The impact of microbes in the orchestration of plants’ resistance to biotic stress: a disease management approach

Matthew Chekwube Enebe1, Olubukola Oluranti Babalola1
1Food Security and Safety Niche Area, Faculty of Natural and Agricultural Sciences, North-West University, Private Bag X2046, Mmabatho, 2735, South Africa

Tóm tắt

Từ khóa


Tài liệu tham khảo

Adam M, Heuer H, Hallmann J (2014) Bacterial antagonists of fungal pathogens also control root-knot nematodes by induced systemic resistance of tomato plants. PLoS One 9(2):e90402. https://doi.org/10.1371/journal.pone.0090402

Akram W, Anjum T, Ali B (2016) Phenylacetic acid is ISR determinant produced by Bacillus fortis iags162, which involves extensive re-modulation in metabolomics of tomato to protect against Fusarium wilt. Front Plant Sci 7:498. https://doi.org/10.3389/fpls.2016.00498

Ali S, Mir ZA, Tyagi A, Mehari H, Meena RP, Bhat JA, Yadav P, Papalou P, Rawat S, Grover A (2017) Overexpression of npr1 in Brassica juncea confers broad spectrum resistance to fungal pathogens. Front Plant Sci 8:1693. https://doi.org/10.3389/fpls.2017.01693

Arseneault T, Goyer C, Filion M (2015) Pseudomonas fluorescens LBUM223 increases potato yield and reduces common scab symptoms in the field. Phytopathol 105:1311–1317

Asari S, Ongena M, Debois D, De Pauw E, Chen K, Bejai S, Meijer J (2017) Insights into the molecular basis of biocontrol of Brassica pathogens by Bacillus amyloliquefaciens UCMB5113 lipopeptides. Ann Bot 120:551–562. https://doi.org/10.1093/aob/mcx089

Ashwin NMR, Barnabas EL, Ramesh Sundar A, Muthumeena M, Malathi P, Viswanathan R (2017) Disease suppressive effects of resistance-inducing agents against red rot of sugarcane. Eur J Plant Pathol 149:285–297. https://doi.org/10.1007/s10658-017-1181-1

Ashwin NMR, Barnabas L, Ramesh Sundar A, Malathi P, Viswanathan R, Masi A, Agrawal GK, Rakwal R (2018) CfPDIP1, a novel secreted protein of Colletotrichum falcatum, elicits defense responses in sugarcane and triggers hypersensitive response in tobacco. Appl Microbiol Biotechnol pp. 1 – 21. doi: https://doi.org/10.1007/s00253-018-9009-2 , 102, 6021

Babalola OO (2010) Beneficial bacteria of agricultural importance. Biotechnol Lett 32(11):1559–1570

Babalola OO (2014) Does nature make provision for backups in the modification of bacterial community structures? Biotech Genetic Eng Rev 30(1):31–48. https://doi.org/10.1080/02648725.2014.921497

Bán R, Baglyas G, Virányi F, Barna B, Posta K, Kiss J, Körösi K (2017) The chemical inducer, BTH (benzothiadiazole) and root colonization by mycorrhizal fungi (Glomus spp.) trigger resistance against white rot (Sclerotinia Sclerotiorum) in sunflower. Acta Biol Hung 68(1):50–59. https://doi.org/10.1556/018.68.2017.1.5

Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486

Berendsen RL, Vismans G, Yu K, Song Y, de Jonge R, Burgman WP, Burmolle M, Herschend J, Bakker PAHM, Pieterse CMJ (2018) Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME J 12:1496–1507

Blainski JML, da Rocha Neto AC, Schimidt EC, Voltolini JA, Rossi MJ, Di Piero RM (2018) Exopolysaccharides from Lactobacillus plantarum induce biochemical and physiological alterations in tomato plant against bacterial spot. Appl Microbiol Biotechnol 1–13. https://doi.org/10.1007/s00253-018-8946-0 , 102

Böhm H, Albert I, Fan L, Reinhard A, Nürnberger T (2014) Immune receptor complexes at the plant cell surface. Curr Opin Plant Biol 20C:47–54. https://doi.org/10.1016/j.pbi.2014.04.007

Bu B, Qiu D, Zeng H, Guo L, Yuan J, Yang X (2014) A fungal protein elicitor PevD1 induces Verticillium wilt resistance in cotton. Plant Cell Rep 33:461–470. https://doi.org/10.1007/s00299-013-1546-7

Caarls L, Elberse J, Awwanah M, Ludwig NR, de Vries M, Zeilmaker T, Van Wees SCM, Schuurink RC, den Ackerveken GV (2017) Arabidopsis jasmonate-induced oxygenases down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid. PNAS pp. 1–6. https://doi.org/10.1073/pnas.1701101114

