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Extracellular DNA: A Relevant Plant Damage-Associated Molecular Pattern (DAMP) for Crop Protection Against Pests—A Review

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Abstract

The immune response against pathogens, both in plants and animals, relies on a complex recognition system of danger signs. This system is based on the recognition of exogenous molecules termed Microbe- or Pathogen-Associated Molecular Patterns (MAMPs/PAMPs), and endogenous signals called “Damage-Associated Molecular Patterns” (DAMPs). This review will focus on DAMPs, which are molecules with a normal physiological state inside the cell, but at the time of damage or infection are usually released to the extracellular media, indicating cell damage. DAMPS are represented by a wide range of molecules consisting in small peptides, proteins, carbohydrates, cell wall fragments, extracellular ATP (eATP), extracellular DNA (eDNA) and volatile organic compounds (VOCs). Here we review plant DAMPs types and a new approach in eDNA use as biotechnological molecules for plant disease prevention. In particular, self-eDNA has gained importance due to its function of growth inhibition observed over a wide variety of organisms, this function is being studied as a new strategy for biological control to obtain highly pathogen-specific products, without wasting time and research resources. On the other hand, eDNA, as other DAMPs, could act as an immune response elicitor, which could conduce to a new approach for the protection of crops against pests.

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Fig. 1
Fig. 2

source of eDNA can be any type of soil pathogen or pest organism (bacteria, weeds, fungi). For immunity induction, as “plant vaccine” approach, doses < 200 µg mL−1 could be used in developed plants (for example; 4-week-old plants); DNA must be obtained from plants of agronomic interest

Fig. 3

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References

  • Acevedo FE, Rivera-Vega LJ, Chung SH, Ray S, Felton GW (2015) Cues from chewing insects: the intersection of DAMPs, HAMPs, MAMPs and effectors. Curr Opin Plant Biol 26:80–86

    CAS  PubMed  Google Scholar 

  • Andersson U, Tracey KJ (2011) HMGB1 is a therapeutic target for sterile inflammation and infection. Annu Rev Immunol 29:139–162

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barbero F, Guglielmotto M, Capuzzo A, Maffei M (2016) Extracellular self-DNA (esDNA), but not heterologous plant or insect DNA (etDNA), induces plasma membrane depolarization and calcium signaling in lima bean (Phaseolus lunatus) and maize (Zea mays). Int J Mol Sci 17:1659. https://doi.org/10.3390/ijms17101659

    Article  CAS  PubMed Central  Google Scholar 

  • Bartels S, Boller T (2015) Quo vadis, Pep? Plant elicitor peptides at the crossroads of immunity, stress, and development. J Exp Bot 66:5183–5193

    CAS  PubMed  Google Scholar 

  • Beloshistov RE, Dreizler K, Galiullina RA et al (2017) Phytaspase-mediated precursor processing and maturation of the wound hormone systemin. New Phytol. https://doi.org/10.1111/nph.14568

    Article  PubMed  Google Scholar 

  • Bhat A, Ryu C (2016) Plant Perceptions of Extracellular DNA and RNA. Molecular Plant 9:956–958

    CAS  PubMed  Google Scholar 

  • Boutrot F, Zipfel C (2017) Function, discovery, and exploitation of plant pattern recognition receptors for broad-spectrum disease resistance. Annu Rev Phytopathol 55:257–286

    CAS  PubMed  Google Scholar 

  • Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss D, Weinrauch Y, Zychlinsky A (2004) Neutrophil extracellular traps kill bacteria. Science 303:1532–1535

    CAS  PubMed  Google Scholar 

  • Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G (2010) A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci USA 107:9452–9457

    CAS  PubMed  PubMed Central  Google Scholar 

  • Butler MS (2008) Natural products to drugs: natural product-derived compounds in clinical trials. Nat Prod Rep 25:475–516

    CAS  PubMed  Google Scholar 

  • Cai R, Lewis J, Yan S, Liu H, Clarke CR et al (2011) The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity. PLoS Pathog 7(8):e1002130. https://doi.org/10.1371/journal.ppat.1002130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao Y, Liang Y, Tanaka K, Nguyen CT, Jedrzejczak RP, Joachimiak A, Stacey G (2014a) The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. eLife 3:e03766

