Skip to main content

Natural Agents Inducing Plant Resistance Against Pests and Diseases

  • Chapter
  • First Online:
Natural Antimicrobial Agents

Abstract

Plant resistance inducers, also referred to as elicitors, are agents that confer improved protection to pathogen or pest attacks by inducing host defense mechanisms. Such products are effective against a wide range of crop enemies, including viruses, bacteria, fungi, oomycetes, nematodes, and herbivores. The mode of action of these products differs from that of traditional pesticides because they do not target directly the bio-aggressor through antifungal activity, but they inhibit its development indirectly via the elicitation of plant defense reactions. In the current context of sustainable agriculture and growing demand for healthy food, plant resistance inducers are considered as an eco-friendly and promising alternative to conventional pesticides, and their implementation in integrated pest management strategy is strongly encouraged. Plant resistance inducers can be of synthetic or natural origin. This chapter will focus on resistance inducers of natural origin including living microorganisms, plant extracts, microbial cell-wall extracts, microbial metabolites, minerals, and ions. An overview on the market and recent advances on the regulation of these products as well as future challenges to promote their development and wide use in disease management programs will be described.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 99.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 129.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abdel-Mawgoud AM, Lépine F, Déziel E (2010) Rhamnolipids: Diversity of structures, microbial origins and roles. Appl Microbiol Biotechnol 86:1323–1336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abouraïcha E, El Alaoui-Talibi Z, El Boutachfaiti R, Petit E, Courtois B et al (2015) Induction of natural defense and protection against Penicillium expansum and Botrytis cinerea in apple fruit in response to bioelicitors isolated from green algae. Sci Hortic 181:121–128

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Agrawal GK, Rakwal R, Tamogami S, Yonekura M, Kubo A et al (2002) Chitosan activates defense/stress responses(s) in the leaves of Oryza staiva seedlings. Plant Physiol Biochem 40:1061–1069

    Article  CAS  Google Scholar 

  • Alexandersson E, Mulugeta T, Lankinen A, Liljeroth E, Andreasson E (2016) Plant resistance inducers against pathogens in solanaceae species - from molecular mechanisms to field application. Int J Mol Sci 17:1673

    Article  PubMed Central  CAS  Google Scholar 

  • Alkooranee JT, Yin Y, Aledan TR, Jiang Y, Lu G et al (2015) Systemic resistance to powdery mildew in Brassica napus (AACC) and Raphanus alboglabra (RRCC) by Trichoderma harzianum TH12. PlosOne 10(11):e0142177

    Article  CAS  Google Scholar 

  • Altenbach D, Robatzek S (2007) Pattern recognition receptors: from the cell surface to intracellular dynamics. Mol Plant Microbe Interact 20:1031–1039

    Article  CAS  PubMed  Google Scholar 

  • Andreu AB, Guevara MG, Wolski EA, Daleo GR, Caldiz DO (2006) Enhancement of natural disease resistance in potatoes by chemicals. Pest Manag Sci 62:162–170

    Article  CAS  PubMed  Google Scholar 

  • Arsenault-Labrecque G, Menzies JG, Bélanger RR (2012) Effect of silicon absorption on soybean resistance to Phakopsora pachyrhizi in different cultivars. Plant Dis 96:37–42

    Article  CAS  Google Scholar 

  • Arseneault T, Pieterse CMJ, Gérin-Ouellet M, Goyer C, Filion M (2014) Long-term induction of defense gene expression in potato by Pseudomonas sp. LBUM223 and Streptomyces scabies. Phytopathology 104:926–932

    Article  CAS  PubMed  Google Scholar 

  • Aziz A, Poinssot B, Daire X, Adrian M, Bezier A et al (2003) Laminarin elicits defense responses in grapevine and induces protection against Botrytis cinerea and Plasmopara viticola. Mol Plant Microbe Interact 16:1118–1128

    Article  CAS  PubMed  Google Scholar 

  • Aziz A, Trotel-Aziz P, Dhuicq L, Jeandet P, Couderchet M et al (2006) Chitosan oligomers and copper sulfate induce grapevine defense reactions and resistance to gray mold and downy mildew. Phytopathology 96:1188–1194

    Article  CAS  PubMed  Google Scholar 

  • Banani H, Roatti B, Ezzahi B, Giovannini O, Gessler G et al (2014) Characterization of resistance mechanisms activated by Trichoderma harzianum T39 and benzothiadiazole to downy mildew in different grapevine cultivars. Plant Pathol 63:334–343

    Article  CAS  Google Scholar 

  • Barriuso J, Ramos Solano B, Gutiérrez Mañero FJ (2008) Protection against pathogen and salt stress by four plant growth-promoting rhizobacteria isolated from Pinus sp. on Arabidopsis thaliana. Phytopathology 98:666–672

    Article  CAS  PubMed  Google Scholar 

  • Barton-Willis PA, Wang MC, Holliday MR, Long MR, Keen NT (1984) Purification and composition of lipopolysaccharides from Pseudomonas syringae pathovar syringae. Physiol Plant Pathol 25:387–398

    Article  CAS  Google Scholar 

  • Baysal-Gurel F, Miller SA (2015) Management of powdery mildew in greenhouse tomato production with biorational products and fungicides. Sci Hortic 1069:179–184

    Google Scholar 

  • Bengtsson M, Wulff E, Jørgensen HJL, Pham A, Lubeck M et al (2009) Comparative studies on the effects of a yucca extract and benzothiadiazole (BTH) on inhibition of Venturia inaequalis in apple leaves. Eur J Plant Pathol 124:187–198

    Article  CAS  Google Scholar 

  • Bengtsson T, Weighill D, Proux-Wéra E, Levander F, Resjö S et al (2014) Proteomics and transcriptomics of the BABA-induced resistance response in potato using a novel functional annotation approach. BMC Genom 15:315

    Article  CAS  Google Scholar 

  • Ben-Jabeur M, Ghabri E, Myriam M, Hamada W (2015) Thyme essential oil as a defense inducer of tomato against gray mold and Fusarium wilt. Plant Physiol Biochem 94:35–40

    Article  CAS  PubMed  Google Scholar 

  • Benouaret R, Goujon E, Trivella A, Richard C, Ledoigt G et al (2013) Water extracts from winery by-products as tobacco defense inducers. Ecotoxicology 23:1574–1581

    Article  CAS  Google Scholar 

  • Benouaret R, Goujon E, Goupil P (2014) Grape marc extract causes early perception events, defence reactions and hypersensitive response in cultured tobacco cells. Plant Physiol Biochem 77:84–89

    Article  CAS  PubMed  Google Scholar 

  • Bhaskara Reddy MV, Arul J, Angers P, Couture L (1999) Chitosan treatment of wheat seeds induces resistance to Fusarium graminearum and improves seed quality. J Agric Food Chem 47:1208–1216

    Article  CAS  PubMed  Google Scholar 

  • Bhuvaneshwari V, Paul PK (2012) Transcriptional and translational regulation of defense enzymes induced by neem fruit extract in tomato. Arch Phytopathol Plant Protect 45:1–12

    Article  CAS  Google Scholar 

  • Boeke SJ, Boersma MG, Alink GM, van Loon JJ, van Huis A et al (2004) Safety evaluation of neem (Azadirachta indica) derived pesticides. J Ethnopharmacol 94:25–41

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Borrayo E, Martinez-Pena MD, Morales-Valencia JA, Cortes-Cruz M, Arteaga-Garibay R (2013) Flagellin complete sequence as an inter-specific molecular phylogenetic marker among bacteria. Afr J Microbiol Res 7:701–703

    CAS  Google Scholar 

  • Bortesia L, Fischer R (2015) The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol Adv 33:41–52

    Article  CAS  Google Scholar 

  • Boubakri H, Chong J, Poutaraud A, Schmitt C, Bertsch C et al (2013a) Riboflavin (Vitamin B2) induces defence responses and resistance to Plasmopara viticola in grapevine. Eur J Plant Pathol 136:837–855

    Article  CAS  Google Scholar 

  • Boubakri H, Waha MA, Chong J, Gertz C, Gandour S et al (2013b) Methionine elicits H2O2 generation and defense gene expression in grapevine and reduces Plasmopara viticola infection. J Plant Physiol 170:1561–1568

    Article  CAS  PubMed  Google Scholar 

  • Burketova L, Trda L, Ott PG, Valentova O (2015) Bio-based resistance inducers for sustainable plant protection against pathogens. Biotechnol Adv 33:994–1004