Cao H, Bowling SA, Gordon AS, Dong X (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583–1592. https://doi.org/10.1105/tpc.6.11.1583

Cawoy H, Mariutto M, Henry G, Fisher C, Vasilyeva N, Thonart P, Dommes J, Ongena M (2014) Plant defense stimulation by natural isolates of Bacillus depends on efficient surfactin production. Mol Plant Microbe Interac 27(2):87–100. https://doi.org/10.1094/MPMI-09-13-0262-R

Cecchini NM, Steffes K, Schlappi MR, Gifford AN, Greenberg JT (2015) Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming. Nature Commun 6:7658. https://doi.org/10.1038/ncomms8658

Chang Y-H, Yan H-Z, Liou R-F (2014) A novel elicitor protein from Phytophthora parasitica induces plant basal immunity and systemic acquired resistance. Mol Plant Pathol pp. 1–14. https://doi.org/10.1111/mpp.12166

Chen Y, Dong J, Bennetzen JL, Zhong M, Yang J, Zhang J, Li S, Hao X, Zhang Z, Wang X (2017) Integrating transcriptome and microRNA analysis identifies genes and microRNAs for AHO-induced systemic acquired resistance in N. tabacum. Scientific Rep 7:12504. Doi: https://doi.org/10.1038/s41598-017-12249-y

Clark KB (2013) Biotic activity of Ca2+ - modulating non-traditional antimicrobial and -viral agents. Front Microbiol 4:381

Constantino NN, Mastouri F, Damarwinasis R, Borrego JE, Moran-Diez ME, Kenerley CM, Gao X, Kolomiets MV (2013) Root-expressed maize lipoxygenase 3 negatively regulates induced systemic resistance to Colletotrichum graminicola in shoots. Front Plant Sci 4(510):1–12. https://doi.org/10.3389/fpls.2013.00510

Crouzet J, Roland J, Peeters E, Trombik T, Ducos E, Nader J, Boutry M (2013) NtPDR1, a plasma membrane ABC transporter from Nicotiana tabacum, is involved in diterpene transport. Plant Mol Biol 82:181–192

D’Alessandro M, Erb M, Ton J, Brandenburg A, Karlen D, Zopfi J, Turlings TCJ (2014) Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions. Plant Cell Environ 37(4):813–826. https://doi.org/10.1111/pce.12220

Dey S, Wenig M, Langen G, Sharma S, Kugler KG, Knappe C, Hause B, Bichlmeier M, Babaeizad V, Imani J, Janzik I, Stempfl T, Hückelhoven R, Kogel K-H, Mayer KFX, Corina Vlot A (2014) Bacteria-triggered systemic immunity in barley is associated with WRKY and ethylene responsive factors but not with salicylic acid1[C][W]. Plant Physiol 166:2133–2151

Ding T, Su B, Chen X, Xie S, Gu S, Wang Q, Huang D, Jiang H (2017) An endophytic bacterial strain isolated from Eucommia ulmoides inhibits southern corn leaf blight. Front Microbiol 8:903. https://doi.org/10.3389/fmicb.2017.00903

Dos Santos PJC, Savi DC, Gomes RR, Goulin EH, Senkiv CDC, Tanaka FAO, Almeida ÁMR, Galli-Terasawa L, Kava V, Glienke C (2016) Diaporthe endophytica and D. terebinthifolii from medicinal plants for biological control of Phyllosticta citricarpa. Microbiol Res 186–187:153–160

Downie JA (2014) Calcium signals in plant immunity: a spiky issue. New Phytol 204:733–735

Egel DS, Kleczewski NM, Mumtaz F, Foster R (2018) Acibenzolar-S-methyl is associated with yield reduction when used for managing bacterial wilt (Erwinia tracheiphila) in cantaloupe. Crop Prot 109:136–141

El-Borollosy AM, Oraby MM (2012) Induced systemic resistance against cucumber mosaic cucumovirus and promotion of cucumber growth by some plant growth-promoting rhizobacteria. Ann Agric Sci 57(2):91–97

El-Shetehy M, Wang C, Shine MB, Yu K, Kachroo A, Kachroo P (2015) Nitric oxide and reactive oxygen species are required for systemic acquired resistance in plants. Plant Signal Behav 10(9):e998544

Farace G, Fernandez O, Jacquens L, Coutte F, Krier F, Jacques P, Clement C, Barka EA, Jacquard C, Dorey S (2014) Cyclic lipopeptides from Bacillus subtilis activate distinct patterns of defence responses in grapevine. Mol Plant Pathol 16:1–11. https://doi.org/10.1111/mpp.12170

