Abstract
Fusarium is a genus among the major pathogens affecting cereals production worldwide. At present, the control of Fusarium diseases in farm largely relies on the use of chemical fungicides, which are persistent in environments and harmful to human health. To reduce the risk of using chemical compounds, it becomes urgent to find an alternative strategy, such as bio-agents to control Fusarium diseases. Beneficial microorganisms underground have been well known for their activity to trigger induced systemic resistance (ISR) against pathogens, existing either in the soil or aboveground. Despite numerous studies suggesting various beneficial microorganisms, also recognized as bio-control agents (BCAs), including Bacillus spp., Trichodema spp., Pseudomomas spp. and others, as capable of suppressing diverse crop diseases, the function and mechanisms underlying ISR triggered by these beneficial microbes in controlling Fusarium diseases remain to be systemically understood. In this review, we summarize the roles of diverse beneficial microbes in limiting crop Fusarium diseases and also discuss the possible involvement of ISR with associated signaling pathways employed in Fusarium disease control. Finally, we consider the practical application of diverse BCAs with ISR activity for ecological and sustainable crop production.
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References
Abdelrahman M, Abdel-Motaal F, El-Sayed M, Jogaiah S, Shigyo M, Ito S, Ichi, Tran LSP (2016) Dissection of Trichoderma longibrachiatum-induced defense in onion (Allium cepa L.) against Fusarium oxysporum f. sp. cepa by target metabolite profiling. Plant Sci 246:128–138. https://doi.org/10.1016/j.plantsci.2016.02.008
Abeysinghe S (2007) Biological control of Fusarium solani f. sp. phaseoli the causal agent of root rot of bean using Bacillus subtilis CA32 and Trichoderma harzianum RU01. Ruhuna J Sci 2:82–88. http://www.ruh.ac.lk/rjs/rjs.html
Abramovitch RB, Martin GB (2004) Strategies used by bacterial pathogens to suppress plant defenses. Curr Opin Plant Biol 7:356–364. https://doi.org/10.1016/j.pbi.2004.05.002
Adenihi AA, Babalola OO (2018) Tackling maize fusariosis: in search of Fusarium graminearum biosuppressors. Arch Microbiol 200:1239–1255. https://doi.org/10.1007/s00203-018-1542-y
Aimé S, Alabouvette C, Steinberg C, Olivain C (2013) The endophytic strain Fusarium oxysporum Fo47: a good candidate for priming the defense responses in tomato roots. Mol Plant Microbe Interact 26:918–926. https://doi.org/10.1094/MPMI-12-12-0290-R
Amira MB, Lopeza D, Mohamedc AT, Khouajab A, Chaard H, Fumanala B, Gousset-Duponta A, Bonhommee L, Labela P, Goupila P, Ribeiroa S, Pujade-Renauda V, Juliena J-L, Auguing D, Venissea JS (2017) Beneficial effect of Trichoderma harzianum strain Ths97 in biocontrolling Fusarium solani causal agent of root rot disease in olive trees. Biol Control 110:70–78. https://doi.org/10.1016/j.biocontrol.2017.04.008
Anjaiah V, Cornelis P, Koedam N (2003) Effect of genotype and root colonization in biological control of fusarium wilts in pigeonpea and chickpea by Pseudomonas aeruginosa PNA1. Can J Microbiol 49:85–91. https://doi.org/10.1139/w03-011
Arfaoui A, El Hadrami A, Mabrouk Y, Sifi B, Boudabous A, El Hadrami I, Daayf F, Chérif M (2007) Treatment of chickpea with Rhizobium isolates enhances the expression of phenylpropanoid defense-related genes in response to infection by Fusarium oxysporum f. sp. ciceris. Plant Physiol Biochem 45:470–479. https://doi.org/10.1016/j.plaphy.2007.04.004
Aysan E, Demir S (2009) Using arbuscular Mycorrhizal fungi and Rhizobium leguminosarum biovar phaseoli against Sclerotinia sclerotiorum (Lib.) de Bary in the Common Bean (Phaseolus vulgaris L.). Plant Pathol J 8:74–78. https://doi.org/10.3923/ppj.2009.74.78
Bacon CW, Hinton DM (2007) Potential for control of seedling blight of wheat caused by Fusarium graminearum and related species using the bacterial endophyte Bacillus mojavensis. Biocontrol Sci Technol 27:81–94. https://doi.org/10.1080/09583150600937006