    PubMed Central  Google Scholar 

  • Cao Y, Tanaka K, Nguyen C, Stacey G (2014b) Extracellular ATP is a central signaling molecule in plant stress responses. Curr Opin Plant Biol 20:82–88

    CAS  PubMed  Google Scholar 

  • Chandra S, Stennis M, Low PS (1997) Measurement of Ca2+ fluxes during elicitation of the oxidative burst in aequorin-transformed tobacco cells. J Biol Chem 272:28274–28280

    CAS  PubMed  Google Scholar 

  • Chen D, Cao Y, Li H et al (2017) Extracellular ATP elicits DORN1-mediated RBOHD phosphorylation to regulate stomatal aperture. Nat Commun 8:2265

    PubMed  PubMed Central  Google Scholar 

  • Chivasa S et al (2009) Extracellular ATP is a regulator of pathogen defence in plants. Plant J 60:436–448

    CAS  PubMed  Google Scholar 

  • Choi HW, Klessig DF (2016) DAMPs, MAMPs, and NAMPs in plant innate immunity. BMC Plant Biol 16:232

    PubMed  PubMed Central  Google Scholar 

  • Choi HW, Manohar M, Manosalva P, Tian M, Moreau M, Klessig DF (2016) Activation of plant innate immunity by extracellular high mobility group box 3 and its inhibition by salicylic acid. PLoS Pathog 12:e1005518

    PubMed  PubMed Central  Google Scholar 

  • Choi J, Tanaka K, Cao Y, Qi Y, Qiu J, Liang Y, Lee SY, Stacey G (2014) Identification of a plant receptor for extracellular ATP. Science 343:290–294

    CAS  PubMed  Google Scholar 

  • Cooksey CJ, Garratt PJ, Dahiya JS, Strange RN (1983) Sucrose: a constitutive elicitor of phytoalexin synthesis. Science 220:1398–1400

    CAS  PubMed  Google Scholar 

  • De Lorenzo G, Ferrari S, Cervone F, Okun E (2018) Extracellular DAMPs in plants and mammals: immunity, tissue damage and repair. Trends Immunol 39:937–950

    PubMed  Google Scholar 

  • De Lorenzo G, Ferrari S, Giovannoni M, Mattei B, Cervone F (2019) Cell wall traits that influence plant development, immunity, and bioconversion. Plant J 97:134–147

    PubMed  Google Scholar 

  • Denoux C, Galletti R, Mammarella N, Gopalan S, Werck D, De Lorenzo G et al (2008) Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. Mol Plant 1:423–445

    CAS  PubMed  Google Scholar 

  • Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11:539–548

    CAS  PubMed  Google Scholar 

  • Duran-Flores D, Heil M (2014) Damaged-self recognition in common bean (Phaseolus vulgaris) shows taxonomic specificity and triggers signaling via reactive oxygen species (ROS). Front Plant Sci 5:585

    PubMed  PubMed Central  Google Scholar 

  • Duran-Flores D, Heil M (2015) Growth inhibition by self-DNA: a phenomenon and its multiple explanations. New Phytol 207:482–485

    PubMed  Google Scholar 

  • Duran-Flores D, Heil M (2016) Sources of specificity in plant damaged-self recognition. Curr Opin Plant Biol 32:77–87

    CAS  PubMed  Google Scholar 

  • Duran-Flores D, Heil M (2018) Extracellular self-DNA as a damage-associated molecular pattern (DAMP) that triggers self-specific immunity induction in plants. Brain Behav Immun 72:78–88

    CAS  PubMed  Google Scholar 

  • Fauth M et al (1998) Cutin monomers and surface wax constituents elicit H2O2 in conditioned cucumber hypocotyl segments and enhance the activity of other H2O2 elicitors. Plant Physiol 117:1373–1380

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrari S, Savatin DV, Sicilia F, Gramegna G, Cervone F, Lorenzo GD (2013) Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development. Front Plant Sci 4:49