Fatima S, Anjum T (2017) Identification of a potential ISR determinant from Pseudomonas aeruginosa PM12 against Fusarium wilt in tomato. Front Plant Sci 8:848. https://doi.org/10.3389/fpls.2017.00848

Fernández-Crespo E, Scalschi L, Llorens E, García-Agustín P, Camañes G (2015) NH4 + protects tomato plants against Pseudomonas syringae by activation of systemic acquired acclimation. J Exp Bot 66(21):6777–6790. https://doi.org/10.1093/jxb/erv382

Ferraz HB, Bertolucci PH, Pereira JS, Lima JG, Andrade LA (1988) Chronic exposure to the fungicide maneb may produce symptoms and signs of CNS manganese intoxication. Neurol 38:550–553

Figueredo MS, Tonelli ML, Ibánez F, Morla F, Cerioni G, Tordable MC, Fabra A (2017) Induced systemic resistance and symbiotic performance of peanut plants challenged with fungal pathogens and co-inoculated with the biocontrol agent Bacillus sp. CHEP5 and Bradyrhizobium sp. SEMIA6144. Microbiol Res 197:65–73

Fujita M, Kusajima M, Okumura Y, Nakajima M, Minamisawa K, Nakashita H (2017) Effects of colonization of a bacterial endophyte, Azospirillum sp. B510, on disease resistance in tomato. Biosci Biotechnol Biochem : https://doi.org/10.1080/09168451.2017.1329621

Fukami J, Ollero FJ, Megías M, Hungria M (2017) Phytohormones and induction of plant-stress tolerance and defense genes by seed and foliar inoculation with Azospirillum brasilense cells and metabolites promote maize growth. AMB Express 7:153. https://doi.org/10.1186/s13568-017-0453-7

Fukasawa-Akada T, Kung S, Watson JA (1996) Phenylalanine ammonia lyase gene structure, expression, and evolution in Nicotiana. Plant Mol Biol 30:711–722

Ghazalibiglar H, Hampton JG, de Jong EvZ, Holyoake A (2016) Is induced systemic resistance the mechanism for control of black rot in Brassica oleracea by a Paenibacillus sp.? Biol Control 92:195–201

Glaeser SP, Imani J, Alabid I, Guo H, Kumar N, Kämpfer P, Hardt M, Blom J, Goesmann A, Rothballer M, Hartmann A, Kogel K-H (2016) Non-pathogenic Rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica. ISME J 10:871–884

Gond SK, Bergen MS, Torres MS, White Jr JF (2015) Endophytic Bacillus spp. produce antifungal lipopeptides and induce host defence gene expression in maize. Microbiol Res 172:79–87

Gong C, Liu Y, S-y L, M-z C, Zhang Y, Wang R-h, H-y C, Li J-f, X-l C, A-x W (2017) Analysis of Clonostachys rosea-induced resistance to grey mould disease and identification of the key proteins induced in tomato fruit. Postharvest Biol Technol 123:83–93

Gruau C, Trotel-Aziz P, Villaume S, Rabenoelina F, Clement C, Baillieul F, Aziz A (2015) Pseudomonas fluorescens PTA-CT2 triggers local and systemic immune response against Botrytis cinerea in grapevine. MPMI 28(10):1117–1129. https://doi.org/10.1094/MPMI-04-15-0092-R

Haidar R, Roudet J, Bonnard O, Dufour MC, Corio-Costet MF, Fert M, Gautier T, Deschamps A, Fermaud M (2016) Screening and modes of action of antagonistic bacteria to control the fungal pathogen Phaeomoniella chlamydospora involved in grapevine trunk diseases. Microbiol Res 192:172–184

Hammerschmidt R (1999) Induced disease resistance: how do induced plants stop pathogens? Physiol Mol Plant Pathol 55:77–84

Hammerschmidt R, Nuckles EM, Kuc J (1982) Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrichum lagenarium. Physiol Plant Pathol 20:73–83

Han Y, Luo Y, Qin S, Xi L, Wan B, Du L (2014) Induction of systemic resistance against tobacco mosaic virus by Ningnanmycin in tobacco. Pestic Biochem Physiol 111:14–18

Hariprasad P, Chandrashekar S, Brijesh Singh S, Niranjana SR (2013) Mechanisms of plant growth promotion and disease suppression by Pseudomonas aeruginosa strain 2apa. J Basic Microbiol 00:1–10. https://doi.org/10.1002/jobm.201200491

Heath MC (1998) Apoptosis, programmed cell death and the hypersensitive cell death. Eur J Plant Pathol 104:117–124