    Article  CAS  PubMed  Google Scholar 

  • Burra D, Berkowitz O, Hedley PE, Morris J, Resjo S et al (2014) Phosphite-induced changes of the transcriptome and secretome in Solanum tuberosum leading to resistance against Phytophthora infestans. BMC Plant Biol 14:254

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Calo JR, Crandall PG, O’Bryan CA, Ricke SC (2015) Essential oils as antimicrobials in food systems-a review. Food Control 54:111–119

    Article  CAS  Google Scholar 

  • Cao HH, Zhang M, Zhao H, Zhang Y, Wang XX et al (2014) Deciphering the mechanism of β-aminobutyric acid-induced resistance in wheat to the grain aphid. Sitobion avenae. PLoS ONE 9(3):e91768

    Article  PubMed  CAS  Google Scholar 

  • Chandler S, Van Hese N, Coutte F, Jacques P, Höfte M et al (2015) Role of cyclic lipopeptides produced by Bacillus subtilis in mounting induced immunity in rice (Oryza sativa L.). Physiol Mol Plant Pathol 91:20–30

    Article  CAS  Google Scholar 

  • Chavan V, Kamble A (2013) β-Aminobutyric acid primed expression of WRKY and defence genes in Brassica carinata against alternaria blight. J Phytopathol 161:859–865

    Article  CAS  Google Scholar 

  • Che YZ, Li YR, Zou HS, Zou LF, Zhang B et al (2011) A novel antimicrobial protein for plant protection consisting of a Xanthomonas oryzae harpin and active domains of cecropin A and melittin. Microb Biotechnol 4:777–793

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen M, Zeng H, Qiu D, Guo L, Yang X et al (2012) Purification and characterization of a novel hypersensitive response-inducing elicitor from Magnaporthe oryzae that triggers defense response in rice. PLoS ONE 7(5):e37654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Takeda T, Aoki Y, Fujita K, Suzuki S et al (2014) Peptidoglycan from fermentation by product triggers defense responses in grapevine. PLoS ONE 9(11):e113340

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chowdhury SP, Uhl J, Grosch R, Alquéres S, Pittroff S et al (2015) Cyclic lipopeptides of Bacillus amyloliquefaciens subsp. plantarum colonizing the lettuce rhizosphere enhance plant defence responses towards the bottom rot pathogen Rhizoctonia solani. Mol Plant Microbe Interact 28:984–995

    Article  CAS  PubMed  Google Scholar 

  • Chung EJ, Hossain MT, Khan A, Kim KH, Jeon CO et al (2015) Bacillus oryzicola sp. nov., an endophytic bacterium isolated from the roots of rice with antimicrobial, plant growth promoting, and systemic resistance inducing activities in rice. Plant Pathol J 31:152–164

    Article  PubMed  PubMed Central  Google Scholar 

  • Cluzet S, Torregrosa C, Jacquet C, Lafitte C, Fournier J et al (2004) Gene expression profiling and protection of Medicago truncatula against a fungal infection in response to an elicitor from green algae Ulva spp. Plant, Cell Environ 27:917–928

    Article  CAS  Google Scholar 

  • Conceição CS, Felix KCS, Mariano RLR, Medeiros EV, Souza EB (2014) Combined effect of yeast and silicon on the control of bacterial fruit blotch in melon. Sci Hortic 174:164–170

    Article  CAS  Google Scholar 

  • Conrath U, Pieterse CM, Mauch-Mani B (2002) Priming in plant-pathogen interactions. Trends Plant Sci 7:210–216

    Article  CAS  PubMed  Google Scholar 

  • Cooper WR, Horton DR (2015) Effects of elicitor of host plant defenses on pear psylla, Cacopsylla pyricola. Entomol Exp Appl 157:300–306

    Article  CAS  Google Scholar 

  • Coqueiro DSO, de Souza AA, Takita MA, Rodrigues CM, Kishi LT et al (2015) Transcriptional profile of sweet orange in response to chitosan and salicylic acid. BMC Genom 16:288

    Article  CAS  Google Scholar 

  • Córdova-Campos O, Adame-Álvarez RM, Acosta-Gallegos JA, Heil M (2012) Domestication affected the basal and induced disease resistance in common bean (Phaseolus vulgaris). Eur J Plant Pathol 134:367–379

    Article  Google Scholar 

  • Cruz AF, Medeiros NL, Benedet GL, Araújo MB, Uesugi CH et al (2015) Control of post-harvest anthracnose infection in guava (Psidium guajava) fruits with phosphites, calcium chloride, acetyl salicylic acid, hot water, and 1-MCP. Hortic Environ Biote 56:330–340

    Article  CAS  Google Scholar 

  • Daayf F, Schmitt A, Belanger RR (1995) The effects of plants extracts of Reynoutria sachalinensis on powdery mildew development and leaf physiology of long English cucumber. Plant Dis 79:577–580

    Article  Google Scholar 

  • Daayf F, Schmitt A, Belanger RR (1997) Evidence of phytoalexins in cucumber leaves infected with powdery mildew-following treatment with leaf extracts of Reynoutria sachalinensis. Plant Physiol 113:719–727

    Article  PubMed  PubMed Central  Google Scholar 

  • Daayf F, Ongena M, Boulanger R, El Hadrami I, Bélanger RR (2000) Induction of phenolic compounds in two cultivars of cucumber by treatment of healthy and powdery mildew-infected plants with extracts of Reynoutria sachalinensis. J Chem Ecol 26:1579–1593

    Article  CAS  Google Scholar 

  • de Freitas MB, Ferreira LG, Hawerroth C, Duarte MER, Noseda MD et al (2015) Ulvans induce resistance against plant pathogenic fungi independently of their sulfation degree. Carbohydr Polym 133:384–390

    Article  PubMed  CAS  Google Scholar 

  • Denancé N, Sánchez-Vallet A, Goffner D, Molina A (2013) Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front Plant Sci 4:155

    Article  PubMed  PubMed Central  Google Scholar 

  • Deora A, Gossen BD, Walley F, McDonald MR (2011) Boron reduces development of clubroot in canola. Can J Plant Pathol 33:475–484

    Article  CAS  Google Scholar 

  • Deravel J, Lemière S, Coutte F, Krier F, VanHese N et al (2014) Mycosubtilin and surfactin are efficient, low ecotoxicity molecules for the biocontrol of lettuce downy mildew. Appl Microbiol Biotechnol 98:6255–6264

    Article  CAS  PubMed  Google Scholar 

  • Desaki Y, Otomo I, Kobayashi D, Jikumaru Y, Kamiya Y et al (2012) Positive crosstalk of MAMP signaling pathways in rice cells. PLoS ONE 7:e51953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dow M, Newman MA, von Roepenack E (2000) The induction and modulation of plant defense responses by bacterial lipolysaccharides. Annu Rev Phytopathol 38:241–261

    Article  CAS  PubMed  Google Scholar 

  • Duijff BJ, Gianinazzi-Pearson V, Lemanceau P (1997) Involvement of the outer membrane lipopolysaccharides in the endophytic colonization of tomato roots by biocontrol Pseudomonas fluorescens strain WCS417r. New Phytol 135:325–334

    Article  CAS  Google Scholar 

  • Dunham WC, Trimmer D (2015) Evolution and future of biocontrol. The global biocontrol and biostimulants E-newsletter. http://www.2bmonthly.com/wp-content/uploads/2015/11/Bill-Dunham-2BMonthly-Evolution-Future-of-Biocontrol-Industry-copy.pdf. Accessed 10 Nov 2016

  • Dworking J (2014) The medium is the message: interspecies and interkingdom signaling by peptidoglycan and related bacterial glycans. Ann Rev Microbiol 68:137–154

    Article  CAS  Google Scholar 

  • El Modafar C, Elgadda M, El Boutachfaiti R, Abouraicha E, Zehhar N et al (2012) Induction of natural defense accompanied by salicylic acid-dependant systemic acquired resistance in tomato seedlings in response to bioelicitors isolated from green algae. Sci Hortic 138:55–63

    Article  CAS  Google Scholar 

  • El-Hadrami A, Adam LR, El-Hadrami I, Daayf F (2010) Chitosan in plant protection. Mar Drugs 8:968–987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erbs G, Newmann MA (2003) The role of lipopolysaccharides in induction of plant defence responses. Mol Plant Pathol 4:421–425

