrium minitans. Purdue University, Thesis
Conrad AM, Telenko DE (2023) Efficacy of biocontrol agents Coniothyrium minitans and Bacillus amyloliquefaciens for managing Sclerotinia sclerotiorum in Indiana soybean. PhytoFrontiers 3:1–29. https://doi.org/10.1094/PHYTOFR-07-22-0080-R
Daranas N, Roselló G, Cabrefiga J, Donati I, Francés J, Badosa E, Spinelli F, Montesinos E, Bonaterra A (2019) Biological control of bacterial plant Diseases with Lactobacillus plantarum strains selected for their broad-spectrum activity. Ann Appl Biol 174(1):92–105. https://doi.org/10.1111/aab.12476
da Silva Ribeiro A, Polonio JC, Costa AT, Dos Santos CM, Rhoden SA, Azevedo JL, Pamphile JA (2018) Bioprospection of culturable endophytic fungi associated with the ornamental plant Pachystachys lutea. Curr Opin Microbiol 75:588–596. https://doi.org/10.1007/s00284-017-1421-9
Day P (1977) Double-stranded RNA in Endothia parasitica PR Day, JA Dodds, JE Elliston, R. A. Jaynes, and S. L. Anagnostakis Authors two and three, Department of Plant Pathology; and authors one, four, and five, Department of Genetics; all at The Connecticut Agricultural Experiment Station, New Haven, CT 06504
Díaz-Díaz M, Bernal-Cabrera A, Trapero A, Medina-Marrero R, Sifontes-Rodríguez S, Cupull-Santana RD, Cupull-Santana RD, García-Bernal M, Agustí-Brisach C (2022) Characterization of actinobacterial strains as potential biocontrol agents against Macrophomina Phaseolina and rhizoctonia solani, the main soilborne pathogens of Phaseolus vulgaris in Cuba. Plants 11(5):645. https://doi.org/10.3390/plants11050645
Díaz-Gutiérrez C, Arroyave C, Llugany M, Poschenrieder C, Martos S, Peláez C (2021) Trichoderma Asperellum as a preventive and curative agent to control Fusarium wilt in Stevia rebaudiana. Biol Control 155:104537. https://doi.org/10.1016/j.biocontrol.2021.104537
de Almeida TT, Ribeiro MAS, Polonio JC, Garcia FP, Nakamura CV, Meurer EC, Sarragiotto MH, Baldoqui DC, Azevedo JL, Pamphile JA (2018) Curvulin and spirostaphylotrichins R and U from extracts produced by two endophytic Bipolaris sp. associated to aquatic macrophytes with antileishmanial activity. Nat Prod Res 32:2783–2790. https://doi.org/10.1080/14786419.2017.1380011
de Andrade LA, Santos CHB, Frezarin ET, Sales LR, Rigobelo EC (2023) Plant growth-promoting rhizobacteria for sustainable agricultural production. Microorganisms 11(4):1088. https://doi.org/10.3390/microorganisms11041088
Desoky ESM, Rady MM, Nader MM, Mostafa NG, Elrys AS, Mathai A, AbuQamar SF, El-Tarabily KA, El-Saadony MT (2022) Integrated application of bacterial carbonate precipitation and silicon nanoparticles enhances productivity, physiological attributes, and antioxidant defenses of wheat (Triticum aestivum L.) under semi-arid conditions. Front Plant Sci 13:947949. https://doi.org/10.3389/fpls.2022.947949
Desoky ESM, Saad AM, El-Saadony MT, Merwad ARM, Rady MM (2020) Plant growth-promoting rhizobacteria: potential improvement in antioxidant defense system and suppression of oxidative stress for alleviating salinity stress in Triticum aestivum (L.) plants. Biocatal Agric Biotechnol 30:101878.https://doi.org/10.1016/j.bcab.2020.101878
De Vrieze M, Varadarajan AR, Schneeberger K, Bailly A, Rohr RP, Ahrens CH, Weisskopf L (2020) Linking comparative genomics of nine potato-associated Pseudomonas isolates with their differing biocontrol potential against late blight. Front Microbiol 11:857. https://doi.org/10.3389/fmicb.2020.00857
Duffy B, Weller D (1996) Biological control of take-all of wheat in the pacific northwest of the Usa using hypovirulent Gaeumannomyces Graminis var. Tritici and fluorescent pseudomonads. J Phytopathol 144:585–590. https://doi.org/10.1111/j.1439-0434.1996.tb00303.x
Duong B, Nguyen HX, Phan HV, Colella S, Trinh PQ, Hoang GT, Nguyen TT, Marraccini P, Lebrun M, Duponnois R (2021) Identification and characterization of Vietnamese coffee bacterial endophytes displaying in vitro antifungal and nematicidal activities. Microbiol Res 242:126613. https://doi.org/10.1016/j.micres.2020.126613