Herrera SD, Grossi C, Zawoznik M, Groppa MD (2016) Wheat seeds harbour bacterial endophytes with potential as plant growth promoters and biocontrol agents of Fusarium graminearum. Microbiol Res 186–187:37–43

Hong CE, Kwon SY, Park JM (2016) Biocontrol activity of Paenibacillus polymyxa AC-1 against Pseudomonas syringae and its interaction with Arabidopsis thaliana. Microbiol Res 185:13–21

Hsu C-K, Micallef SA (2017) Plant-mediated restriction of Salmonella enterica on tomato and spinach leaves colonized with Pseudomonas plant growth-promoting rhizobacteria. Int J Food Microbiol 259:1–6

Hu Z, Shao S, Zheng C, Sun Z, Shi J, Yu J, Qi Z, Shi K (2018) Induction of systemic resistance in tomato against Botrytis cinerea by N-decanoyl-homoserine lactone via jasmonic acid signaling. Planta 247:1217–1227. https://doi.org/10.1007/s00425-018-2860-7

Huot B, Yao J, Montgomery BL, He SY (2014) Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol Plant 7:1267–1287

Jiang C-H, Huang Z-Y, Xie P, Gu C, Li K, Wang D-C, Yu Y-Y, Fan Z-H, Wang C-J, Wang Y-P, Guo Y-H, Guo J-H (2015) Transcription factors WRKY70 and WRKY11 served as regulators in rhizobacterium Bacillus cereus AR156-induced systemic resistance to Pseudomonas syringae pv. Tomato DC3000 in Arabidopsis. J Exp Bot1–18. Doi: https://doi.org/10.1093/jxb/erv445 , 67, 157, 174

Kamatham S, Neela KB, Pasupulati AK, Pallu R, Singh SS, Gudipalli P (2016) Benzoylsalicylic acid isolated from seed coats of Givotia rottleriformis induces systemic acquired resistance in tobacco and Arabidopsis. Phytochem 126:11–22

Karimi E, Safaie N, Shams-Baksh M, Mahmoudi B (2016) Bacillus amyloliquefaciens SB14 from rhizosphere alleviates Rhizoctonia damping-off disease on sugar beet. Microbiol Res 192:221–230

Khare D, Choi H, Huh SU, Bassin B, Kim J, Martinoia E, Sohn KH, Paek K-H, Lee Y (2017) Arabidopsis ABCG34 contributes to defense against necrotrophic pathogens by mediating the secretion of camalexin. PNAS 114:1–9. https://doi.org/10.1073/pnas.1702259114

Kim J-S, Lee J, Lee C-H, Woo SY, Kang H, Seo S-G, Kim S-H (2015) Activation of pathogenesis-related genes by the rhizobacterium, Bacillus sp. JS, which induces systemic resistance in tobacco plants. Plant Pathol J 31(2):195–201

Kong HG, Shin TS, Kim TH, Ryu C-M (2018) Stereoisomers of the bacterial volatile compound 2,3-Butanediol differently elicit systemic defense responses of pepper against multiple viruses in the field. Front Plant Sci 9:90. https://doi.org/10.3389/fpls.2018.00090

Kusajima M, Okumura Y, Fujita M, Nakashita H (2017) Abscisic acid modulates salicylic acid biosynthesis for systemic acquired resistance in tomato. Biosci Biotechnol Biochem 81:1850–1853. https://doi.org/10.1080/09168451.2017.1343121

Lai Y-R, Lin P-Y, Chen C-Y, Huang C-J (2016) Feasible management of southern corn leaf blight via induction of systemic resistance by Bacillus cereus C1L in combination with reduced use of dithiocarbamate fungicides. Plant Pathol J 32(5):481–488. https://doi.org/10.5423/PPJ.OA.02.2016.0044

Lai J, Cao X, Yu T, Wang Q, Zhang Y, Zheng X, Lu H (2018) Effect of Cryptococcus laurentii on inducing disease resistance in cherry tomato fruit with focus on the expression of defense-related genes. Food Chem 254:208–216

Lamdan N-L, Shalaby S, Ziv T, Kenerley CM, Horwitz BA (2015) Secretome of Trichoderma interacting with maize roots: role in induced systemic resistance. Mol Cell Proteomics 14:1054–1063. https://doi.org/10.1074/mcp.M114.046607

Lee BD, Dutta S, Ryu H, Yoo S-J, Suh D-S, Park K (2015) Induction of systemic resistance in Panax ginseng against Phytophthora cactorum by native Bacillus amyloliquefaciens HK34. J Ginseng Res 39:213–220