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gravino M, Locci F, Tundo S, Cervone F, Savatin DV, De Lorenzo G (2017) Immune responses induced by oligogalacturonides are differentially affected by AvrPto and loss of BAK1/BKK1 and PEPR1/PEPR2. Molecular Plant Pathology 18:582–595

    CAS  PubMed  Google Scholar 

  • Green TR, Ryan CA (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175:776–777

    CAS  PubMed  Google Scholar 

  • Guan AY, Liu CL, Sun XF, Xie Y, Wang MA (2016) Bioorg Med Chem 24:342–353

    CAS  PubMed  Google Scholar 

  • Gust AA, Pruitt R, Nürnberger T (2017) Sensing danger: key to activating plant immunity. Trends Plant Sci 22:779–791

    CAS  PubMed  Google Scholar 

  • Haruta M, Sabat G, Stecker K, Minkoff BB, Sussman MR (2014) A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343:408–411

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harvey AL (2008) Natural products in drug discovery. Drug Discov Today 13:894–901

    CAS  PubMed  Google Scholar 

  • Heil M (2009) Damaged-self recognition in plant herbivore defense. Trends Plant Sci 14:356–363

    CAS  PubMed  Google Scholar 

  • Heil M (2012) Damaged-self recognition as a general strategy for injury detection. Plant Signal Behav 7:576–580

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heil M, Land W (2014) Danger signals-damaged-self recognition across the tree of life. Front Plant Sci 5:579

    Google Scholar 

  • Heil M, Vega I (2019) Chapter five: nucleic acid sensing in plants and mammals: facts and caveats. nucleic acid sensing and immunity—part B. Int Rev Cell Mol Biol 345:225–285

    PubMed  Google Scholar 

  • Henry G, Thonart P, Ongena M (2012) PAMPs, MAMPs, DAMPs and others: an update on the diversity of plant immunity elicitors. Biol Agron Soc Environ 16(2):257–268

    Google Scholar 

  • Hideo I (2006) Impact of fungicide resistance in plant pathogens on crop disease control and agricultural environment. JARQ 40(3):205–211

    Google Scholar 

  • Hou S, Liu Z, Shen H, Wu D (2019) Damage-associated molecular pattern-triggered immunity in plants. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00646

    Article  PubMed  PubMed Central  Google Scholar 

  • Hou S, Wang X, Chen D, Yang X, Wang M, Turra D, Di Pietro A, Zhang W (2014) The secreted peptide PIP1 amplifies immunity through receptor-like kinase 7. PLoS Pathog 10:e1004331

    PubMed  PubMed Central  Google Scholar 

  • Huang HJ, Cui JR, Xia X, Chen J, Ye YX, Zhang CX, Hong XY (2019) Salivary DNase II from Laodelphax striatellus acts as an effector that suppresses plant defense. New Phytol 224:860–874

    CAS  PubMed  Google Scholar 

  • Huffaker A, Pearce G, Ryan CA (2006) An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc Natl Acad Sci USA 103:10098–10103

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jing Y, Bian Y, Hu Z, Wang L, Sean XQ (2018) Deep learning for drug design: an artificial intelligence paradigm for drug discovery in the big data era. AAPS J 20:58

    PubMed  Google Scholar 

  • Kauss H, Fauth M, Merten A, Jeblick W (1999) Cucumber hypocotyls respond to cutin monomers via both an inducible and a constitutive H2O2-generating system. Plant Physiol 120:1175–1182

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kawasaki T, Kawai T, Akira S (2011) Recognition of nucleic acids by pattern-recognition receptors and its relevance in autoimmunity. Immunol Rev 243(1):61–73

    CAS  PubMed  PubMed Central  Google Scholar 

  • Koehn FE, Carter GT (2005) The evolving role of natural products in drug discovery. Nat Rev Drug Discov 4:894–901

    Google Scholar 

  • Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16:3496–3507

    CAS  PubMed  PubMed Central  Google Scholar 

  • Land WG, Agostinis P, Gasser S, Garg AD, Linkermann A (2016) Transplantation and damage-associated molecular patterns (DAMPs). Am J Transpl 16:3338–3361