Eberl L, Vandamme P (2016) Members of the genus Burkholderia: good and bad guys. F1000Res 5:1–10. https://doi.org/10.12688/f1000research.8221.1
El-Mageed A, Taia A, Gyushi MA, Hemida KA, El-Saadony MT, El-Mageed A, AbuQamar SF, El-Tarabily KA, Abdelkhalik A (2022) Coapplication of effective microorganisms and nanomagnesium boosts the agronomic, physio-biochemical, osmolytes, and antioxidants defenses against salt stress in Ipomoea batatas. Front Plant Sci 13:883274. https://doi.org/10.3389/fpls.2022.883274
El-Maraghy SS, Tohamy TA, Hussein KA (2020) Role of plant-growth promoting fungi (PGPF) in defensive genes expression of Triticum aestivum against wilt Disease. Rhizosphere 15:100223. https://doi.org/10.1016/j.rhisph.2020.100223
Elnahal AS, El-Saadony MT, Saad AM, Desoky ESM, El-Tahan AM, Rady MM, AbuQamar SF, El-Tarabily KA (2022) The use of microbial inoculants for biological control, plant growth promotion, and sustainable agriculture: a review. Eur J Plant Pathol 162(4):759–792. https://doi.org/10.1007/s10658-021-02393-7
El-Saadony MT, Saad AM, Najjar AA, Alzahrani SO, Alkhatib FM, Shafi ME, Fouda SEE, El-Tahan AM, Hassan MA (2021) The use of biological selenium nanoparticles to suppress Triticum aestivum L. crown and root rot Diseases induced by Fusarium species and improve yield under drought and heat stress. Saudi J Biol Sci 28(8):4461–4471. https://doi.org/10.1016/j.sjbs.2021.04.043
El-Saadony MT, Saad AM, Soliman SM, Salem HM, Ahmed AI, Mahmood M, Babalghith AO, Elrys AS, El-Tarabily KA, AbuQamar SF (2022) Plant growth-promoting microorganisms as biocontrol agents of plant Diseases: mechanisms, challenges and future perspectives. Front Plant Sci 13:923880. https://doi.org/10.3389/fpls.2022.923880
Elsayed SS, Sehsah MD, Oueslati MA, Ibrahim OM, Hamden S, Seddek NH, AbdElgawad H, El-Saadony MT, El-Tahan AM (2023) The effect of using fresh farmyard manure (animal manure) on the severity of Fusarium verticilioides in soil, root, stem, and kernels as well as lodging and borer incidence of maize plants. Front Plant Sci 13:998440. https://doi.org/10.3389/fpls.2022.998440
El-Tarabily KA (2003) An endophytic chitinase-producing isolate of Actinoplanes missouriensis, with potential for biological control of root rot of lupin caused by Plectosporium tabacinum. Aust J Bot 51:257–266. https://doi.org/10.1071/BT02107
El-Tarabily KA, Hardy GE, St J, Sivasithamparam K (2010) Performance of three endophytic actinomycetes in relation to plant growth promotion and biological control of Pythium aphanidermatum, a pathogen of cucumber under commercial field production conditions in the United Arab Emirates. Eur J Plant Pathol 128:527–539. https://doi.org/10.1007/s10658-010-9689-7
El-Tarabily KA, Hardy GE, St J, Sivasithamparam K, Hussein AM, Kurtböke DI (1997) The potential for the biological control of cavity spot Disease of carrots caused by Pythium coloratum by Streptomycete and non-streptomycete actinomycetes in Western Australia. New Phytol 137:495–507. https://doi.org/10.1046/j.1469-8137.1997.00856.x
El-Tarabily KA, Nassar AH, Hardy GE, St J, Sivasithamparam K (2009) Plant growth promotion and biological control of Pythium aphanidermatum, a pathogen of cucumber, by endophytic actinomycetes. J Appl Microbiol 106:13–26. https://doi.org/10.1111/j.1365-2672.2008.03926.x
El-Tarabily KA, Sivasithamparam K (2006) Non-streptomycete actinomycetes as biocontrol agents of soil-borne fungal plant pathogens and as plant growth promoters. Soil Biol Biochem 38:1505–1520. https://doi.org/10.1016/j.soilbio.2005.12.017
El-Tarabily KA, Sykes ML, Kurtböke DI, Hardy GE, St J, Barbosa AM, Dekker RFH (1996) Synergistic effects of a cellulase-producing Micromonospora carbonacea and an antibiotic-producing Streptomyces violascens on the suppression of Phytophthora cinnamomi root-rot of Banksia Grandis. Canad J Bot 74:618–624. https://doi.org/10.1139/b96-078
Figueroa M, Ortiz D, Henningsen EC (2021) Tactics of host manipulation by intracellular effectors from plant pathogenic fungi. Curr Opin Plant Biol 62:102054. https://doi.org/10.1016/j.pbi.2021.102054
Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186–194. https://doi.org/10.1038/nature10947
Gao Z, Zhang B, Liu H, Han J, Zhang Y (2017) Identification of endophytic Bacillus velezensis ZSY-1 strain and antifungal activity of its volatile compounds against Alternaria solani and Botrytis Cinerea. Biol Control 105:27–39. https://doi.org/10.1016/j.biocontrol.2016.11.007
García-Pedrajas M, Cañizares M, Sarmiento-Villamil JL, Jacquat AG, Dambolena JS (2019) Mycoviruses in biological control: from basic research to field implementation. Phytopathology 109:1828–1839. https://doi.org/10.1094/PHYTO-05-19-0166-RVW
Ghabrial SA, Castón JR, Jiang D, Nibert ML, Suzuki N (2015) 50-plus years of fungal viruses. Virology 479:356–368. https://doi.org/10.1016/j.virol.2015.02.034
Ghabrial SA, Suzuki N (2009) Viruses of plant pathogenic fungi. Annu Rev Phytopathol 47:353–384. https://doi.org/10.1146/annurev-phyto-080508-081932
Gómez-Godínez LJ, Aguirre-Noyola JL, Martínez-Romero E, Arteaga-Garibay RI, Ireta-Moreno J, Ruvalcaba-Gómez JM (2023) A look at plant-growth-promoting bacteria. Plants 12(8):1668. https://doi.org/10.3390/plants12081668
Goswami D, Thakker JN, Dhandhukia PC (2016) Portraying mechanics of plant growth promoting rhizobacteria (PGPR): a review. Cogent Food Agric 2(1):1127500. https://doi.org/10.1080/23311932.2015.1127500
Grützmacher DD, Grützmacher AD, Agostinetto D, Loeck AE, Roman R, Peixoto SC, Zanella R (2008) Monitoramento De agrotóxicos em dois mananciais hídricos no Sul do Brasil. Rev Bras Eng Agríc Ambient 12:632–637. https://doi.org/10.1590/S1415-43662008000600010
Haas D, Défago G (2005) Biological control of soilborne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3(4):307–319. https://doi.org/10.1038/nrmicro1129
Haase S, Sciocco-Cap A, Romanowski V (2015) Baculovirus insecticides in Latin America: historical overview, current status and future perspectives. Viruses 7(5):2230–2267. https://doi.org/10.3390/v7052230
Hallmann J, Quadt-Hallmann A, Rodrıguez-Kabana R, Kloepper J (1998) Interactions between Meloidogyne incognita and endophytic bacteria in cotton and cucumber. Soil Biol Biochem 30(7):925–937. https://doi.org/10.1016/S0038-0717(97)00183-1
Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2(1):43–56. https://doi.org/10.1038/nrmicro797
Hassan MA, El-Saadony MT, Mostafa NG, El-Tahan AM, Mesiha PK, El-Saadony FM, Hassan AM, El-Shehawi AM, Ashry NM (2021) The use of previous crops as sustainable and eco-friendly management to fight Fusarium oxysporum in sesame plants. Saudi J Biol Sci 28(10):5849–5859. https://doi.org/10.1016/j.sjbs.2021.06.041
Hazarika DJ, Goswami G, Gautom T, Parveen A, Das P, Barooah M, Boro RC (2019) Lipopeptide mediated biocontrol activity of endophytic Bacillus subtilis against fungal phytopathogens. BMC Microbiol 2(1):71. https://doi.org/10.1186/s12866-019-1440-8
Heiniger U, Rigling D (1994) Biological control of chestnut blight in Europe. Annu Rev Phytopathol 32:581–599. https://doi.org/10.1146/annurev.py.32.090194.003053
Heng NC, Wescombe PA, Burton JP, Jack RW, Tagg JR (2007) The diversity of bacteriocins in Gram-positive bacteria. Bacteriocins: ecology and evolution. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 45–92
Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiol 158(Pt 1):17–25. https://doi.org/10.1099/mic.0.052274-0
Heydari A, Pessarakli M (2010) A review on biological control of fungal plant pathogens using microbial antagonists. J Biol Sci 10(4):273–290. https://doi.org/10.3923/jbs.2010.273.290
Hillman BI, Annisa A, Suzuki N (2018) Viruses of plant-interacting fungi. Adv Virus Res 100:99–116. https://doi.org/10.1146/annurev-phyto-080508-081932
Huang CJ, Tsay JF, Chang SY, Yang HP, Wu WS, Chen CY (2012) Dimethyl disulfide is an induced systemic resistance elicitor produced by Bacillus cereus C1L. Pest Manag Sci 68:1306–1310. https://doi.org/10.1002/ps.3301
Hussain T, Khan AA, Mohamed HI (2022) Potential efficacy of biofilm-forming biosurfactant Bacillus firmus HussainT-Lab. 66 against Rhizoctonia solani and mass spectrometry analysis of its metabolites. Int J Pept Res Ther 38(2):90–101. https://doi.org/10.5423/PPJ.OA.11.2021.0173