Bacon CW, Yates IE, Hinton DM, Meredith F (2001) Biological control of Fusarium moniliforme in maize. Environ Health Perspect 109(Suppl):325–332. https://doi.org/10.2307/3435026
Bai G, Shaner G (2004) Management and resistance in wheat and barley to Fusarium head blight. Annu Rev Phytopathol 42:135–161. https://doi.org/10.1146/annurev.phyto.42.040803.140340
Bakker PAHM, Pieterse CMJ, van Loon LC (2007) Induced systemic resistance by fluorescent Pseudomonas spp. J Phytopathol 97(2):239–243. https://doi.org/10.1094/PHYTO-97-2-0239
Bakker MG, Brown DW, Kelly AC, Kim H-S, Kurtzman CP, Mccormick SP, O’Donnell KL, Proctor RH, Vaughan MM, Ward TJ (2018) Fusarium mycotoxins: a trans-disciplinary overview. Can J Plant Path 40(2):161–171. https://doi.org/10.1080/07060661.2018.1433720
Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S (2004) Bacterial persistence as a phenotypic switch. Science 305:1622–1625. https://doi.org/10.1126/science.1099390
Beckers GJM, Jaskiewicz M, Liu Y, Underwood WR, He SY, Zhang S, Conrath U (2009) Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell Online 21:944–953. https://doi.org/10.1105/tpc.108.062158
Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. https://doi.org/10.1016/j.tplants.2012.04.001
Bezemer TM, Van Dam NM (2005) Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol Evol 20:617–624. https://doi.org/10.1016/j.tree.2005.08.006
Blacutt AA, Mitchell TR, Bacon CW, Gold SE (2016) Bacillus mojavensis RRC101 lipopeptides provoke physiological and metabolic changes during antagonism against Fusarium verticillioides. Mol Plant Microbe Interact 29:713–723
Blagodatskaya E, Kuzyakov Y (2008) Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biol Fertil Soils 45:115–131. https://doi.org/10.1007/s00374-008-0334-y
Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406. https://doi.org/10.1146/annurev.arplant.57.032905.105346
Bradley GG, Punjaa ZK (2010) Composts containing fluorescent pseudomonads suppress fusarium root and stem rot development on greenhouse cucumber. Can J Microbiol 56:896–905. https://doi.org/10.1139/W10-076
Buonaurio R, Scarponi L, Ferrara M, Sidoti P, Bertona A (2002) Induction of systemic acquired resistance in pepper plants by acibenzolar-S-methyl against bacterial spot disease. Eur J Plant Pathol 108:41–49. https://doi.org/10.1023/A:1013984511233
Burketova L, Trda L, Ott PG, Valentova O (2015) Bio-based resistance inducers for sustainable plant protection against pathogens. Biotechnol Adv 33:994–1004. https://doi.org/10.1016/j.biotechadv.2015.01.004
Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48:489–499. https://doi.org/10.1007/s00374-012-0691-4
Choudhary DK, Johri BN (2009) Interactions of Bacillus spp. and plants—with special reference to induced systemic resistance (ISR). Microbiol Res 164:493–513. https://doi.org/10.1016/j.micres.2008.08.007
Choudhary DK, Prakash A, Johri BN (2007) Induced systemic resistance (ISR) in plants: mechanism of action. Indian J Microbiol 47:289–297. https://doi.org/10.1007/s12088-007-0054-2
Conrath U, Thulke O, Katz V, Schwindling S, Kohler A (2001) Priming as a mechanism in induced systemic resistance of plants. Eur J Plant Pathol 107:113–119. https://doi.org/10.1023/A:1008768516313
Conrath U, Beckers GJM, Flors V, García-Agustín P, Jakab G, Mauch F, Newman M-A, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19:1062–1071. https://doi.org/10.1094/MPMI-19-1062
Cooney JM, Lauren DR, Di Menna ME (2001) Impact of competitive fungi on trichothecene production by Fusarium graminearum. J Agric Food Chem 49:522–526. https://doi.org/10.1021/jf0006372
Cui H, Tsuda K, Parker JE (2015) Effector-triggered immunity: from pathogen perception to robust defense. Annu Rev Plant Biol 66:487–511. https://doi.org/10.1146/annurev-arplant-050213-040012
De Cal A, Sztejnberg A, Sabuquillo P, Melgarejo P (2009) Management Fusarium wilt on melon and watermelon by Penicillium oxalicum. Biol Control 51:480–486. https://doi.org/10.1016/j.biocontrol.2009.08.011