    Article  CAS  PubMed  Google Scholar 

  • Erbs G, Silipo A, Aslam S, De Castro C, Liparoti V et al (2008) Peptidoglycan and muropeptides from pathogens Agrobacterium and Xanthomonas elicit plant innate immunity: structure and activity. Chem Biol 15:438–448

    Article  CAS  PubMed  Google Scholar 

  • Eshraghi L, Anderson J, Aryamanesh N, Shearer B, McComb J et al (2011) Phosphite primed defence responses and enhanced expression of defence genes in Arabidopsis thaliana infected with Phytophthora cinnamomi. Plant Pathol 60:1086–1095

    Article  CAS  Google Scholar 

  • Falcón-Rodríguez AB, Costales D, Cabrera JC, Martínez-Téllez MA (2011) Chitosan physico-chemical properties modulate defense responses and resistance in tobacco plant against the oomycete Phytophtora nicotianae. Pest Biochem Physiol 100:221–228

    Article  CAS  Google Scholar 

  • Faoro F, Maffi D, Cantu D, Iriti M (2008) Chemical-induced resistance against powdery mildew in barley: the effects of chitosan and benzothiadazole. Biocontrol 53:384–401

    Article  CAS  Google Scholar 

  • Farace G, Fernandez O, Jacquens L, Coutte F, Krier F et al (2015) Cyclic lipopeptides from Bacillus subtilis activate distinct patterns of defence responses in grapevine. Physiol Mol Plant Pathol 16:177–187

    Article  CAS  Google Scholar 

  • Felix G, Boller T (2003) Molecular sensing of bacteria in plants. The highly conserved RNA-binding motif RNP-1 of bacterial cold shock proteins is recognized as an elicitor signal in tobacco. J Biol Chem 278:6201–6208

    Article  CAS  PubMed  Google Scholar 

  • Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18:265–276

    Article  CAS  PubMed  Google Scholar 

  • Ferrari S, Galletti R, Denoux C, De Lorenzo G, Ausubel FM et al (2007) Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires phytoalexin deficient3. Plant Physiol 144:367–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferraz HGM, Resende RS, Silveira PR, Andrade CCL, Milagres EA et al (2014) Rhizobacteria induces resistance against Fusarium wilt of tomato by increasing the activity of defense enzymes. Bragantia, Campinas 73:274–283

    Article  Google Scholar 

  • Ferraz HGM, Resende RS, Moreira PC, Silveira PR, Milagres EA et al (2015) Antagonistic rhizobacteria and jasmonic acid induce resistance against tomato bacterial spot. Bragantia, Campinas 74:417–427

    Article  Google Scholar 

  • Ferreira HA, do Nascimento CWA, Datnoff LE, de Sousa Nunes GH, Preston W, et al (2015) Effects of silicon on resistance to bacterial fruit blotch and growth of melon. Crop Prot 78:277-283

    Google Scholar 

  • Floryszak-Wieczorek J, Arasimowicz-Jelonek M, Milczarek G, Janus L, Pawlak-Sprada S et al (2012) Nitric oxide-mediated stress imprint in potato as an effect of exposure to a priming agent. Mol Plant Microbe Interact 25:1469–1477

    Article  CAS  PubMed  Google Scholar 

  • Fofana B, McNally DJ, Labbe C, Boulanger R, Benhamou N et al (2002) Milsana-induced resistance in powdery mildew-infected cucumber plants correlates with the induction of chalcone synthase and chalcone isomerase. Physiol Mol Plant Pathol 61:121–132

    Article  CAS  Google Scholar 

  • Fotoohiyan Z, Rezaee S, Bonjar GHS, Mohammadi AH, Moradi M (2015) Induction of systemic resistance by Trichoderma harzianum isolates in pistachio plants infected with Verticillium dahliae. J Nuts 6:95–111

    Google Scholar 

  • Fousia S, Paplomatas EJ, Tjamos SE (2015) Bacillus subtilis QST 713 confers protection to tomato plants against Pseudomonas syringae pv tomato and induces plant defence-related genes. J Phytopathol 164:264–270

    Article  CAS  Google Scholar 

  • Frenkel O, Yermiyahu U, Forbes GA, Fry WE, Shtienberg D (2010) Restriction of potato and tomato late blight development by sub-phytotoxic concentrations of boron. Plant Pathol 59:626–633

    Article  CAS  Google Scholar 

  • Garcion C, Lamotte O, Cacas JL, Métraux JP (2014) Mechanisms of defence to pathogens: biochemistry and physiology. In: Walters DR, Newton AC, Lyon GD (eds) Induced resistance for plant defence: A sustainable approach to crop protection. Blackwell Publishing Ltd, Oxford, pp 106–136

    Google Scholar 

  • Gauthier A, Trouvelot S, Kelloniemi J, Frettinger P, Wendehenne D et al (2014) The sulfated laminarin triggers a stress transcriptome before priming the SA- and ROS-dependent defenses during grapevine’s induced resistance against Plasmopara viticola. PLoS ONE 9(2):e88145

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ghazalibiglar H, Hampton JG, van Zijll de Jong E, 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

    Google Scholar 

  • Ghazanfar MU, Wakil W, Sahi ST (2011) Induction of resistance in chickpea (Cicer arietinum L.) against Ascochyta rabiei by applying chemicals and plant extracts. Chil J Agric Res 71:52–62

    Article  Google Scholar 

  • Gómez-Ariza J, Campo S, Rufat M, Estopà M, Messeguer J et al (2007) Sucrose-mediated priming of plant defense responses and broad-spectrum disease resistance by overexpression of the maize pathogenesis-related PRms protein in rice plants. Mol Plant Microbe Interact 20:832–842

    Article  PubMed  CAS  Google Scholar 

  • Gomez-Gomez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011

    Article  CAS  PubMed  Google Scholar 

  • Görlach J, Volrath S, Knauf-Beiter G, Hengy G, Beckhove U et al (1996) Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8:629–643

    Article  PubMed  PubMed Central  Google Scholar 

  • Goupil P, Benouaret R, Charrier O, ter Halle A, Richard C et al (2012) Grape marc extract acts as elicitor of plant defence responses. Ecotoxicology 21:1541–1549

    Article  CAS  PubMed  Google Scholar 

  • Granado J, Felix G, Boller T (1995) Perception of fungal sterols in plants. Plant Physiol 107:485–490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gruau C, Trotel-Aziz P, Villaume S, Rabenoelina F, Clément C et al (2015) Pseudomonas fluorescens PTA-CT2 triggers local and systemic immune response against Botrytis cinerea in grapevine. Mol Plant Microbe Interact 28:1117–1129

    Article  CAS  PubMed  Google Scholar 

  • Gu R, Zhu S, Zhou J, Liu N, Shi J (2014) Inhibition on brown rot disease and induction of defence response in harvested peach fruit by nitric oxide solution. Eur J Plant Pathol 139:369–378

    Article  CAS  Google Scholar 

  • Gupta A, Khulbe D, Srinivas P, Ankita (2014a) Induction of systemic resistance in adzuki bean through seed bacterisation. Seed Sci Tech 42:332–343

    Google Scholar 

  • Gupta KJ, Mur LAJ, Brotman Y (2014b) Trichoderma asperelloides suppresses nitric oxide generation elicited by Fusarium oxysporum in Arabidopsis roots. Mol Plant Microbe Interact 27:307–314

    Article  CAS  PubMed  Google Scholar 

  • Guzman-Valle P, Bravo-Luna L, Montes-Belmont R, Guigon-Lopez C, Sepulveda-Jimenez G (2014) Induction of resistance to Sclerotium rolfsii in different varieties of onion by inoculation with Trichoderma asperellum. Eur J Plant Pathol 138:223–229

    Article  Google Scholar 

  • Haggag WWM, Hussein MM, Mehanna HM, El-Moneim D (2014) Bacteria polysaccharides elicit resistance of wheat against some biotic and abiotic stress. Int J Pharm Sci Rev Res 29:292–298

    CAS  Google Scholar 

  • Hahn MG, Albersheim P (1978) Host-pathogen interactions XIV. Isolation and partial characterization of an elicitor from yeast extract. Plant Physiol 62:107–111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haiko J, Westerlund-Wikström B (2013) The role of the bacterial flagellum in adhesion and virulence. Biology 2:1242–1267