Hutchings MI, Truman AW, Wilkinson B (2019) Antibiotics: past, present and future. Curr Opin Microbiol 51:72–80. https://doi.org/10.1016/j.mib.2019.10.008
Jain A, Sarsaiya S, Wu Q, Lu Y, Shi J (2019) A review of plant leaf fungal Diseases and its environment speciation. Bioengineered 10:409–424. https://doi.org/10.1080/21655979.2019.1649520
Jantasorn A, Moungsrimuangdee B, Dethoup T (2016) In vitro antifungal activity evaluation of five plant extracts against five plant pathogenic fungi causing rice and economic crop Diseases. J Biopestic 9(1):1–7. https://doi.org/10.57182/jbiopestic.9.1.01-07
Jatoi GH, Lihua G, Xiufen Y, Gadhi MA, Keerio AU, Abdulle YA, Qiu D (2019) A novel protein elicitor PeBL2, from Brevibacillus laterosporus A60, induces systemic resistance against Botrytis Cinerea in Tobacco plant. Plant Pathol J 35(3):208–218. https://doi.org/10.5423/PPJ.OA.11.2018.0276
Kaddes A, Fauconnier ML, Sassi K, Nasraoui B, Jijakli MH (2019) Endophytic fungal volatile compounds as solution for sustainable agriculture. Molecules 24(6):1065. https://doi.org/10.3390/molecules24061065
Kamil FH, Saeed EE, El-Tarabily KA, AbuQamar SF (2018) Biological control of mango dieback Disease caused by Lasiodiplodia theobromae using Streptomycete and non-streptomycete actinobacteria in the United Arab Emirates. Front Microbiol 9:829. https://doi.org/10.3389/fmicb.2018.00829
Kanchiswamy CN, Malnoy M, Maffei ME (2015) Chemical diversity of microbial volatiles and their potential for plant growth and productivity. Front. Plant Sci 6:151. https://doi.org/10.3389/fpls.2015.00151
Katz L, Baltz RH (2016) Natural product discovery: past, present, and future. J Ind Microbiol Biotechnol 43(2–3):155–176. https://doi.org/10.1007/s10295-015-1723-5
Khan RAA, Najeeb S, Hussain S, Xie B, Li Y (2020) Bioactive secondary metabolites from Trichoderma spp. against phytopathogenic fungi. Microorganisms 8(6):817. https://doi.org/10.3390/microorganisms8060817
Khatri DK, Tiwari DN, Bariya HS (2017) Chitinolytic efficacy and secretion of cell wall degrading enzymes from Trichoderma spp. in response to phyto-pathological fungi. J Appl Biol Biotechnol 5(6):1–8. https://doi.org/10.7324/JABB.2017.50601
Köhl J, Booij K, Kolnaar R, Ravensberg WJ (2019) Ecological arguments to reconsider data requirements regarding the environmental fate of microbial biocontrol agents in the registration procedure in the European Union. Biocontrol 64:469–487. https://doi.org/10.1007/s10526-019-09964-y
Khunnamwong P, Lertwattanasakul N, Jindamorakot S, Suwannarach N, Matsui K, Limtong S (2020) Evaluation of antagonistic activity and mechanisms of endophytic yeasts against pathogenic fungi causing economic crop Diseases. Folia Microbiol 65:573–590. https://doi.org/10.1007/s12223-019-00764-6
Kong WL, Li PS, Wu XQ, Wu TY, Sun XR (2020) Forest tree associated bacterial diffusible and volatile organic compounds against various phytopathogenic fungi. Microorganisms 8(4):590. https://doi.org/10.3390/microorganisms8040590
Kumari S, Khanna V (2020) Induction of systemic resistance in chickpea (Cicer arietinum L.) against Fusarium oxysporum f. sp. ciceris by antagonistic rhizobacteria in assistance with native mesorhizobium. Curr Microbiol 77:85–98. https://doi.org/10.1007/s00284-019-01805-6
Kumar V, Tiwari SK (2017) Halocin HA1: an archaeocin produced by the haloarchaeon Haloferax larsenii HA1. Process Biochem 61:202–208. https://doi.org/10.1016/j.procbio.2017.06.010
Lamichhane J, Dachbrodt-Saaydeh S, Kudsk P, Messéan A (2016) Conventional pesticides in agriculture: benefits versus risks. Plant Dis 100:10–24. https://doi.org/10.1094/PDIS-05-15-0574-FE
Legein M, Smets W, Vandenheuvel D, Eilers T, Muyshondt B, Prinsen E, Prinsen E, Samson R, Lebeer S (2020) Modes of action of microbial biocontrol in the phyllosphere. Front Microbiol 11:1619. https://doi.org/10.3389/fmicb.2020.01619