Dean R, Van Kan JAL, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430. https://doi.org/10.1111/j.1364-3703.2011.00783.x
Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP (2011) Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9:749–759. https://doi.org/10.1038/nrmicro2637
Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209. https://doi.org/10.1146/annurev.phyto.42.040803.140421
Fatima S, Anjum T (2017) Identification of a potential ISR determinant from Pseudomonas aeruginosa PM12 against Fusarium wilt in tomato. Front Plant Sci 8:1–14. https://doi.org/10.3389/fpls.2017.00848
Ferrigo D, Raiola A, Causin R (2016) Fusarium toxins in cereals: occurence, legislation, factors promoting the appearance and their management. Molecules 21:627. https://doi.org/10.3390/molecules21050627
Filion M, St-Arnaud M, Fortin JA (1999) Direct interaction between the arbuscular mycorrhizal fungus Glomus intraradices and different rhizosphere microorganisms. New Phytol 141:525–533. https://doi.org/10.1046/j.1469-8137.1999.00366.x
Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64:839–863. https://doi.org/10.1146/annurev-arplant-042811-105606
Gao G, Yin D, Chen S, Xia F, Yang J, Li Q, Wang W (2012) Effect of biocontrol agent Pseudomonas fluorescens 2P24 on soil fungal community in cucumber rhizosphere using T-RFLP and DGGE. PLoS ONE 7(2):e31806. https://doi.org/10.1371/journal.pone.0031806
Gerhardson B (2002) Biological substitutes for pesticides. Trends Biotechnol 20(8):338–343
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227. https://doi.org/10.1146/annurev.phyto.43.040204.135923
Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117. https://doi.org/10.1139/m95-015
Goellner K, Conrath U (2008) Priming: it’s all the world to induced disease resistance. Sustain Dis Manag Eur Context. https://doi.org/10.1007/978-1-4020-8780-6_3
Gómez-Gómez L (2004) Plant perception systems for pathogen recognition and defence. Mol Immunol 41:1055–1062. https://doi.org/10.1016/j.molimm.2004.06.008
Gong AD, Li HP, Yuan QS, Song XS, Yao W, He WJ, Zhang JB, Liao YC (2015) Antagonistic mechanism of iturin A and plipastatin A from Bacillus amyloliquefaciens S76-3 from wheat spikes against Fusarium graminearum. PLoS ONE 10:e0116871
Gu Q, Yang Y, Yuan Q, Shi G, Wu L, Lou Z, Huo R, Wu H, Borriss R, Gao X (2017) Bacillomycin D produced by Bacillus amyloliquefaciens is involved in the antagonistic interaction with the plant-pathogenic fungus Fusarium graminearum. Appl Environ Microbiol. https://doi.org/10.1128/AEM.01075-17
Hanson LE, Howell CR (2004) Elicitors of plant defense responses from biocontrol strains of Trichoderma viren. Phytopathology 94:171–176. https://doi.org/10.1094/PHYTO.2004.94.2.171
Hasan MM, Rahman SME, Kim GH, Abdallah E, Oh DH (2012) Antagonistic potentiality of Trichoderma harzianum towards seed-borne fungal pathogens of winter wheat cv. Protiva in vitro and in vivo. J Microbiol Biotechnol 22:585–591. https://doi.org/10.4014/jmb.1107.07063
Hassan Dar G, Zargar M, Beigh G (1997) Biocontrol of Fusarium root rot in the common bean (Phaseolus vulgaris L.) by using symbiotic Glomus mosseae and Rhizobium leguminosarum. Microb Ecol 34:74–80. https://doi.org/10.1007/s002489900036
Hause B, Fester T (2005) Molecular and cell biology of arbuscular mycorrhizal symbiosis. Planta 221:184–196. https://doi.org/10.1007/s00425-004-1436-x
Heath MC (2000) Hypersensitive response-related death. Plant Mol Biol 44:321–334. https://doi.org/10.1023/A:1026592509060
Heil M, Bostock RM (2002) Induced systemic resistance (ISR) against pathogens in the context of induced plant defences. Ann Bot 89:503–512. https://doi.org/10.1093/aob/mcf076
Heinen R, Biere A, Harvey JA, Bezemer TM (2018) Effects of soil organisms on aboveground plant-insect interactions in the field: patterns, mechanisms and the role of methodology. Front Ecol Evol 6:1–15. https://doi.org/10.3389/fevo.2018.00106
Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25. https://doi.org/10.1099/mic.0.052274-0
Hillocks RJ (2012) Farming with fewer pesticides: EU pesticide review and resulting challenges for UK agriculture. Crop Prot 31:85–93. https://doi.org/10.1016/j.cropro.2011.08.008
Hossain M, Sultana F, Kubota M, Koyama H, Hyakumachi M (2007) The plant growth-promoting fungus Penicillium simplicissimum GP17-2 induces resistance in Arabidopsis thaliana by activation of multiple defense signals. Plant Cell Physiol 48:1724–1736. https://doi.org/10.1093/pcp/pcm144
Hwang SF, Chang KF, Chakravarty P (1992) Effects of vesicular-arbuscular mycorrhizal fungi on the development of Verticillium and Fusarium wilts of alfalfa. Plant Dis 76:239. https://doi.org/10.1094/PD-76-0239
Ismail Y, Mccormick S, Hijri M (2013) The arbuscular mycorrhizal fungus, glomus irregulare, controls the mycotoxin production of Fusarium sambucinum in the pathogenesis of potato. FEMS Microbiol Lett 348:46–51. https://doi.org/10.1111/1574-6968.12236
Jaiti F, Meddich A, El Hadrami I (2007) Effectiveness of arbuscular mycorrhizal fungi in the protection of date palm (Phoenix dactylifera L.) against bayoud disease. Physiol Mol Plant Pathol 71:166–173. https://doi.org/10.1016/j.pmpp.2008.01.002
Jetiyanon K, Jetiyanon K, Kloepper JW, Kloepper JW (2002) Mixtures of plant growth-promoting rhizobacteria for induction of systemic resistance against multiple plant diseases. Biol Control 24:285–291. https://doi.org/10.1016/S1049-9644(02)00022-1
Jogaiah S, Abdelrahman M, Tran L-SP, Ito S-I (2018) Different mechanisms of Trichoderma virens-mediated resistance in tomato against Fusarium wilt involve the jasmonic and salicylic acid pathways. Mol Plant Pathol 19(4):870–882
Junaid JM, Dar NA, Bhat TA, Bhat AH, Bhat MA (2013) Commercial biocontrol agents and their mechanism of action in the management of plant pathogens. Int J Mod Plant Anim Sci 1:39–57. www.ModernScientificPress.com/Journals/IJPlant.aspx
Kalia A, Gosal SK (2011) Effect of pesticide application on soil microorganisms. Arch Agron Soil Sci 57:569–596. https://doi.org/10.1080/03650341003787582
Katz VA, Thulke OU, Conrath U (1998) A benzothiadiazole primes parsley cells for augmented elicitation of defense responses. Plant Phyiol 117:1333–1339. https://doi.org/10.1104/pp.117.4.1333
Khan N, Maymon M, Hirsch A (2017) Combating Fusarium infection using bacillus-based antimicrobials. Microorganisms 5:75. https://doi.org/10.3390/microorganisms5040075
Kimani VN, Chen L, Liu Y, Raza W, Zhang N, Mungai LK, Shen Q, Zhang R (2016) Characterization of extracellular polymeric substances of Bacillus amyloliquefaciens SQR9 induced by root exudates of cucumber (Cucumis sativus L.) at different developmental stages. J Basic Microbiol. https://doi.org/10.1002/jobm.201600104
Kistler HC, Rep M, Ma L-J (2013) Structural dynamics of Fusarium genomes. In: Brown DW, Proctor RH (eds) Fusarium, genomics, molecular and cellular biology. Caister Academic Press, Norfolk, pp 31–42
Kköprü A (2005) Biological control of Fusarium wilt in tomato caused by Fusarium oxysporum f. sp. lycopersici by AMF Glomus intraradices and some rhizobacteria. J Phytopathol 550:544–550. https://doi.org/10.1111/j.1439-0434.2005.01018.x
Król P, Igielski R, Pollmann S, Kepczyńska E (2015) Priming of seeds with methyl jasmonate induced resistance to hemi-biotroph Fusarium oxysporum f.sp. lycopersici in tomato via 12-oxo-phytodienoic acid, salicylic acid, and flavonol accumulation. J Plant Physiol 179:122–132. https://doi.org/10.1016/j.jplph.2015.01.018
Kumar D (2014) Salicylic acid signaling in disease resistance. Plant Sci 228:127–134. https://doi.org/10.1016/j.plantsci.2014.04.014
Larena I, Sabuquillo P, Melgarejo P, De Cal A (2003) Biocontrol of Fusarium and Verticillium wilt of tomato by Penicillium oxalicum under greenhouse and field conditions. J Phytopathol 151:507–512. https://doi.org/10.1046/j.1439-0434.2003.00762.x