Lee G, Lee S-H, Kim KM, Ryu C-M (2017) Foliar application of the leaf-colonizing yeast Pseudozyma churashimaensis elicits systemic defense of pepper against bacterial and viral pathogens. Sci Rep 7:39432. https://doi.org/10.1038/srep39432

Li CY, Hu WC, Pan B, Liu Y, Yuan SF, Ding YY, Li R, Zheng XY, Shen B, Shen QR (2017) Rhizobacterium Bacillus amyloliquefaciens strain SQRT3-mediated induced systemic resistance controls bacterial wilt of tomato. Pedosphere 27(6):1135–1146

Li Y, Li Q, Hong Q, Lin Y, Mao W, Zhou S (2018) Reactive oxygen species triggering systemic programmed cell death process via elevation of nuclear calcium ion level in tomatoes resisting tobacco mosaic virus. Plant Sci 270:166–175

Liang Y, Cui S, Tang X, Zhang Y, Qiu D, Zeng H, Guo L, Yuan J, Yang X (2018) An asparagine-rich protein Nbnrp1 modulate Verticillium dahliae protein PevD1-induced cell death and disease resistance in Nicotiana benthamiana. Front Plant Sci 9:303. https://doi.org/10.3389/fpls.2018.00303

Linlin L, Peng G, Hua J, Tianlai L (2016) Different proteomics of Ca2+ on SA-induced resistance to Botrytis cinerea in tomato. Hortic Plant J 2(3):154–162

Liu J-J, Williams H, Li XR, Schoettle AW, Sniezko RA, Murray M, Zamany A, Roke G, Chen H (2017) Profiling methyl jasmonate-responsive transcriptome for understanding induced systemic resistance in whitebark pine (Pinus albicaulis). Plant Mol Biol Doi 95:359–374. https://doi.org/10.1007/s11103-017-0655-z

Lopez-Gresa MP, Lison P, Yenush L, Conejero V, Rodrigo I, Belles JM (2016) Salicylic acid is involved in the basal resistance of tomato plants to citrus exocortis viroid and tomato spotted wilt virus. PLoS One 11(11):e0166938. https://doi.org/10.1371/journal.pone.0166938

Lu F, Liang X, Lu H, Li Q, Chen Q, Zhang P, Li K, Liu G, Yan W, Song J, Duan C, Zhang L (2017) Overproduction of superoxide dismutase and catalase confers cassava resistance to Tetranychus cinnabarinus. Sci Rep 7:40179. https://doi.org/10.1038/srep40179

Lucas JA, García-Cristobal J, Bonilla A, Ramos B, Gutierrez-Manero J (2014) Beneficial rhizobacteria from rice rhizosphere confers high protection against biotic and abiotic stress inducing systemic resistance in rice seedlings. Plant Physiol Biochem 82:44–53

Luiz C, Rocha Neto AC, Di Piero RM (2015) Resistance to Xanthomonas gardneri in tomato leaves induced by polysaccharides from plant or microbial origin. J Plant Pathol 97(1):119–127. https://doi.org/10.4454/JPP.V97I1.029

Ma Z, Ongena M, Hofte M (2017) The cyclic lipopeptide orfamide induces systemic resistance in rice to Cochliobolus miyabeanus but not to Magnaporthe oryzae. Plant Cell Rep 36:1731–1746. https://doi.org/10.1007/s00299-017-2187-z

Malfanova N, Lugtenberg BJJ, Berg G (2013) Bacterial endophytes: who and where, and what are they doing there. In: deBruijn, F.J. (ed.), molecular microbial ecology of the rhizosphere. Wiley-Blackwell Hoboken, NJ, USA, p. 391–403

Martínez-Hidalgo P, García JM, Pozo MJ (2015) Induced systemic resistance against Botrytis cinerea by Micromonospora strains isolated from root nodules. Front Microbiol 6:922. https://doi.org/10.3389/fmicb.2015.00922

Martınez-Medina A, Fernandez I, Lok GB, Pozo MJ, Pieterse CMJ, Van Wees SCM (2016) Shifting from priming of salicylic acid- to jasmonic acid-regulated defences by Trichoderma protects tomato against the root knot nematode Meloidogyne incognita. New Phytol 213:1363–1377. https://doi.org/10.1111/nph.14251

Mauch F, Mauch-Mani B, Boller T (1988) Antifungal hydrolases in pea tissue: II. Inhibition of fungal growth by combinations of chitinase and β-1.3-glucanase. Plant Physiol 88:936–942

Meco G, Bonifati V, Vanacore N, Fabrizio E (1994) Parkinsonism after chronic exposure to the fungicide maneb (manganese ethylene-bis-dithiocarbamate). Scand J Work Environ Health 20:301–305