Liu L, Xie J, Cheng J, Fu Y, Li G, Yi X, Jiang D (2014) Fungal negative-stranded RNA virus that is related to bornaviruses and nyaviruses. Proc Natl Acad Sci 111:12205–12210. https://doi.org/10.1073/pnas.1401786111
Liu Y, Teng K, Wang T, Dong E, Zhang M, Tao Y, Zhong J (2020) Antimicrobial Bacillus velezensis HC6: production of three kinds of lipopeptides and biocontrol potential in maize. J Appl Microbiol 128(1):242–254. https://doi.org/10.1111/jam.14459
Li X, Garbeva P, Liu X klein Gunnewiek. PJA, Clocchiatti A, Hundscheid MPJ, Wang X, Boer W (2020) 1, 1025–1035
Lopes R, Tsui S, Gonçalves PJ, de Queiroz MV (2018) A look into a multifunctional toolbox: endophytic Bacillus species provide broad and underexploited benefits for plants. World J Microbiol Biotechnol 34:1–10. https://doi.org/10.1007/s11274-018-2479-7
Lund ME, Mourtzinis S, Conley SP, Ané JM (2018) Soybean cyst nematode control with Pasteuria nishizawae under different management practices. Agron J 110:2534–2540. https://doi.org/10.2134/agronj2018.05.0314
Lutfia A, Munir E, Yurnaliza Y (2020) Molecular identification of endophytic fungi from torch ginger (Etlingera elatior) antagonist to phytopathogenic fungi. Biodivers J Biol Diver 21(6):2681–2689. https://doi.org/10.13057/biodiv/d210641
Maindad D, Kasture V, Chaudhari H, Dhavale D, Chopade B, Sachdev D (2014) Characterization and fungal inhibition activity of siderophore from wheat rhizosphere associated Acinetobacter calcoaceticus strain HIRFA32. Indian J Med Microbiol 54(3):315–322. https://doi.org/10.1007/s12088-014-0446-z
Ma LJ, Geiser DM, Proctor RH, Rooney AP, O’Donnell K, Trail F, Gardiner DM, Manners JM, Kazan K (2013) Fusarium pathogenomics. Annu Rev Microbiol 67:399–416. https://doi.org/10.1146/annurev-micro-092412-155650
Marzano SYL, Domier LL (2016) Novel mycoviruses discovered from metatranscriptomics survey of soybean phyllosphere phytobiomes. Virus Res 213:332–342. https://doi.org/10.1016/j.virusres.2015.11.002
Marzano SYL, Hobbs HA, Nelson BD, Hartman GL, Eastburn DM, McCoppin NK, Domier LL (2015) Transfection of Sclerotinia sclerotiorum with in vitro transcripts of a naturally occurring interspecific recombinant of Sclerotinia Sclerotiorum hypovirus 2 significantly reduces virulence of the fungus. J Virol 89:5060–5071. https://doi.org/10.1128/JVI.03199-14
Mazguene S, Rossi M, Gogliettino M, Palmieri G, Cocca E, Mirino S, Imadalou-Idres N, Benallaoua S (2018) Isolation and characterization from solar salterns of North Algeria of a haloarchaeon producing a new halocin. Extremophiles 22(2):259–270. https://doi.org/10.1007/s00792-017-0994-3
Mckenna F, El-Tarabily KA, Hardy GE, St J, Dell B (2001) Novel in vivo use of a polyvalent Streptomyces phage to disinfest Streptomyces scabies infected seed potatoes. Plant Pathol 50:666–675. https://doi.org/10.1046/j.1365-3059.2001.00648.x
Mejía LC, Rojas EI, Maynard Z, Van Bael S, Arnold AE, Hebbar P, Samuels GJ, Robbins N, Herre EA (2008) Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biol Control 46(1):4–14. https://doi.org/10.1016/j.biocontrol.2008.01.012
Milgroom MG, Cortesi P (2004) Biological control of chestnut blight with hypovirulence: a critical analysis. Annu Rev Phytopathol 42:311–338. https://doi.org/10.1146/annurev.phyto.42.040803.140325
Milijašević-Marčić S, Stepanović M, Todorović B, Duduk B, Stepanović J, Rekanović E, Potočnik I (2017) Biological control of green mould on Agaricus Bisporus by a native Bacillus subtilis strain from mushroom compost. Eur J Plant Pathol 148:509–519. https://doi.org/10.1007/s10658-016-1107-3
Montes-Osuna N, Gómez-Lama Cabanás C, Valverde-Corredor A, Berendsen RL, Prieto P, Mercado-Blanco J (2021) Assessing the involvement of selected phenotypes of Pseudomonas simiae PICF7 in olive root colonization and biological control of Verticillium Dahliae. Plants 10(2):412. https://doi.org/10.3390/plants10020412
Moreira JC, Jacob SC, Peres F, Lima JS, Meyer A, Oliveira-Silva JJ, Sarcinelli PN, Batista DF, Egler M, Faria MVC (2002) Integrated evaluation of the health impact of pesticide use in a community at Nova Friburgo, RJ. Ciência & saúde Coletiva 7(2):299–311. https://doi.org/10.1590/S1413-81232002000200010