Lee T, Park D, Kim K, Lim SM, Yu NH, Kim S, Kim HY, Jung KS, Jang JY, Park JC, Ham H, Lee S, Hong SK, Kim JC (2017) Characterization of Bacillus amyloliquefaciens DA12 showing potent antifungal activity against mycotoxigenic Fusarium species. Plant Pathol J 33:499–507. https://doi.org/10.5423/PPJ.FT.06.2017.0126
Leeman M (1995) Induction of systemic resistance against fusarium wilt of radish by lipopolysaccharides of Pseudomonas fluorescens. Phytopathology 85:1021–1027. https://doi.org/10.1094/Phyto-85-1021
Li B, Li Q, Xu Z, Zhang N, Shen Q, Zhang R (2014) Responses of beneficial Bacillus amyloliquefaciens SQR9 to different soilborne fungal pathogens through the alteration of antifungal compounds production. Front Microbiol 5:1–11. https://doi.org/10.3389/fmicb.2014.00636
Li Y, Gu Y, Li J, Xu M, Wei Q, Wang Y (2015) Biocontrol agent Bacillus amyloliquefaciens LJ02 induces systemic resistance against cucurbits powdery mildew. Front Microbiol 6:883. https://doi.org/10.3389/fmicb.2015.00883
Li Y, Sun R, Yu J, Saravanakumar K, Chen J (2016) Antagonistic and biocontrol potential of Trichoderma asperellum ZJSX5003 against the maize stalk rot pathogen Fusarium graminearum. Indian J Microbiol 56:318–327. https://doi.org/10.1007/s12088-016-0581-9
Liu Y, Chen L, Wu G, Feng H, Zhang G, Shen Q, Zhang R (2017) Identification of root-secreted compounds involved in the communication between cucumber, the beneficial Bacillus amyloliquefaciens, and the soil-borne pathogen Fusarium oxysporum. Mol Plant Microbe Interact 30:53–62. https://doi.org/10.1094/MPMI-07-16-0131-R
Ma L-J, van der Does HC, Borkovich KA et al (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464(18):367–373. https://doi.org/10.1038/nature08850
Ma L-J, 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
Macho AP, Zipfel C (2014) Plant PRRs and the activation of innate immune signaling. Mol Cell 54:263–272. https://doi.org/10.1016/j.molcel.2014.03.028
Manivel BS, Rajkumar SG (2018) Mycopesticides: fungal based pesticides for sustainable agriculture. In: Fungi and their role in sustainable development: current perspectives. Springer, Singapore, pp 183–203. https://doi.org/10.1007/978-981-13-0393-7_11
Marschner P, Timonen S (2005) Interactions between plant species and mycorrhizal colonization on the bacterial community composition in the rhizosphere. Appl Soil Ecol 28:23–36. https://doi.org/10.1016/j.apsoil.2004.06.007
Martínez-Álvarez JC, Castro-Martínez C, Sánchez-Peña P, Gutiérrez-Dorado R, Maldonado-Mendoza IE (2016) Development of a powder formulation based on Bacillus cereus sensu lato strain B25 spores for biological control of Fusarium verticillioides in maize plants. World J Microbiol Biotechnol 32:75. https://doi.org/10.1007/s11274-015-2000-5
Martínez-Medina A, Pascual JA, Pérez-Alfocea F, Albacete A, Roldán A (2010) Trichoderma harzianum and Glomus intraradices modify the hormone disruption induced by Fusarium oxysporum infection in melon plants. Phytopathology 100:682–688. https://doi.org/10.1094/PHYTO-100-7-0682
Matinez-Medina A, Flors V, Heil M, Mauch-Mani B, Peiterse CMJ, Pozo MJ, Ton J, van Dam NM, Conrath U (2016) Recognizing plant defense priming. Trends Plant Sci 21(10):818–822
Matyjaszczyk E (2018) Plant protection means used in organic farming throughout the European Union. Pest Manag Sci 74:505–510. https://doi.org/10.1002/ps.4789
Mauch-Mani B, Baccelli I, Luna E, Flors V (2017) Defense priming: an adaptive part of induced resistance. Annu Rev Plant Biol 68:485–512. https://doi.org/10.1146/annurev-arplant-042916-041132
Maurhofer M, Keel C, Haas D, Defago G (1995) Influence of plant species on disease suppression by Pseudomonas fluorescens strain CHA0 with enhanced antibiotic production. Plant Pathol 44:40–50. https://doi.org/10.1111/j.1365-3059.1995.tb02714.x
Metraux J-P, Signer H, Ryals J, Ward E, Wyss-Benz M, Gaudin J, Raschdorf K, Schmid E, Blum W, Inverardi B (1990) Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250(4983):1004–1006. https://doi.org/10.1126/science.250.4983.1004