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Han Q, Wu F, Wang X, Qi H, Shi L et al (2015) The bacterial lipopeptide iturins induce Verticillium dahliae cell death by affecting fungal signalling pathways and mediate plant defence responses involved in pathogen-associated molecular pattern-triggered immunity. Environ Microbiol 17:1166–1188

    Article  CAS  PubMed  Google Scholar 

  • Hassan MAE, Abo-Elyousr KAM (2013) Activation of tomato plant defence responses against bacterial wilt caused by Ralstonia solanacearum using DL-3-aminobutyric acid (BABA). Eur J Plant Pathol 136:145–157

    Article  CAS  Google Scholar 

  • Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K et al (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA 104:12217–12222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hendricks KEM, Donahoo RS, Roberts PD, Christman MC (2013) Effect of copper on growth characteristics and disease control of the recently introduced Guignardia citricarpa on citrus in Florida. Am J Plant Sci 4:282–290

    Article  CAS  Google Scholar 

  • Hoitink HA, Madden LV, Dorrance AE (2006) Systemic resistance induced by Trichoderma spp.: interactions between the host, the pathogen, the biocontrol agent, and soil organic matter quality. Phytopathology 96:186–189

    Article  CAS  PubMed  Google Scholar 

  • Huang W, Ji H, Gheysen G, Debode J, Kyndt T (2015) Biochar-amended potting medium reduces the susceptibility of rice to root-knot nematode infections. BMC Plant Biol 15:267

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huang W, Ji H, Gheysen G, Kyndt T (2016) Thiamine-induced priming against root-knot nematode infection in rice involves lignification and H2O2 generation. Mol Plant Pathol 17:614–24

    Article  CAS  PubMed  Google Scholar 

  • Iriti M, Faoro F (2008) Abscisic acid is involved in chitosan-induced resistance to tobacco necrosis virus (TNV). Plant Physiol Biochem 46:1106–1111

    Article  CAS  PubMed  Google Scholar 

  • Iriti M, Sironi M, Gomarasca S, Casazza AP, Soave C et al (2006) Cell death mediated antiviral effect of chitosan in tobacco. Plant Physiol Biochem 44:893–900

    Article  CAS  PubMed  Google Scholar 

  • Iriti M, Picchi V, Rossoni M, Gomarasca S, Ludwig N et al (2009) Chitosan antitranspirant activity is due to abscisic acid-dependent stomatal closure. Environ Exp Bot 66:493–500

    Article  CAS  Google Scholar 

  • Jain S, Choudhary DK (2014) Induced defense-related proteins in soybean (Glycine max L. Merrill) plants by Carnobacterium sp. SJ-5 upon challenge inoculation of Fusarium oxysporum. Planta 239:1027–1040

    Article  CAS  PubMed  Google Scholar 

  • Ji H, Kyndt T, He W, Vanholme B, Gheysen G (2015) β-aminobutyric acid-induced resistance against root-knot nematodes in rice is based on increased basal defence. Mol Plant Microbe Interact 28:519–533

    Article  CAS  PubMed  Google Scholar 

  • Jia X, Meng Q, Zeng H, Wang W, Yin H (2016) Chitosan oligosaccharides induces resistance to Tobacco mosaic virus in Arabidopsis via the salicylic acid-mediated signalling pathway. Nature https://doi.org/10.1038/srep26144

  • Jiang CH, Fan ZH, Xie P, Guo JH (2016) Bacillus cereus AR156 extracellular polysaccharides served as a novel micro-associated molecular pattern to induced systemic immunity to Pst DC3000 in Arabidopsis. Front Microbiol 9(7):664

    Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–32

    Article  CAS  PubMed  Google Scholar 

  • Kano A, Gomi K, Yamasaki-Kokudo Y, Satoh M, Fukumoto T et al (2010) A rare sugar, D-allose, confers resistance to rice bacterial blight with upregulation of defense-related genes in Oryza sativa. Phytopathology 100:85–90

    Article  CAS  PubMed  Google Scholar 

  • Kano A, Hosotani K, Gomi K, Yamasaki-Kokudo Y, Shirakawa C et al (2011) D-Psicose induces upregulation of defense-related genes and resistance in rice against bacterial blight. J Plant Physiol 168:1852–1857

    Article  CAS  PubMed  Google Scholar 

  • Kauss H, Jeblick W, Domard A (1989) The degree of polymerization and N-acetylation of chitosan determine its ability to elicit callose formation in suspension cells and protoplasts of Catharanthus roseus. Planta 178:385–392

    Article  CAS  PubMed  Google Scholar 

  • Keen NT, Partidge J, Zaki A (1972) Pathogen-produced elicitor of a chemical defense mechanism in soybean monogenically resistant to Phytophthora megasperma var. sojae. Phytopathology 62:768

    Google Scholar 

  • Keen NT, Yoshikawa M, Wang MC (1983) Phytoalexin elicitor activity of carbohydrates from Phytophthora megasperma f.sp. glycinea and other sources. Plant Physiol 71:466–471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan W, Rayirath UP, Subramanian S, Jithesk MN, Rayorath P et al (2009) Seaweed extracts as biostimulants of plant growth and development. J Plant Growth Regul 28:386–399

    Article  CAS  Google Scholar 

  • Kim SE, Rajapakse N (2005) Enzymatic production and biological activities of chitosan oligosaccharides (COS): a review. Carbohydr Polym 62:357–368

    Article  CAS  Google Scholar 

  • Klarzynski O, Descamps V, Plesse B, Yvin JC, Kloareg B et al (2003) Sulfated fucan oligosaccharides elicit defense responses in tobacco and local and systemic resistance against tobacco mosaic virus. Mol Plant Microbe Interact 16:115–122

    Article  CAS  PubMed  Google Scholar 

  • Klemptner RL, Sherwood JS, Tugizimana F, Dubery IA, Piater LA (2014) Ergosterol, an orphan fungal microbe-associated molecular pattern (MAMP). Mol Plant Pathol 15:747–761

    Article  CAS  PubMed  Google Scholar 

  • Klüsener B, Young JJ, Murata Y, Allen GJ, Mori IC et al (2002) Convergence of calcium signaling pathways of pathogenic elicitors and abscisic acid in Arabidopsis guard cells. Plant Physiol 130:2152–2163

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Koch E, Weil B, Wächter R, Wohlleben S, Spiess H et al (2006) Evaluation of selected microbial strains and commercial alternative products as seed treatments for the control of Tilletia tritici, Fusarium culmorum, Drechslera graminea and D. teres. J Plant Dis Prot 113:150–158

    Article  Google Scholar 

  • Konstantinidou-Doltsinis S, Markellou E, Kasselaki A, Fanouraki MN, Koumaki CM et al (2006) Efficacy of Milsana, a formulated plant extract from Reynoutria sachalinensis, against powdery mildew of tomato (Leveillula taurica). Biocontrol 51:375–392

    Article  Google Scholar 

  • Kuc J (1982) Induced immunity to plant disease. Bioscience 32:854–860

    Article  Google Scholar 

  • Kuc J (1995) Phytoalexins, stress metabolism, and disease resistance in plants. Ann Rev Phytopathol 33:275–297

    Article  CAS  Google Scholar 

  • Kumar A, Gond SK, Mishra A, Sharma VK, Verma SK et al (2015) Salicylic acid and its role in systemic resistance induced by Pseudomonas fluorescens to early blight disease of tomato. Vegetos 28:12–19

    Google Scholar 

  • Kurth F, Mailänder S, Bönn M, Feldhahn L, Herrmann S et al (2014) Streptomyces-induced resistance against oak powdery mildew involves host plant responses in defense, photosynthesis, and secondary metabolism pathways. Mol Plant Microbe Interact 27:891–900

    Article  CAS  PubMed  Google Scholar 

  • Kyungseok P, Kloepper JW, Ryu CM (2008) Rhizobacterial exopolysaccharides elicit induced resistance on cucumber. J Microbiol Biotechnol 18:1095–1100

    Google Scholar 

  • Lahlali R, Peng G (2014) Clonostachys rosea confers suppression of clubroot on canola via antibiosis and induced host resistance. Plant Pathol 63:447–455

    Article  CAS  Google Scholar 

  • Lahlali R, McGregor L, Song T, Gossen BD, Narisawa K et al (2014) Heteroconium chaetospira induces resistance to clubroot via upregulation of host genes involved in jasmonic acid, ethylene, and auxin biosynthesis. PLoS ONE 9(4):e94144