Miliute I, Buzaite O, Baniulis D, Stanys V (2015) Bacterial endophytes in agricultural crops and their role in stress tolerance: a review. Zemdirbyste-Agriculture 102(4):465–478

Mishra AK, Morang P, Deka M, Kumar NS, Kumar DBS (2014) Plant growth-promoting rhizobacterial strain-mediated induced systemic resistance in tea (Camellia sinensis (l.) o. kuntze) through defense-related enzymes against brown root rot and charcoal stump rot. Appl Biochem Biotechnol 174:506–521. https://doi.org/10.1007/s12010-014-1090-0

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(3):255–264

Nair A, Kolet SP, Thulasiram HV, Bhargava S (2014) Systemic jasmonic acid modulation in mycorrhizal tomato plants and its role in induced resistance against Alternaria alternata. Plant Biol pp. 1–7. https://doi.org/10.1111/plb.12277

Nanda AK, Andrio E, Marino D, Pauly N, Dunand C (2010) Reactive oxygen species during plant-microorganism early interactions. J Integr Plant Biol 52:195–204

Nassar AMK, Adss IAA (2016) 2,4-Dichlorophenoxy acetic acid, abscisic acid, and hydrogen peroxide induced resistance-related components against potato early blight (Alternaria solani, Sorauer). Ann Agri Sci 61(1):15–23

Naveed M, Qureshi MA, Zahir ZA, Hussain MB, Sessitsch A, Mitter B (2015) L – Tryptophan-dependent biosynthesis of indole-3-acetic acid (IAA) improves plant growth and colonization of maize by Burkholderia phytofirmans PsJN. Ann Microbiol 65:1391–1389

Nawrocka J, Małolepsza U, Szymczak K, Szczech M (2018) Involvement of metabolic components, volatile compounds, PR proteins, and mechanical strengthening in multilayer protection of cucumber plants against Rhizoctonia solani activated by Trichoderma atroviride TRS25. Protoplasma 255:359–373. https://doi.org/10.1007/s00709-017-1157-1

Naznin HA, Kiyohara D, Kimura M, Miyazawa M, Shimizu M, Hyakumachi M (2014) Systemic resistance induced by volatile organic compounds emitted by plant growth-promoting fungi in Arabidopsis thaliana. PLoS One 9(1):e86882. https://doi.org/10.1371/journal.pone.0086882

Nie P, Li X, Wang S, Guo J, Zhao H, Niu D (2017) Induced systemic resistance against Botrytis cinerea by Bacillus cereus AR156 through a JA/ET- and NPR1-dependent signaling pathway and activates PAMP-triggered immunity in arabidopsis. Front Plant Sci 8:238. https://doi.org/10.3389/fpls.2017.00238

Niu D, Wang X, Wang Y, Song X, Wang J, Guo J, Zhao H (2016) Bacillus cereus AR156 activates PAMP-triggered immunity and induces a systemic acquired resistance through a NPR1-and SA-dependent signaling pathway. Biochem Biophys Res Commun 469:120–125

O’hanlon KA, Knorr K, Jorgensesn LN, Nicolaisen M, Boelt B (2012) Exploring the potential of symbiotic fungal endophytes in cereal disease suppression. Biol Control 63:69–78

Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521

Pieterse CMJ, Zamioudis CBRL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375

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(719):1–10. https://doi.org/10.3389/fpls.2014.00719

Raaijmakers JM, Mazzola M (2016) Soil immune responses. Sci 352:1392–1393

Rais A, Jabeen Z, Shair F, Hafeez FY, Hassan MN (2017) Bacillus spp., a bio-control agent enhances the activity of antioxidant defense enzymes in rice against Pyricularia oryzae. PLoS One 12(11):e0187412. https://doi.org/10.1371/journal.pone.0187412

Raut SA, Borkar SG (2014) PR-proteins accumulation in tomato plant due to application of resistance inducing chemicals during period of induced resistance against Alternaria leaf blight. Sci Int J 2:72–75

Raza W, Yousaf S, Rajer FU (2016) Plant growth promoting activity of volatile organic compounds produced by biocontrol strains. Sci Lett 4:40–43

Salas-Marina MA, Isordia-Jasso MI, Islas-Osuna MA, Delgado-Sánchez P, Jiménez-Bremont JF, Rodríguez-Kessler M, Rosales-Saavedra MT, Herrera-Estrella A, Casas-Flores S (2015) The Epl1 and Sm1 proteins from Trichoderma atroviride and Trichoderma virens differentially modulate systemic disease resistance against different life style pathogens in Solanum lycopersicum. Front Plant Sci 6(77):1–13