Musa Z, Ma J, Egamberdieva D, Abdelshafy Mohamad OA, Abaydulla G, Liu Y, Li WJ, Li L (2020) Diversity and antimicrobial potential of cultivable endophytic actinobacteria associated with the medicinal plant Thymus roseus. Front Microbiol 11:191. https://doi.org/10.3389/fmicb.2020.00191
Nawrocka J, Małolepsza U (2013) Diversity in plant systemic resistance induced by Trichoderma. Biol Control 67(2):149–156. https://doi.org/10.1016/j.biocontrol.2013.07.005
Nerva L, Ciuffo M, Vallino M, Margaria P, Varese G, Gnavi G, Turina M (2016) Multiple approaches for the detection and characterization of viral and plasmid symbionts from a collection of marine fungi. Virus Res 219:22–38. https://doi.org/10.1016/j.virusres.2015.10.028
Ni L, Punja ZK (2019) Management of fungal diseases on cucumber (Cucumis sativus L.) and tomato (Solanum lycopersicum L.) crops in greenhouses using Bacillus subtilis (Chapter). Bacilli and Agrobiotechnology: Phytostimulation and Biocontrol: Volume 2, 1–28
Nuss DL (2005) Hypovirulence: mycoviruses at the fungal–plant interface. Nat Rev Microbiol 3:632–642. https://doi.org/10.1038/nrmicro1206
Odelade KA, Babalola OO (2019) Bacteria, fungi and archaea domains in rhizospheric soil and their effects in enhancing agricultural productivity. Int J Environ Res Public Health 16(20):3873. https://doi.org/10.3390/ijerph16203873
Olanrewaju OS, Glick BR, Babalola OO (2017) Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol 33(11):197. https://doi.org/10.1007/s11274-017-2364-9
Olowe OM, Akanmu AO, Asemoloye MD (2020) Exploration of microbial stimulants for induction of systemic resistance in plant Disease management. Ann Appl Biol 177:282–293. https://doi.org/10.1111/aab.12631
Osaki H, Nakamura H, Sasaki A, Matsumoto N, Yoshida K (2006) An endornavirus from a hypovirulent strain of the violet root rot fungus, Helicobasidium mompa. Virus Res 118:143–149. https://doi.org/10.1016/j.virusres.2005.12.004
Palm ME (2001) Systematics and the impact of invasive fungi on agriculture in the United States: knowledge of the systematics of plant-inhabiting fungi is fundamental for making appropriate plant quarantine decisions and thereby safeguarding US plant resources. Bioscience 51:141–147. https://doi.org/10.1641/0006-3568(2001)051[0141:SATIOI]2.0.CO;2
Pang F, Solanki MK, Wang Z (2022) Streptomyces can be an excellent plant growth manager. World J Microbiol Biotechnol 38(11):193. https://doi.org/10.1007/s11274-022-03380-8
Pavela R, Vrchotová N (2008) Growth inhibitory effect of extracts from Reynoutria sp. plants against Spodoptera littoralis larvae. Agrociencia 42:573–584
Pedro, de Oliveira Mirelle, Takaki Teresa Cristina Castilho et al (2013) Synthesis characterization and antifungal activity of quaternary derivatives of chitosan on Aspergillus flavus Microbiological Research 168(1) 50–55. https://doi.org/10.1016/j.micres.2012.06.006
Pei DF, Wu QQ, Luo H, Paul NC, Deng JX, Zhou Y (2019) Diversity and antifungal activity of endophytes associated with Spiranthes sinensis (Orchidaceae, Magnoliophyta) in China. Int J Appl Microbiol Biotechnol Res 7:7–17. https://doi.org/10.33500/ijambr.2019.07.003
Peixoto Neto PDS, Azevedo JL, Araújo WD (2002) Microrganismos endofíticos. Biotecnologia Ciência & Desenvolvimento 29:62–77
Penha RO, Vandenberghe LP, Faulds C, Soccol VT, Soccol CR (2020) Bacillus lipopeptides as powerful pest control agents for a more sustainable and healthy agriculture: recent studies and innovations. Planta 251(3):1–15. https://doi.org/10.1007/s00425-020-03357-7
Peters LP, Prado LS, Silva FI, Souza FS, Carvalho CM (2020) Selection of endophytes as antagonists of Colletotrichum gloeosporioides in açaí palm. Biol Control 150:104350. https://doi.org/10.1016/j.biocontrol.2020.104350
Quehenberger J, Shen L, Albers S, Siebers B, Spadiut O (2017) Sulfolobus—a potential key organism in future biotechnology. Front Microbiol 8:2474. https://doi.org/10.3389/fmicb.2017.02474