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lankinen A, Abreha KB, Alexandersson E, Andersson S, Andreasson E (2016) Nongenetic inheritance of induced resistance in a wild annual plant. Phytopathology 106:877–883

    Article  CAS  PubMed  Google Scholar 

  • Laquitaine L, Gomès E, François J, Marchive C, Pascal S et al (2006) Molecular basis of ergosterol-induced protection of grape against Botrytis cinerea: induction of type I LTP promoter activity, WRKY, and stilbene synthase gene expression. Mol Plant Microbe Interact 19:1103–1112

    Article  CAS  PubMed  Google Scholar 

  • Leach JE, Sherwood J, Fulton RW, Sequeira L (1983) Comparison of soluble proteins associated with disease resistance induced by bacterial lipopolysaccharide and viral necrosis. Physiol Plant Pathol 23:377–385

    Article  CAS  Google Scholar 

  • Ley SV, Denholm AA, Wood A (1993) The chemistry of azadirachtin. Nat Prod Rep 10:109–157

    Article  CAS  Google Scholar 

  • Li YR, Ma WX, Che YZ, Zou LF, Zakria M et al (2013) A highly-conserved single-stranded DNA-binding protein in Xanthomonas functions as a harpin-like protein to trigger plant immunity. PLoS ONE 8(2):e56240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Ding X, Wang C, Ke H, Wu Z et al (2016) Control of tomato yellow leaf curl virus disease by Enterobacter asburiae BQ9 as a result of priming plant resistance in tomatoes. Turk J Biol 40:150–159

    Article  CAS  Google Scholar 

  • Liljeroth E, Lankinen A, Wiik L, Burra DD, Alexandersson E et al (2016) Potassium phosphite combined with reduced doses of fungicides provides efficient protection against potato late blight in large-scale field trials. Crop Prot 86:42–55

    Article  CAS  Google Scholar 

  • Lim S, Borza T, Peters RD, Coffin RH, Al-Mughrabi KI et al (2013) Proteomics analysis suggests broad functional changes in potato leaves triggered by phosphites and a complex indirect mode of action against Phytophthora infestans. J Proteomic 93:207–223

    Article  CAS  Google Scholar 

  • Lin W, Hu X, Zhang W, Rogers WJ, Cai W (2005) Hydrogen peroxide mediates defence responses induced by chitosans of different molecular weights in rice. J Plant Physiol 162:937–944

    Article  CAS  PubMed  Google Scholar 

  • Liu B, Li JF, Ao Y, Qu J, Lo Z et al (2012) Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 24:3406–3419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luna E, van Hulten M, Zhang Y, Berkowitz O, López A et al (2014) Plant perception of β-aminobutyric acid is mediated by an aspartyl-tRNA synthetase. Nat Chem Biol 10:450–456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luna E, Beardon E, Ravnskov S, Scholes JD, Ton J (2016) Optimizing chemically induced resistance in tomato against Botrytis cinerea. Plant Dis 100:704–710

    Article  CAS  Google Scholar 

  • Lyon GD, Newton AC, Walters DR (2014) Induced resistance in crop protection: the future, drivers and barriers. In: Walters DR, Newton AC, Lyon GD (eds) Induced resistance for plant defence: a sustainable approach to crop protection. Blackwell Publishing Ltd, Oxford, pp 149–170

    Google Scholar 

  • Mabrouk Y, Mejri S, Belhadj O (2016) Biochemical mechanisms of induced resistance by rhizobial lipopolysaccharides in pea against crenate broomrape. Rev Bras Bot 39:107–114

    Article  Google Scholar 

  • Machinandiarena MF, Lobato MC, Feldman ML, Daleo GR, Andreu AB (2012) Potassium phosphite primes defense responses in potato against Phytophthora infestans. J Plant Physiol 169:1417–1424

    Article  CAS  PubMed  Google Scholar 

  • Magnin-Robert M, Quantinet D, Couderchet M, Aziz A, Trotel-Aziz P (2013) Differential induction of grapevine resistance and defense reactions against Botrytis cinerea by bacterial mixtures in vineyards. Biocontrol 58:117–131

    Article  Google Scholar 

  • Mao J, Liu Q, Yang X, Long C, Zhao M et al (2010) Purification and expression of a protein elicitor from Alternaria tenuissima and elicitor-mediated defence responses in tobacco. Ann Appl Biol 156:411–420

    Article  CAS  Google Scholar 

  • Martínez-Hidalgo P, García JM, Pozo MJ (2015) Induced systemic resistance against Botrytis cinerea by Micromonospora strains isolated from root nodules. Front Microbiol 2(6):922

    Google Scholar 

  • Massoud K, Barchietto T, Le Rudulier T, Pallandre L, Didierlaurent L et al (2012) Dissecting phosphite-induced priming in Arabidopsis infected with Hyaloperonospora arabidopsidis. Plant Physiol 159:286–298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mehari ZH, Elad Y, Rav-David D, Graber ER, Meller-Harel Y (2015) Induced systemic resistance in tomato (Solanum lycopersicum) against Botrytis cinerea by biochar amendment involves jasmonic acid signaling. Plant Soil 395:31–44

    Article  CAS  Google Scholar 

  • Mei L, Liang Y, Zhang L, Wang Y, Guo Y (2014) Induced systemic resistance and growth promotion in tomato by an indole-3-acetic acid-producing strain of Paenibacillus polymyxa (double effect). Ann Appl Biol 165:270–279

    Article  CAS  Google Scholar 

  • Meller-Harel Y, Elad Y, Rav-David D, Borenstein M, Shulchani R et al (2012) Biochar mediates systemic response of strawberry to foliar fungal pathogens. Plant Soil 357:245–257

    Article  CAS  Google Scholar 

  • Ménard R, Alban S, de Ruffray P, Jamois F, Franz G et al (2004) Beta-1,3 glucan sulfate, but not beta-1,3 glucan, induces the salicylic acid signaling pathway in tobacco and Arabidopsis. Plant Cell 16:3020–3032

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Monaghan J, Zipfel C (2012) Plant pattern recognition receptor complexes at the plasma membrane. Curr Opin Plant Biol 15:349–357

    Article  CAS  PubMed  Google Scholar 

  • Moyer C, Peres NA (2008) Evaluation of biofungicides for control of powdery mildew of gerbera daisy. Proc Fla State Hortic Soc 121:389–394

    Google Scholar 

  • Murali M, Amruthesh KN (2015) Plant growth-promoting fungus Penicillium oxalicum enhances plant growth and induces resistance in pearl millet against downy mildew disease. J Phytopathol 163:743–754

    Article  CAS  Google Scholar 

  • Murthy KN, Uzma F, Srinivas CC (2014) Induction of systemic resistance in tomato against Ralstonia solanacearum by Pseudomonas fluorescens. Am J Plant Sci 5:1799–1811

    Article  Google Scholar 

  • Mustafa G, Randoux B, Tisserant B, Fontaine J, Magnin-Robert M et al (2016) Phosphorus supply, arbuscular mycorrhizal fungal species, and plant genotype impact on the protective efficacy of mycorrhizal inoculation against wheat powdery mildew. Mycorrhiza 26:685–697

    Article  CAS  PubMed  Google Scholar 

  • Nair A, Kolet SP, Thulasiram HV, Bhargava S (2015a) Role of methyl jasmonate in the expression of mycorrhizal induced resistance against Fusarium oxysporum in tomato plants. Physiol Mol Plant Pathol 92:139–145

    Google Scholar 

  • Nair A, Kolet SP, Thulasiram HV, Bhargava S (2015b) Systemic jasmonic acid modulation in mycorrhizal tomato plants and its role in induced resistance against Alternaria alternata. Plant Biol (Stuttg)17: 625-631

    Google Scholar 

  • Ndimba BK, Chivasa S, Hamilton JM, Simon WJ, Slabas AR (2003) Proteomic analysis of changes in the extracellular matrix of Arabidopsis cell suspension cultures induced by fungal elicitors. Proteomics 3:1047–1059

    Article  CAS  PubMed  Google Scholar 

  • Newman MA, Sundelin T, Nielsen JT, Erbs G (2013) MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front Plant Sci 16(4):139