Molinari S, Fanelli E, Leonetti P (2014) Expression of tomato salicylic acid (SA)-responsive pathogenesis-related genes in Mi-1-mediated and SA-induced resistance to root-knot nematodes. Mol Plant Pathol 15:255–264. https://doi.org/10.1111/mpp.12085
Munkvold GP (2017) Fusarium species and their associated mycotoxins. In: Moretti A, Susca A (eds) Mycotoxigenic fungi: methods and protocols, methods in molecular biology, vol 1542. Springer, Berlin. https://doi.org/10.1007/978-1-4939-6707-0_4
Neumeister B, Bartmann P, Gaedicke G, Marre R (2009) A fatal infection due to Fusarium oxysporum in a child with Wilms’ tumour. Case report and review of the literature. Mycoses 35:115–119. https://doi.org/10.1111/j.1439-0507.1992.tb00831.x
Newman JRS, Ghaemmaghami S, Ihmels J, Breslow DK, Noble M, DeRisi JL, Weissman JS (2006) Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441:840–846. https://doi.org/10.1038/nature04785
Nguyen PA, Strub C, Fontana A, Schorr-Galindo S (2017) Crop molds and mycotoxins: alternative management using biocontrol. Biol Control 104:10–27. https://doi.org/10.1016/j.biocontrol.2016.10.004
Ongena M, Jourdan E, Adam A, Paquot M, Brans A, Joris B, Arpigny JL, Thonart P (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9:1084–1090. https://doi.org/10.1111/j.1462-2920.2006.01202.x
Oros G, Naár Z (2017) Mycofungicide: Trichoderma based preparation for foliar applications. Am J Plant Sci 8:113–125. https://doi.org/10.4236/ajps.2017.82009
Pestka JJ (2010) Toxicological mechanisms and potential health effects of deoxynivalenol and nivalenol. Word Mycotoxin J 3:323–347. https://doi.org/10.3920/WMJ2010.1247
Pieterse CMJ (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580. https://doi.org/10.1105/tpc.10.9.1571
Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375. https://doi.org/10.1146/annurev-phyto-082712-102340
Pineda A, Zheng SJ, van Loon JJA, Pieterse CMJ, Dicke M (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15:507–514. https://doi.org/10.1016/j.tplants.2010.05.007
Planchamp C, Glauser G, Mauch-Mani B (2015) Root inoculation with Pseudomonas putida KT2440 induces transcriptional and metabolic changes and systemic resistance in maize plants. Front Plant Sci 5:1–10. https://doi.org/10.3389/fpls.2014.00719
Ploetz RC, Kema GHJ, Ma L-J (2015) Impact of diseases on export and smallholder production of banana. Annu Rev Phytopathol 53:269–288. https://doi.org/10.1146/annurev-phyto-080614-120305
Pozo MJ, Van Loon LC, Pieterse CMJ (2004) Jasmonates—signals in plant-microbe interactions. J Plant Growth Regul 23:211–222. https://doi.org/10.1007/s00344-004-0031-5
Purrington CB (2000) Costs of resistance. Curr Opin Plant Biol 3:305–308. https://doi.org/10.1016/S1369-5266(00)00085-6
Qiu M, Zhang R, Xue C, Zhang S, Li S, Zhang N, Shen Q (2012) Application of bio-organic fertilizer can control Fusarium wilt of cucumber plants by regulating microbial community of rhizosphere soil. Biol Fertil Soils 48:807–816
Ram RM, Keswani C, Bisen K, Tripathi R, Singh SP, Singh HB (2018) Biocontrol technology: eco-friendly approaches for sustainable agriculture. Omics Technol Bio-Eng 2:177–190. https://doi.org/10.1016/B978-0-12-815870-8.00010-3
Raza W, Ling N, Zhang R, Huang Q, Xu Y, Shen Q (2017) Success evaluation of the biological control of Fusarium wilts of cucumber, banana, and tomato since 2000 and future research strategies. Crit Rev Biotechnol 37:202–212. https://doi.org/10.3109/07388551.2015.1130683
Rillig MC, Rolff J, Tietjen B, Wehner J, Andrade-Linares DR (2015) Community priming-effects of sequential stressors on microbial assemblages. FEMS Microbiol Ecol 91:1–7. https://doi.org/10.1093/femsec/fiv040
Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343. https://doi.org/10.1146/annurev-phyto-073009-114447
Rosier A, Bishnoi U, Lakshmanan V (2016) A perspective on inter-kingdom signaling in plant—beneficial microbe interactions. Plant Mol Biol 90:537. https://doi.org/10.1007/s11103-016-0433-3
Ross AF (1961) Localized acquired resistance to plant virus infection in hypersensitive hosts. Virology 14:329–339. https://doi.org/10.1016/0042-6822(61)90318-X