Rana KL, Kour D, Yadav N, Yadav AN (2020) 10 - endophytic microbes in nanotechnology: current development, and potential biotechnology applications (chapter). Microbial endophytes (Book). Elsevier, pp 231–262. https://doi.org/10.1016/B978-0-12-818734-0.00010-3
Rani A, Saini KC, Bast F, Mehariya S, Bhatia SK, Lavecchia R, Zuorro A (2021) Microorganisms: a potential source of bioactive molecules for antioxidant applications. Molecules 26(4):1142. https://doi.org/10.3390/molecules26041142
Rao TB, Chopperla R, Methre R, Punniakotti E, Venkatesh V, Sailaja B, Reddy MR, Yugander A, Laha G, Madhav MS (2019) Pectin induced transcriptome of a Rhizoctonia solani strain causing sheath blight Disease in rice reveals insights on key genes and RNAi machinery for development of pathogen derived resistance. Plant Mol Biol 100:59–71. https://doi.org/10.1007/s11103-019-00843-9
Rigling D, Prospero S (2018) Cryphonectria parasitica, the causal agent of chestnut blight: invasion history, population biology and Disease control. Mol Plant Pathol 19:7–20. https://doi.org/10.1111/mpp.12542
Rojas-Solís D, Zetter-Salmón E, Contreras-Pérez M, del Carmen Rocha-Granados M, Macías-Rodríguez L, Santoyo G (2018) Pseudomonas stutzeri E25 and Stenotrophomonas maltophilia CR71 endophytes produce antifungal volatile organic compounds and exhibit additive plant growth-promoting effects. Biocatal Agric Biotechnol 13:46–52. https://doi.org/10.1016/j.bcab.2017.11.007
Roscetto E, Contursi P, Vollaro A, Fusco S, Notomista E, Catania MR (2018) Antifungal and anti-biofilm activity of the first cryptic antimicrobial peptide from an archaeal protein against Candida spp. clinical isolates. Sci Rep 8(1):17570. https://doi.org/10.1038/s41598-018-35530-0
Rotolo C, De Miccolis Angelini RM, Pollastro S, & Faretra F (2016) A TaqMan-based qPCR assay for quantitative detection of the biocontrol agents Bacillus subtilis strain QST713 and Bacillus amyloliquefaciens subsp. plantarum strain D747. BioControl 61:91-101
Saad AM, Salem HM, El-Tahan AM, El-Saadony MT, Alotaibi SS, El-Shehawi AM, Alkahtani MA, Ahmed AE, Swelum AA (2022) Biological control: an effective approach against nematodes using black pepper plants (Piper nigrum L). Saudi J Biol Sci 29(4):2047–2055. https://doi.org/10.1016/j.sjbs.2022.01.004
Sabra MA, Alaidaroos BA, Jastaniah SD, Heflish AI, Ghareeb RY, Mackled MI, El-Saadony MT, Abdelsalam NR, Conte-Junior CA (2022) Comparative effect of commercially available nanoparticles on soil bacterial community and Botrytis fabae caused brown spot: in vitro and in vivo experiment. Front Microbiol 13:934031. https://doi.org/10.3389/fmicb.2022.934031
Saeed EE, Sham A, Salmin Z, Abdelmowla Y, Iratni R, El-Tarabily KA, AbuQamar SF (2017) Streptomyces globosus UAE1, a potential effective biocontrol agent for black scorch Disease in date palm plantations. Front Microbiol 8:1455. https://doi.org/10.3389/fmicb.2017.01455
Sanogo S & Lujan P (2022) Seed, plant, and soil treatment with selected commercial Bacillus-based and Streptomyces-based biofungicides and chemical fungicides and development of Phytophthora blight on chile pepper. Arch. Phytopathol. Pflanzenschutz 55(3):331-343
Santos CMD, Ribeiro ADS, Garcia A, Polli AD, Polonio JC, Azevedo JL, Pamphile JA (2019) Enzymatic and antagonist activity of endophytic fungi from Sapindus saponaria L.(Sapindaceae). Acta Biol Colomb 24(2):322–330. https://doi.org/10.15446/abc.v24n2.74717
Sass G, Nazik H, Penner J, Shah H, Ansari SR, Clemons KV, Groleau MC, Dietl AM, Visca P, Haas H (2018) Studies of Pseudomonas aeruginosa mutants indicate pyoverdine as the central factor in inhibition of aspergillus fumigatus biofilm. J Bacteriol 200(1):e00345. https://doi.org/10.1128/JB.00345-17
Schardl CL, Phillips TD (1997) Protective grass endophytes: where are they from and where are they going? Plant Dis 81:430–438. https://doi.org/10.1094/PDIS.1997.81.5.430
Schoelz JE, Stewart LR (2018) The role of viruses in the phytobiome. Annu Rev Virol 5:93–111. https://doi.org/10.1146/annurev-virology-092917-043421