    Google Scholar 

  • Nguyen HP, Chakravarthy S, Velasquez AC, McLane HL, Zeng L et al (2010) Methods to study PAMP-triggered immunity using tomato and Nicotiana benthamiana. Mol Plant Microbe Interact 23:991–999

    Article  CAS  PubMed  Google Scholar 

  • Niu D, Wang X, Wang Y, Song X, Wang J et al (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(1):120–125

    Article  CAS  PubMed  Google Scholar 

  • Nürnberger T, Brunner F, Kemmerling B, Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198:249–266

    Article  PubMed  Google Scholar 

  • Nwodo UU, Green E, Okoh AL (2012) Bacterial exopolysaccharides: Functionality and Prospects. Int J Mol Sci 13:14002–14015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Obanor FO, Walter M, Jones EE, Jaspers MV (2013) Efficacy of systemic acquired resistance inducers in olive leaf spot management. Australas Plant Pathol 42:163–168

    Article  CAS  Google Scholar 

  • Okon Levy N, Meller Harel Y, Haile ZM, Elad Y, Rav-David E et al (2015) Induced resistance to foliar diseases by soil solarization and Trichoderma harzianum. Plant Pathol 64:365–374

    Article  CAS  Google Scholar 

  • Olson S (2015) An analysis of the biopesticide market now and where it is going. Outlooks Pest Manage 26:5

    Article  Google Scholar 

  • Ors M, Couleaud G, Maumene C, Siah A, Randoux B, et al (2014) Cultivar- and dose-dependent efficacy of wheat resistance inducers against Septoria tritici blotch in laboratory and field conditions. XIII Meeting of the Working Group Biological control of fungal and bacterial plant pathogens, Uppsala, Sweden

    Google Scholar 

  • Ortmann I, Conrath U, Moerschbacher BM (2006) Exopolysaccharides of Pantoea agglomerans have different priming and eliciting activities in suspension-cultured cells of monocots and dicots. FEBS Lett 580:4491–4494

    Article  CAS  PubMed  Google Scholar 

  • Ortmann I, Moerschbacher BM (2006) Spent growth medium of Pantoea agglomerans primes wheat suspension cells for augmented accumulation of hydrogen peroxide and enhanced peroxidase activity upon elicitation. Planta 224:963–970

    Article  CAS  PubMed  Google Scholar 

  • Pasini C, Daquila F, Curir P, Gullino ML (1997) Effectiveness of antifungal compounds against rose powdery mildew (Sphaerotheca pannosa var. rosae) in glasshouses. Crop Prot 16:251–256

    Article  CAS  Google Scholar 

  • Paul PK, Sharma PD (2002) Azadirachta indica leaf extract induces resistance in barley against leaf stripe disease. Physiol Mol Plant Pathol 61:3–13

    Article  CAS  Google Scholar 

  • Paulert R, Ebbinghaus D, Urlass C, Moerschbacher BM (2010) Priming of the oxidative burst in rice and wheat cell cultures by ulvan, a polysaccharide from green macroalgae, and enhanced resistance against powdery mildew in wheat and barley plants. Plant Pathol 59:634–642

    Article  CAS  Google Scholar 

  • Peng DH, Qiu DW, Ruan LF, Zhou CF, Sun M (2011) Protein elicitor PemG1 from Magnaporthe grisea induces systemic acquired resistance (SAR) in plants. Mol Plant Microbe Interact 24:1239–1246

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Montaño F, Alías-Villegas C, Bellogín RA, del Cerro P, Espuny MR et al (2014) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Res 169:325–336

    Article  PubMed  Google Scholar 

  • Pharand B, Carisse O, Benhamou N (2002) Cytological aspects of compost-mediated induced resistance against fusarium crown and root rot in tomato. Phytopathology 92:424–438

    Article  PubMed  Google Scholar 

  • Pieterse CM, van Wees SC, van Pelt JA, Knoester M, Laan R et al (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pretali L, Bernard L, Butterfield TS, Trevisan M, Lucini L (2016) Botanical and biological pesticides elicit a similar Induced Systemic Response in tomato (Solanum lycopersicum) secondary metabolism. Phytochemistry 130:56–63

    Article  CAS  PubMed  Google Scholar 

  • Raaijmakers JM, De Bruijn I, Nybroe O, Ongena M (2010) Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev 34:1037–1062

    Article  CAS  PubMed  Google Scholar 

  • Raho N, Ramirez L, Lanteri L, Gonorazky G, Lamattina L et al (2011) Phosphatidic acid production in chitosan-elicited tomato cells, via both phospholipase D and phospholipase C/diacylglycerol kinase, requires nitric oxide. J Plant Physiol 168:534–538

    Article  CAS  PubMed  Google Scholar 

  • Raizada RB, Srivastava MK, Kaushal RA, Singh RP (2001) Azadirachtin, a neem biopesticide: subchronic toxicity assessment in rats. Food Chem Toxicol 39:477–483

    Article  CAS  PubMed  Google Scholar 

  • Rakwal R, Tamogami S, Agrawal GK, Iwahashi H (2002) Octadecanoid signaling component “burst” in rice (Oryza sativa L.) seedling leaves upon wounding by cut and treatment with fungal elicitor protein. Biochem Biophys Res Commun 295:1041–1045

    Article  CAS  PubMed  Google Scholar 

  • Randoux B, Renard D, Nowak E, Sanssene J, Courtois J et al (2006) Inhibition of Blumeria graminis f. sp. tritici germination and partial enhancement of wheat defenses by Milsana. Phytopathology 96:1278–1286

    Article  CAS  PubMed  Google Scholar 

  • Ravensberg W (2015) Crop protection in 2030: towards a natural, efficient, safe and sustainable approach. International Symposium Swansea University, 7–9 Sept 2015

    Google Scholar 

  • Reignault P, Walters D (2007) Topical applications of inducers for disease control. In: Walters D, Lyon G (eds) Induced resistance for plant defence: a sustainable approach to crop protection. Blackwell Publishing Ltd, Oxford, pp 207–258

    Google Scholar 

  • Renard-Merlier D, Randoux B, Nowak E, Farcy F, Durand R et al (2007) Iodus 40, salicylic acid, heptanoyl salicylic acid and trehalose exhibit different efficacies and defence targets during a wheat/powdery mildew interaction. Phytochemistry 68:1156–1164

    Article  CAS  PubMed  Google Scholar 

  • Rosyidah A, Wardiyati T, Abadi AL, Maghfoer MD, Aini LQ (2014) Induced resistance of potato (Solanum tuberosum L.) toward Ralstonia solanacearum disease with combination of several bio-control microbes. J Biol Agric Healthc 4:90–98

    Google Scholar 

  • Salla TD, Astarita LV, Santarém ER (2016) Defense responses in plants of Eucalyptus elicited by Streptomyces and challenged with Botrytis cinerea. Planta 243:1055–1070

    Article  CAS  PubMed  Google Scholar 

  • Sanchez L, Courteaux B, Hubert J, Kauffmann S, Renault JH et al (2012) Rhamnolipids elicit defense responses and induce disease resistance against biotrophic, hemibiotrophic, and necotrophic pathogens that require different signaling pathways in Arabidopsis and highlight a central role for salicylic acid. Plant Physiol 160:1630–1641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sang MK, Kim EN, Han GD, Kwack MS, Jeun YC (2014) Priming-mediated systemic resistance in cucumber induced by Pseudomonas azotoformans GC-B19 and Paenibacillus elgii MM-B22 against Colletotrichum orbiculare. Phytopathology 104:834–842

    Article  CAS  PubMed  Google Scholar 

  • Sangha JS, Ravichandran S, Prithiviraj K, Critchley AT, Prithiviraj B (2010) Sulfated macroalgal polysaccharides λ-carrageenan and ι-carrageenan differentially alter Arabidopsis thaliana resistance to Sclerotinia sclerotiorum. Physiol Mol Plant Pathol 75:38–45

    Article  CAS  Google Scholar 

  • Sarosh BR, Sivaramakrishnan S, Shetty HS (2005) Elicitation of defense related enzymes and resistance by L-methionine in pearl millet against downy mildew disease caused by Sclerospora graminicola. Plant Physiol Biochem 43:808–815

    Article  CAS  PubMed  Google Scholar 

  • Sato I, Yoshida S, Iwamoto Y, Aino M, Hyakumachi M et al (2014) Suppressive potential of Paenibacillus strains isolated from the tomato phyllosphere against Fusarium crown and root rot of tomato. Microbes Environ 29:168–177