Salas-Marina MA, Silva-Flores MA, Uresti-Rivera EE, Castro-Longoria E, Herrera-Estrella A, Casas-Flores S (2011) Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance through jasmonic acid/ethylene and salicylic acid pathways. Eur J Plant Pathol 131:15–26. https://doi.org/10.1007/s10658-011-9782-6
Saravanakumar K, Fan L, Fu K, Yu C, Wang M, Xia H, Sun J, Li Y, Chen J (2016) Cellulase from Trichoderma harzianum interacts with roots and triggers induced systemic resistance to foliar disease in maize. Sci Rep 6:1–18. https://doi.org/10.1038/srep35543
Saravanakumar K, Li Y, Yu C, Wang Q (2017) Effect of Trichoderma harzianum on maize rhizosphere microbiome and biocontrol of Fusarium Stalk rot. Sci Rep. https://doi.org/10.1038/s41598-017-01680-w
Saravanakumar K, Dou K, Lu Z, Wang X, Li Y, Chen J (2018) Enhanced biocontrol activity of cellulase from Trichoderma harzianum against Fusarium graminearum through activation of defense-related genes in maize. Physiol Mol Plant Pathol 103:130–136. https://doi.org/10.1016/j.pmpp.2018.05.004
Sarkar PK, Hasenack B, Nout MJR (2002) Diversity and functionality of Bacillus and related genera isolated from spontaneously fermented soybeans (Indian Kinema) and locust beans (African Soumbala). Int J Food Microbiol 77:175–186. https://doi.org/10.1016/S0168-1605(02)00124-1
Slaughter A, Daniel X, Flors V, Luna E, Hohn B, Mauch-Mani B (2012) Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol 158:835–843. https://doi.org/10.1104/pp.111.191593
Starnaud M, Hamel C, Vimard B, Caron M, Fortin JA (1995) Altered growth of Fusarium oxysporum f. sp. chrysanthemi in an in vitro dual culture system with the vesicular-arbuscular mycorrhizal fungus Glomus intraradices growing on Daucus carota transformed roots. Mycorrhiza 5:431–438. https://doi.org/10.1007/s005720050093
Strack D, Fester T, Hause B, Schliemann W, Walter MHMH (2003) Review paper arbuscular mycorrhiza: biological, chemical, and molecular aspects. Rev Lit Arts Am 29:1955–1979. https://doi.org/10.1023/A:1025695032113
Tabassum T, Farooq M, Ahmad R, Zohaib A, Wahid A (2017) Seed priming and transgenerational drought memory improves tolerance against salt stress in bread wheat. Plant Physiol Biochem 118:362–369. https://doi.org/10.1016/j.plaphy.2017.07.007
Termorshuizen A, Jeger MJ (2008) Strategies of soilborne plant pathogenic fungi in relation to disease suppression. Fungal Ecol 1(4):108–114. https://doi.org/10.1016/j.funeco.2008.10.006
Thatcher LF, Manners JM, Kazan K (2009) Fusarium oxysporum hijacks COI1-mediated jasmonate signaling to promote disease development in Arabidopsis. Plant J 58:927–939. https://doi.org/10.1111/j.1365-313X.2009.03831.x
van der Ent S, Koornneef A, Ton J, Pieterse CMJ (2009a) Induced resistance—orchestrating defence mechanisms through crosstalk and priming. Annu Plant Rev Mol Asp Plant Disease Resist 34:334–371. https://doi.org/10.1002/9781444301441.ch11
Van der Ent S, Van Wees SCM, Pieterse CMJ (2009b) Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70:1581–1588. https://doi.org/10.1016/j.phytochem.2009.06.009
van Hulten M, Pelser M, van Loon L, Pieterse C, Ton J (2006) Costs and benefits of priming for defense in Arabidopsis. Proc Natl Acad Sci USA 103:5602–5607. https://doi.org/10.1073/pnas.0510213103
van Lenteren JC, Bolckmans K, Köhl J, Ravensberg WJ, Urbaneja A (2018) Biological control using invertebrates and microorganisms: plenty of new opportunities. Biocontrol 63:39–59. https://doi.org/10.1007/s10526-017-9801-4
Van Loon LC, Bakker PAHM (2006) Root-associated bacteria inducing systemic resistance. In: Gnanamanickam SS (ed) Plant-associated bacteria. Springer, Dordrecht, pp 269–316. https://doi.org/10.1007/978-1-4020-4538-7_8
Van Peer R, Schippers B (1992) Lipopolysaccharides of plant-growth promoting Pseudomonas sp. strain WCS417r induce resistance in carnation to Fusarium wilt. Neth J Plant Pathol 98:129–139. https://doi.org/10.1007/BF01996325