Selim HM, Gomaa NM, Essa AM (2016) Antagonistic effect of endophytic bacteria against some phytopathogens. Egypt J Bot 56(3):613–626. https://doi.org/10.21608/ejbo.2016.2721
Selim HM, Gomaa NM, Essa AM (2017) Application of endophytic bacteria for the biocontrol of Rhizoctonia solani (Cantharellales: ceratobasidiaceae) damping-off Disease in cotton seedlings. Biocontrol Sci Technol 27:81–95. https://doi.org/10.1080/09583157.2016.1258452
Shand RF, Leyva KJ (2008) Archaeal Antimicrobials: An Undiscovered Country, Archaea: New Models for Prokaryotic Biology (Edited by: Paul Blum). Caister Academic Press, U.K
Silva RN, Monteiro VN, Steindorff AS, Gomes EV, Noronha EF, Ulhoa CJ (2019) Trichoderma/pathogen/plant interaction in pre-harvest food security. Fungal Biol 123(8):565–583. https://doi.org/10.1016/j.funbio.2019.06.010
South KA, Peduto Hand F, Jones ML (2020) Beneficial bacteria identified for the control of Botrytis Cinerea in petunia greenhouse production. Plant Dis 104:1801–1810. https://doi.org/10.1094/PDIS-10-19-2276-RE
Stahr M, Quesada-Ocampo L (20200. Assessing the role of temperature, inoculum density, and wounding on disease progression of the fungal pathogen Ceratocystis fimbriata causing black rot in sweetpotato. Plant Dis 104: 930–937. https://doi.org/10.1094/PDIS-12-18-2224-RE
Tanapichatsakul C, Pansanit A, Monggoot S, Brooks S, Prachya S, Kittakoop P, Panuwet P, Pripdeevech P (2020) Antifungal activity of 8-methoxynaphthalen-1-ol isolated from the endophytic fungus diatrype palmicola MFLUCC 17–0313 against the plant pathogenic fungus athelia rolfsii on tomatoes. PeerJ 8:e9103. https://doi.org/10.7717/peerj.9103
Tortora ML, Díaz-Ricci JC, Pedraza RO (2011) Azospirillum brasilense siderophores with antifungal activity against Colletotrichum Acutatum. Arch Microbiol 193(4):275–286. https://doi.org/10.1007/s00203-010-0672-7
Vejan P, Abdullah R, Khadiran T, Ismail S, Nasrulhaq Boyce A (2016. Role of plant growth promoting rhizobacteria in agricultural sustainability—a review. Molecules 21(5):573. https://doi.org/10.3390/molecules21050573
Xiao X, Cheng J, Tang J, Fu Y, Jiang D, Baker TS, Ghabrial SA, Xie J (2014) A novel partitivirus that confers hypovirulence on plant pathogenic fungi. J Virol 88(17):10120–10133. https://doi.org/10.1128/JVI.01036-14
Xiao Y, Li HX, Li C, Wang JX, Li J, Wang MH, Ye YH (2013) Antifungal screening of endophytic fungi from Ginkgo biloba for discovery of potent anti-phytopathogenic fungicides. FEMS Microbiol Lett 339:130–136
Xie J, Jiang D (2014) New insights into mycoviruses and exploration for the biological control of crop fungal Diseases. Annu Rev Phytopathol 52:45–68. https://doi.org/10.1146/annurev-phyto-102313-050222
Yan Y, Yuan Q, Tang J, Huang J, Hsiang T, Wei Y, Zheng L (2018) Colletotrichum Higginsianum as a model for understanding host–pathogen interactions: a review. Int J Mol Sci 19(7):2142. https://doi.org/10.3390/ijms19072142
Yeh C, Wang C, Chen Y, Tsai S, Chung W (2021) Potential of a volatile-producing endophytic fungus nodulisporium sp. PDL-005 for the control of Penicillium Digitatum. Biol Control 152:104459. https://doi.org/10.1016/j.biocontrol.2020.104459
Yu X, Li B, Fu Y, Jiang D, Ghabrial SA, Li G, Peng Y, Xie J, Cheng J, Huang J (2010) A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci 107(18):8387–8392. https://doi.org/10.1073/pnas.0913535107
Yu X, Li B, Fu Y, Xie J, Cheng J, Ghabrial SA, Li G, Yi X, Jiang D (2013) Extracellular transmission of a DNA mycovirus and its use as a natural fungicide. Proc Natl Acad Sci 110(4):1452–1457. https://doi.org/10.1073/pnas.1213755110
Zhou T, Boland GJ (1998) Suppression of dollar spot by hypovirulent isolates of Sclerotinia homoeocarpa. Phytopathology 88(8):788–794. https://doi.org/10.1094/PHYTO.1998.88.8.788
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Alamoudi, S.A. Using some microorganisms as biocontrol agents to manage phytopathogenic fungi: a comprehensive review. J Plant Pathol 106, 3–21 (2024). https://doi.org/10.1007/s42161-023-01542-7
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DOI: https://doi.org/10.1007/s42161-023-01542-7