    Article  PubMed  PubMed Central  Google Scholar 

  • Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36:407–477

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schmid J, Sieber V, Rehim B (2015) Bacterial exopolysaccahrides: biosynthesis pathways and engineering strategies. Front Microbiol 6:496

    Article  PubMed  PubMed Central  Google Scholar 

  • Schmitt A (2002) Induced responses by plant extracts from Reynoutria sachalinensis: a case study. In “induced resistance in plants against insects and diseases”. IOBC/wprs Bull 25:83–88

    Google Scholar 

  • Segarra G, Santpere G, Elena G, Trillas I (2013) Enhanced Botrytis cinerea resistance of Arabidopsis plants grown in compost may be explained by increased expression of defense-related genes, as revealed by microarray analysis. PLoS ONE 8(2):e56075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Selim ME (2015) Effectiveness of Trichoderma biotic applications in regulating the related defense genes affecting tomato early blight disease. J Plant Pathol Microb 6:311

    Article  Google Scholar 

  • Sharma R, Singh D, Pal R (2013) Synergistic influence of pre-harvest calcium sprays and postharvest hot water treatment on fruit firmness, decay, bitter pit incidence and postharvest quality of royal delicious apples (Malus x domestica Borkh). Am J Plant Sci 4:153–159

    Article  CAS  Google Scholar 

  • Singh V, Louis J, Ayre BG, Reese JC, Pegadaraju V, Shah J (2011) Trehalose phosphate synthase11-dependent trehalose metabolism promotes Arabidopsis thaliana defense against the phloem-feeding insect Myzus persicae. Plant J 67:94–104

    Article  CAS  PubMed  Google Scholar 

  • Singh BN, Singh A, Singh BR, Singh HB (2014) Trichoderma harzianum elicits induced resistance in sunflower challenged by Rhizoctonia solani. J Appl Microbiol 116:654–666

    Article  CAS  PubMed  Google Scholar 

  • Son JS, Sumayo M, Hwang YJ, Kim BS, Ghim SY (2014) Screening of plant growth-promoting rhizobacteria as elicitor of systemic resistance against gray leaf spot disease in pepper. Appl Soil Ecol 73:1–8

    Article  Google Scholar 

  • Song GC, Choi HK, Ryu CM (2013) The folate precursor para-aminobenzoic acid elicits induced resistance against Cucumber mosaic virus and Xanthomonas axonopodis. Ann Bot 111:925–934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song Y, Chen D, Lu K, Sun Z, Zeng R (2015) Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Front Plant Sci 28(6):786

    Google Scholar 

  • Stadnik MJ, de Freitas MB (2014) Algal polysaccharides as source of plant resistance inducers. Trop Plant Pathol 39:111–118

    Article  Google Scholar 

  • Stangarlin JR, Kuhn OJ, Assi L, Schwan-Estrada KRF (2011) Control of plant diseases using extracts from medicinal plants and fungi. In: MendezVilas A (ed) Science against microbial pathogens: communicating current research and technological advances, pp 1033–1042

    Google Scholar 

  • Strieker M, Tanovic A, Marahiel MA (2010) Nonribosomal peptide synthetases: structures and dynamics. Curr Opin Struct Biol 20:234–240

    Article  CAS  PubMed  Google Scholar 

  • Sun A, Nie S, Xing D (2012) Nitric oxide-mediated maintenance of redox homeostasis contributes to NPR1-dependent plant innate immunity triggered by lipopolysaccharides. Plant Physiol 160:1081–1096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Surekha CH, Neelapu NRR, Siva Prasad B, Sankar Ganesh P (2014) Induction of defense enzymes and phenolic content by Trichoderma viride in Vigna mungo infested with Fusarium oxysporum and Alternaria alternata. Int J Agri Sci Res 4:31–40

    Google Scholar 

  • Tayeh C, Siah A, Randoux B, Halama P, Walters DR et al (2014a) Topical application of inducers for disease control. In: Walters DR, Newton AC, Lyon GD (eds) Induced resistance for plant defence: A sustainable approach to crop protection. Blackwell Publishing Ltd, Oxford, pp 193–231

    Google Scholar 

  • Tayeh C, Randoux B, Vincent D, Bourdon N, Reignault P (2014b) Exogenous trehalose induces defenses in wheat before and during a biotic stress caused by powdery mildew. Phytopathology 104:293–305

    Article  CAS  PubMed  Google Scholar 

  • Tesfagiorgis HB, Laing MD, Annegarnet HJ (2014) Evaluation of biocontrol agents and potassium silicate for the management of powdery mildew of zucchini. Biol Control 73:8–15

    Article  Google Scholar 

  • Tian S, Wan Y, Qin G, Xu Y (2006) Induction of defense responses against Alternaria rot by different elicitors in harvested pear fruit. Appl Microbiol Biotechnol 70:729–734

    Article  CAS  PubMed  Google Scholar 

  • Tinivella F, Hirata L, Celan M, Wrigh SAI, Amein T et al (2009) Control of seed-borne pathogens on legumes by microbial and other alternative seed treatments. Eur J Plant Pathol 123:139–151

    Article  Google Scholar 

  • Ton J, Jakab G, Toquin V, Flors V, Iavicoli A (2005) Dissecting the beta-aminobutyric acid-induced priming phenomenon in Arabidopsis. Plant Cell 17:987–999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tonelli ML, Fabra A (2014) The biocontrol agent Bacillus sp. CHEP5 primes the defense response against Cercospora sojina. World J Microbiol Biotechnol 30:2503–2509

    Article  CAS  PubMed  Google Scholar 

  • Toribio J, Escalante AE, Soberóron-Chavéz G (2010) Rhamnolipids: production in bacteria other than Pseudomonas aeruginosa. Eur J Lipids Sci Technol 112:1082–1087

    Article  CAS  Google Scholar 

  • Tran H, Ficke A, Asiimwe T, Höfte M, Raaijmakers JM (2007) Role of the cyclic lipopeptide massetolide A in biological control of Phytophthora infestans and in colonization of tomato plants by Pseudomonas fluorescens. New Phytol 175:731–742

    Article  CAS  PubMed  Google Scholar 

  • Trdá L, Fernandez O, Boutrot F, Héloir MC, Kelloniemi J et al (2014) The grapevine flagellin receptor VvFLS2 differentially recognizes flagellin-derived epitopes from the endophytic growth-promoting bacterium Burkholderia phytofirmans and plant pathogenic bacteria. New Phytol 201:1371–1384

    Article  PubMed  CAS  Google Scholar 

  • Trouvelot S, Héloir MC, Poinssot B, Gauthier A, Paris F et al (2014) Carbohydrates in plant immunity and plant protection: roles and potential application as foliar sprays. Front Plant Sci 5:592

    Article  PubMed  PubMed Central  Google Scholar 

  • Tubajika KM, Civerolo EL, Puterka GJ, Hashim JM, Luvisi DA (2007) The effects of kaolin, harpin, and imidacloprid on development of Pierce’s disease in grape. Crop Prot 26:92–99

    Article  CAS  Google Scholar 

  • Van Bockhaven J, Spıchal L, Novak O, Strnad M, Asano T et al (2014) Silicon induces resistance to the brown spot fungus Cochliobolus miyabeanus by preventing the pathogen from hijacking the rice ethylene pathway. New Phytol 206:761–773

    Article  CAS  Google Scholar 

  • Van Peer R, Niemann GJ, Schippers B (1991) Induced Resistance and phytoalexin accumulation in biological control of fusarium wilt of carnation by Pseudomonas sp. strain WCS417r. Phytopathology 81:728–734

    Article  Google Scholar 

  • 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 96:119–132

    Article  Google Scholar 

  • Van Wees SCM, Pieterse CMJ, Trijssenaar A, Van’t Westende YAM, Hartog F, et al (1997) Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Mol Plant Microbe Interact 10:716–724

    Google Scholar 

  • Vander P, Varum KM, Domard A, El Gueddari NE, Moerschbacher BM (1998) Comparison of the ability of partially N-adetylated chitosans and chitooligosaccharides to elicit resistance reactions in wheat leaves. Plant Physiol 111:1353–1359

    Article  Google Scholar 

  • Varnier AL, Sanchez L, Vatsa P, Boudesocque L, Garcia-Brugger A et al (2009) Bacterial rhamnolipids are novel MAMPs conferring resistance to Botrytis cinerea in grapevine. Plant Cell Environ 32:178–193