Santhanam R, Luu VT, Weinhold A, Goldberg J, Oh Y, Baldwin IT (2015) Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping. PNAS pp. 1–8. https://doi.org/10.1073/pnas.1505765112

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 6:35543. https://doi.org/10.1038/srep35543

Sharma CK, Vishnoi VK, Dubey RC, Maheshwari DK (2018) A twin rhizospheric bacterial consortium induces systemic resistance to a phytopathogen Macrophomina phaseolina in mung bean. Rhizosphere 5:71–75

Shine MB, Xiao X, Kachroo P, Kachroo A (2018) Signaling mechanisms underlying systemic acquired resistance to microbial pathogens. Plant Sci : https://doi.org/10.1016/j.plantsci.2018.01.001

Singh UB, Malviya D, Wasiullah Singh S, Pradhan JK, Singh BP, Roy M, Imram M, Pathak N, Baisyal BM, Rai JP, Sarma BK, Singh RK, Sharma PK, Kaur SD, Manna MC, Sharma SK, Sharma AK (2016) Bio-protective microbial agents from rhizosphere eco-systems trigger plant defense responses provide protection against sheath blight disease in rice (Oryza sativa L.). Microbiol Res 192:300–312

Song GC, Ryu CM (2013) Two volatile organic compounds trigger plant self-defense against a bacterial pathogen and a sucking insect in cucumber under open field conditions. Int J Mol Sci 14:9803–9819

Song Y, Chen D, Lu K, Sun Z, Zeng R (2015) Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Front Plant Sci 6:786. https://doi.org/10.3389/fpls.2015.00786

Spence C, Alff E, Johnson C, Ramos C, Donofrio N, Sundaresan V, Bais H (2014) Natural rice rhizospheric microbes suppress rice blast infections. BMC Plant Biol 14:130

Srikantaramas S, Yamazaki M, Saito K (2008) Mechanisms of resistance to self-produced toxic secondary metabolites in plants. Phytochem Rev 7:467–477

Stamler RA, Holguin O, Dungan B, Schaub T, Sanogo S, Goldberg N, Randall JJ (2015) BABA and Phytophthora nicotianae induce resistance to Phytophthora capsici in Chile pepper (Capsicum annuum). PLoS One 10(5):e0128327. https://doi.org/10.1371/journal.pone.0128327

Stangarlin JR, Kuhn OJ, Toledo MV, Portz RL, Schwan-Estrada KRF, Pascholati SF (2011) A defesa vegetal contra fitopatógenos. Sci Agrar Paranaen 10(1):18–46

Su F, Villaume S, Rabenoelina F, Crouzet J, Clément C, Vaillant-Gaveau N, Dhondt-Cordelier S (2017a) Different Arabidopsis thaliana photosynthetic and defense responses to hemibiotrophic pathogen induced by local or distal inoculation of Burkholderia phytofirmans. Photosynth Res 134(2):201–214. https://doi.org/10.1007/s11120-017-0435-2

Su P, Tan X, Li C, Zhang D, Cheng J, Zhang S, Zhou X, Yan Q, Peng J, Zhang Z, Liu Y, Lu X (2017b) Photosynthetic bacterium Rhodopseudomonas palustris GJ-22 induces systemic resistance against viruses. Microbial Biotechnol 10:612–624

Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008) Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–956. https://doi.org/10.1126/science.1156970

Tahir HAS, Gu Q, Wu H, Raza W, Safdar A, Huang Z, Rajer FU, Gao X (2017) Effect of volatile compounds produced by Ralstonia solanacearum on plant growth promoting and systemic resistance inducing potential of Bacillus volatiles. BMC Plant Biol 17:133. https://doi.org/10.1186/s12870-017-1083-6

Tonelli ML, Fabra A (2014) The biocontrol agent Bacillus sp. CHEP5 primes the defense response against Cercospora sojina. World J Microbiol Biotechnol pp.1–7. Doi: https://doi.org/10.1007/s11274-014-1675-3 , 30, 2503, 2509

Tonelli ML, Magallanes-Noguera C, Fabra A (2017) Symbiotic performance and induction of systemic resistance against Cercospora sojina in soybean plants co-inoculated with Bacillus sp. CHEP5 and Bradyrhizobium japonicum E109. Arch Microbiol 199:1283–1291. https://doi.org/10.1007/s00203-017-1401-2

Toyota M, Spencer D, Sawai-Toyota S, Jiaqi W, Zhang T, Koo AJ, Howe GA, Gilroy S (2018) Glutamate triggers long-distance, calcium-based plant defense signaling. Sci 361:1112–1115