Van Wees SC, Van der Ent S, Pieterse CM (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448. https://doi.org/10.1016/j.pbi.2008.05.005
Veenstra A, Rafudeen MS, Murray SL (2019) Trichoderma asperellum isolated from African maize seed directly inhibits Fusarium verticillioides growth in vitro. Eur J Plant Pathol 153(1):279–283
Viterbo A, Wiest A, Brotman Y, Chet I, Kenerley C (2007) The 18mer peptaibols from Trichoderma virens elicit plant defence responses. Mol Plant Pathol 8:737–746. https://doi.org/10.1111/j.1364-3703.2007.00430.x
Walters D, Heil M (2007) Costs and trade-offs associated with induced resistance. Physiol Mol Plant Pathol 71:3–17. https://doi.org/10.1016/j.pmpp.2007.09.008
Walters DR, Ratsep J, Havis ND (2013) Controlling crop diseases using induced resistance: challenges for the future. J Exp Bot 64:1263–1280. https://doi.org/10.1093/jxb/ert026
Weller DM (1988) Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu Rev Phytopathol 26:379–407. https://doi.org/10.1146/annurev.py.26.090188.002115
Wu Q, Sun R, Ni M, Yu J, Li Y, Yu C, Dou K, Ren J, Chen J (2017) Identification of a novel fungus, Trichoderma asperellum GDFS1009, and comprehensive evaluation of its biocontrol efficacy. PLoS ONE 12:1–20. https://doi.org/10.1371/journal.pone.0179957
Wu G, Liu Y, Xu Y, Zhang G, Shen Q, Zhang R (2018) Exploring elicitors of the beneficial rhizobacterium Bacillus amyloliquefaciens SQR9 to induce plant systemic resistance and their interactions with plant signaling pathways. Mol Plant Microbe Interact 31(5):560–567. https://doi.org/10.1094/MPMI-11-17-0273-R
Wyckhuys KAG, Bentley JW, Lie R, Nghiem LTP, Fredrix M (2018) Maximizing farm-level uptake and diffusion of biological control innovations in today’s digital era. Biocontrol 63:133–148. https://doi.org/10.1007/s10526-017-9820-1
Xie S, Jiang H, Ding T, Xu Q, Chai W, Cheng B (2018) Bacillus amyloliquefaciens FZB42 represses plant miR846 to induce systemic resistance via a jasmonic acid-dependent signalling pathway. Mol Plant Pathol 19:1612–1623. https://doi.org/10.1111/mpp.12634
Xiong W, Guo S, Jousset A, Zhao Q, Wu H, Li R, Kowalchuk GA, Shen Q (2017) Bio-fertilizer application induces soil suppressiveness against Fusarium wilt disease by reshaping the soil microbiome. Soil Biol Biochem 114:238–247
Xue C, Penton CR, Shen Z, Zhang R, Huang Q, Li R, Ruan Y, Shen Q (2015) Manipulating the banana rhizosphere microbiome for biological control of panama disease. Sci Rep 5:11124. https://doi.org/10.1038/srep11124
Yao H, Wu F (2010) Soil microbial community structure in cucumber rhizosphere of different resistance cultivars to fusarium wilt. FEMS Microbiol Ecol 72:456–463. https://doi.org/10.1111/j.1574-6941.2010.00859.x
Zhang N, He X, Zhang J, Raza W, Yang X-M, Ruan Y-Z, Shen Q-R, Huang Q-W (2014) Suppression of Fusarium wilt of banana with application of bio-organic fertilizers. Pedosphere 24(5):613–624
Zhang F, Chen C, Zhang F, Gao L, Liu J, Chen L, Fan X, Liu C, Zhang K, He Y, Chen C, Ji X (2017) Trichoderma harzianum containing 1-aminocyclopropane-1-carboxylate deaminase and chitinase improved growth and diminished adverse effect caused by Fusarium oxysporum in soybean. J Plant Physiol 210:84–94. https://doi.org/10.1016/j.jplph.2016.10.012
Acknowledgements
This work is partially supported by grants from the NSFC (No. 31671702, No. 31471508), the National Key Research and Development Program of China (No. 2016YFD0101002), the Technology Foundation for Selected Overseas Chinese Scholar, Ministry of Personnel of China (No. G0101500090), and the Innovation Team Program for Jiangsu Universities (2014).
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Nguvo, K.J., Gao, X. Weapons hidden underneath: bio-control agents and their potentials to activate plant induced systemic resistance in controlling crop Fusarium diseases. J Plant Dis Prot 126, 177–190 (2019). https://doi.org/10.1007/s41348-019-00222-y
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DOI: https://doi.org/10.1007/s41348-019-00222-y