    Article  CAS  Google Scholar 

  • Vatsa P, Sanchez L, Clément C, Baillieul F, Dorey S (2010) Rhamnolipid biosurfactants as new players in animal and plant defense against microbes. Int J Mol Sci 11:2095–5108

    Article  CAS  Google Scholar 

  • Veloso J, Alabouvette C, Olivain C, Flors V, Pastor V et al (2016) Modes of action of the protective strain Fo47 in controlling verticillium wilt of pepper. Plant Pathol 65:997–1007

    Article  CAS  Google Scholar 

  • Vera J, Castro J, Contreras RA, Gonzalez A, Moenne A (2012) Oligo-carrageenans induce a longterm and broad-range protection against pathogens in tobacco plants (var. Xanthi). Physiol Mol Plant Pathol 79:31–39

    Article  CAS  Google Scholar 

  • Vergnes S, Ladouce N, Fournier S, Ferhout H, Attia F et al (2014) Foliar treatments with Gaultheria procumbens essential oil induce defense responses and resistance against a fungal pathogen in Arabidopsis. Front Plant Sci 5:477

    Article  PubMed  PubMed Central  Google Scholar 

  • Villaverde JJ, Sevilla-Moran B, Sandín-Espana P, Lopez-Goti C, Alonso-Prados JL (2014) Biopesticides in the framework of the European Pesticide Regulation (EC) No. 1107/2009. Pest Manag Sci 70:2–5

    Article  CAS  PubMed  Google Scholar 

  • Waewthongrak W, Pisuchpen S, Leelasuphakul W (2015) Effect of Bacillus subtilis and chitosan applications on green mold (Penicilium digitatum Sacc.) decay in citrus fruit. Postharvest Biol Technol 99:44–49

    Article  CAS  Google Scholar 

  • Walters DR, Fountaine JM (2009) Practical application of induced resistance to plant diseases: an appraisal of effectiveness under field conditions. J Agric Sci 147:523–535

    Article  CAS  Google Scholar 

  • Walters DR, Bennett AE (2014) Microbial induction of resistance to pathogens. In: Walters DR, Newton AC, Lyon GD (eds) Induced resistance for plant defence: a sustainable approach to crop protection. Blackwell Publishing Ltd, Oxford, pp 149–170

    Google Scholar 

  • Walters DR, Paterson L, Walsh DJ, Havis ND (2009) Priming for plant defense in barley provides benefits only under high disease pressure. Physiol Mol Plant Pathol 73:95–100

    Article  CAS  Google Scholar 

  • Walters DR, Paterson L, Havis ND (2010) Control of foliar diseases of spring barley using resistance elicitors. Proc Crop Prot North Britain 91–96

    Google Scholar 

  • Walters DR, Ratsep J, Havis ND (2013) Controlling crop diseases using induced resistance: challenges for the future. J Exp Bot 64:1263–1280

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Wang L, Wang J, Jin P, Liu H et al (2014) Bacillus cereus AR156-induced resistance to Colletotrichum acutatum is associated with priming of defense responses in loquat fruit. PLoS ONE 9(11):e112494

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang H, Yang X, Guo L, Zeng H, Qiu D (2015) PeBL1, a novel protein elicitor from Brevibacillus laterosporus strain A60, activates the defense responses and systemic resistance in Nicotiana benthamiana. Appl Environ Microbiol 81:2706–2716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang K, Liao Y, Xiong Q, Kan J, Cao S et al (2016) Induction of direct or priming resistance against Botrytis cinerea in strawberries by β-aminobutyric acid and their effects on sucrose metabolism. J Agric Food Chem 64:5855–5865

    Article  CAS  PubMed  Google Scholar 

  • Waqas M, Khan AL, Hamayun M, Shahzad R, Kim YH et al (2015) Endophytic infection alleviates biotic stress in sunflower through regulation of defence hormones, antioxidants and functional amino acids. Eur J Plant Pathol 141:803–824

    Article  CAS  Google Scholar 

  • Willmann R, Lajunen HM, Erbs G, Newman MA, Kolb D et al (2011) Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proc Natl Acad Sci USA 108:19824–19829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xing K, Zhu X, Peng X, Qin Q (2015) Chitosan antimicrobial and eliciting properties for pest control in agriculture: a review. Agron Sustain Dev 35:569–588

    Article  CAS  Google Scholar 

  • Yacoub A, Gerbore J, Magnin N, Chambon P, Dufour MC et al (2016) Ability of Pythium oligandrum strains to protect Vitis vinifera L., by inducing plant resistance against Phaeomoniella chlamydospora, a pathogen involved in Esca, a grapevine trunk disease. Biol Control 92:7–16

    Article  Google Scholar 

  • Yamamoto S, Shiraishi S, Kawagoe Y, Mochizuki M, Suzuki S (2015) Impact of Bacillus amyloliquefaciens S13-3 on control of bacterial wilt and powdery mildew in tomato. Pest Manag Sci 71:722–727

    Article  CAS  PubMed  Google Scholar 

  • Yang M, Ji X (2009) Studies on the induce-resistance effect of harpin on downy mildew and Botrytis cinerea of cucumber. Chin Agric Sci Bull 25:228–230

    Google Scholar 

  • Yao Q, Yang XF, Liang Y, Xu F, Liu Z et al (2007) Expression of a Magnaporthe grisea elicitor and its biological function in activating resistance in rice. Rice Sci 14:149–156

    Article  Google Scholar 

  • Yap MN, Rojas CM, Yang CH, Charkowski AO (2006) Harpin mediates cell aggregation in Erwinia chrysanthemi 3937. ‎J Bacteriol 188:2280-2284

    Google Scholar 

  • Yin H, Li S, Zhao X, Du Y, Ma X (2006) cDNA microarray analysis of gene expression in Brassica napus treated with oligochitosan elicitor. Plant Physiol Biochem 44:910–916

    Article  CAS  PubMed  Google Scholar 

  • Yin H, Zhao X, Du Y (2008) The primary study of oligochitosan inducing resistance to Sclerotinie scleraotiorum on B. napus. J Biotechnol 136:600–601

    Article  Google Scholar 

  • Younes I, Rinaudo M (2015) Chitin and chitosan preparation from marine sources. Structure, properties, applications. Mar Drugs 13:1173–1174

    Article  CAS  Google Scholar 

  • Yu T, Yu C, Lu H, Zunun M, Chen F et al (2012) Effect of Cryptococcus laurentii and calcium chloride on control of Penicillium expansum and Botrytis cinerea infections in pear fruit. Biol Control 61:169–175

    Article  CAS  Google Scholar 

  • Yu C, Zeng L, Sheng K, Chen F, Zhou T et al (2014) γ-Aminobutyric acid induces resistance against Penicillium expansum by priming of defence responses in pear fruit. Food Chem 159:29–37

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zeidler D, Dubery IA, Schmitt-Koplin P, Von Rad U, Durner J (2010) Lipopolysaccharides mobility in leaf tissues of Arabidopsis thaliana. Mol Plant Pathol 11:747–755

    CAS  PubMed  Google Scholar 

  • Zhang Y, Yang X, Liu Q, Qiu D, Zhang Y et al (2010) Purification of novel protein elicitor from Botrytis cinerea that induces disease resistance and drought tolerance in plants. Microbiol Res 165:142–151

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Yong D, Zhang Y, Shi X, Li B et al (2016a) Streptomyces rochei A-1 induces resistance and defense-related responses against Botryosphaeria dothidea in apple fruit during storage. Postharvest Biol Technol 115:30–37

    Article  CAS  Google Scholar 

  • Zhang F, Ge H, Zhang F, Guo N, Wang Y et al (2016b) Biocontrol potential of Trichoderma harzianum isolate T-aloe against Sclerotinia sclerotiorum in soybean. Plant Physiol Biochem 100:64–74

    Article  CAS  PubMed  Google Scholar 

  • Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG et al (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ali Siah .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Siah, A. et al. (2018). Natural Agents Inducing Plant Resistance Against Pests and Diseases. In: Mérillon, JM., Riviere, C. (eds) Natural Antimicrobial Agents. Sustainable Development and Biodiversity, vol 19. Springer, Cham. https://doi.org/10.1007/978-3-319-67045-4_6

Download citation

Publish with us

Policies and ethics