Vacheron J, Renoud S, Muller D, Babalola OO, Prigent-Combaret C (2015) Alleviation of abiotic and biotic stresses in plants by Azospirillum. In: Cassain FD et al., (eds), Handbook for Azospirillum, Technical issues and protocol, Springer international publishing Switzerland, pp. 333–365

Van Lelyveld LJ, Brodrick HT (1975) Enzymic responses of avocado leaves to Phytophthora root rot. Agroplantae 7:13–16

Vanitha SC, Niranjana SR, Umesha S (2009) Role of phenylalanine ammonia lyase and polyphenol oxidase in host resistance to bacterial wilt of tomato. J Phytopathol 157:552–557

Velivelli SLS, Lojan P, Cranenbrouck S, de Boulois HD, Suarez JP, Declerck S, Franco J, Prestwich BD (2015) The induction of ethylene response factor 3 (ERF3) in potato as a result of co-inoculation with Pseudomonas sp. R41805 and Rhizophagus irregularis MUCL 41833—a possible role in plant defense. Plant Signal Behav 10(2):e988076

Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Woo SL, Lorito M (2008) Trichoderma–plant–pathogen interactions. Soil Biol Biochem 40:1–10

Vitti A, La Monaca E, Sofo A, Scopa A, Cuypers A, Nuzzaci M (2015) Beneficial effects of Trichoderma harzianum T-22 in tomato seedlings infected by cucumber mosaic virus (CMV). BioControl 60:135–147. https://doi.org/10.1007/s10526-014-9626-3

Walley JW, Shen Z, McReynolds MR, Schmelz EA, Briggs SP (2018) Fungal-induced protein hyperacetylation in maize identified by acetylome profiling. PNAS pp. 1 – 6. www.pnas.org/cgi/doi/10.1073/pnas.1717519115 , 115, 215

Wang N, Liu M, Guo L, Yang X, Qiu D (2016) A novel protein elicitor (PeBA1) from Bacillus amyloliquefaciens NC6 induces systemic resistance in tobacco. Int J Biol Sci 12(6):757–767. https://doi.org/10.7150/ijbs.14333

Wei Y, Xu M, Wu H, Tu S, Pan L, Tu K (2016) Defense response of cherry tomato at different maturity stages to combined treatment of hot air and Cryptococcus laurentii. Postharvest Biol Technol 117:177–186

Xu QT, Fan HY, Jiang Z, Zhou ZQ, Yang L, Mei FZ, Qu LH (2013) Cell wall degradation and the dynamic changes of Ca2+ and related enzymes in the developing aerenchyma of wheat (Triticum aestivum L.) under waterlogging. Acta Biol Hung 64:328–340

Yan Y, Tang L, Hu J, Wang J, Adelakun TA, Yang D, Di Y, Zhang Y, Hao X (2018) Munronin O, a potential activator for plant resistance. Pestic Biochem Physiol 146:13–18

Yoodee S, Kobayashi Y, Songnuan W, Boonchird C, Thitamadee S, Kobayashi I, Narangajavana J (2018) Phytohormone priming elevates the accumulation of defense-related gene transcripts and enhances bacterial blight disease resistance in cassava. Plant Physiol Biochem 122:65–77

Yu C, Fan L, Gao J, Wang M, Wu Q, Tang J, Li Y, Chen J (2015) The platelet-activating factor acetylhydrolase gene derived from Trichoderma harzianum induces maize resistance to Curvularia lunata through the jasmonic acid signaling pathway. J Environ Sci Health 50(10):708–717. https://doi.org/10.1080/03601234.2015.1048104

Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant-Microbe Interact 25:139–150

Zeng W, He SY (2010) A prominent role of the flagellin receptor flagellin-sensing2 in mediating stomatal response to Pseudomonas syringae pv tomato DC3000 in Arabidopsis. Plant Physiol 153(3):1188–1198

Zhang Y, Yan X, Guo H, Zhao F, Huang L (2018) A novel protein elicitor BAR11 from Saccharothrix yanglingensis Hhs.015 improves plant resistance to pathogens and interacts with catalases as targets. Front Microbiol 9:700. https://doi.org/10.3389/fmicb.2018.00700

Zheng X-Y, Zhou M, Yoo H, Pruneda-Paz JL, Spivey NW, Kay SA, Dong X (2015) Spatial and temporal regulation of biosynthesis of the plant immune signal salicylic acid. PNAS 112(30):9166–9173

Zhu F, Xi D-H, Yuan S, Xu F, Zhang D-W, Lin H-H (2014) Salicylic acid and jasmonic acid are essential for systemic resistance against tobacco mosaic virus in Nicotiana benthamiana. Mol Plant Microbe Interact 27(6):567–577. https://doi.org/10.1094/MPMI-11-13-0349-R