    CAS  Google Scholar 

  • Lee MW, Huffaker A, Crippen D, Robbins RT, Goggin FL (2018) Plant elicitor peptides promote plant defenses against nematodes in soy-bean. Mol Plant Pathol. https://doi.org/10.1111/mpp.12570

    Article  PubMed  PubMed Central  Google Scholar 

  • Locci F, Benedetti M, Pontiggia D, Citterico M, Caprari C, Mattei B, Cervone F, De Lorenzo G (2019) An Arabidopsis berberine bridge enzyme-like protein specifically oxidizes cellulose oligomers and plays a role in immunity. Plant J 98(3):540–554

    CAS  PubMed  Google Scholar 

  • Lotze MT, Tracey KJ (2005) High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 5:331–342

    CAS  PubMed  Google Scholar 

  • Lyne PD (2002) Structure-based virtual screening: an overview. Drug Discov Today 7:1047–1055

    CAS  PubMed  Google Scholar 

  • Matzinger P (1994) Tolerance, danger, and the extended family. Annu Rev Immunol 12:991–1045

    CAS  PubMed  Google Scholar 

  • Mazzoleni S, Bonanomi G, Incerti G, Chiusano M, Termolino P, Migliozzi A, Senatore M, Giannino F et al (2014) New perspectives on the use of nucleic acids in pharmacological applications: inhibitory action of extracellular self-DNA in biological systems. Phytochem Rev 13:937–946

    CAS  Google Scholar 

  • Mazzoleni S, Bonanomi G, Incerti G, Chiusano M, Termolino P, Mingo A, Senatore M, Giannino F et al (2015) Inhibitory and toxic effects of extracellular self-DNA in litter: a mechanism for negative plant–soil feedbacks? New Phytol 205:1195–1210

    CAS  PubMed  Google Scholar 

  • Mazzoleni S, Carteni F, Bonanomi G, Senatore M, Termolino P, Giannino F, Incerti G, Rietkerk M, Lanzotti V, Chiusano M (2015) Inhibitory effects of extracellular self-DNA: a general biological process? New Phytol 206:127–132. https://doi.org/10.1111/nph.13306

    Article  CAS  PubMed  Google Scholar 

  • Newman DJ, Cragg GM (2012) Natural products as sources of new drugs over the 30 years from 1981 to 2010. J Nat Prod 75:3012–3043

    Google Scholar 

  • O'Neill LAJ (2013) Sensing the dark side of DNA. Science 339:763–764

    CAS  PubMed  Google Scholar 

  • Pan X, Dong F, Wu X, Xu J, Liu X, Zheng Y (2019) Progress of the discovery, application, and control technologies of chemical pesticides in China. J Integr Agric 18(4):840–853

    CAS  Google Scholar 

  • Park HJ, Wang WW, Curlango G, Xiong ZG, Lin ZR, Huskey DA, Hawes MC, Vanetten HD, Turgeon BG (2019) A DNase from a fungal phytopathogen is a virulence factor likely deployed as counter defense against host-secreted extracellular DNA. MBio 10:e02805–02818

    CAS  PubMed  PubMed Central  Google Scholar 

  • Paungfoo-Lonhienne C, Lonhienne TG, Mudge SR, Schenk PM, Christie M, Carroll BJ, Schmidt S (2010) DNA is taken up by root hairs and pollen, and stimulates root and pollen tube growth. Plant Physiol 153:799–805

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pearce G (2011) Systemin, hydroxyproline-rich systemin and the induction of protease inhibitors. Curr Protein Pept Sci 12:399–408

    CAS  PubMed  Google Scholar 

  • Pearce G, Bhattacharya R, Chen YC, Barona G, Yamaguchi Y, Ryan CA (2009) Isolation and characterization of hydroxyproline-rich glycopeptide signals in black nightshade leaves. Plant Physiol 150:1422–1433

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pearce G, Moura DS, Stratmann J, Ryan CA (2001) Production of multiple plant hormones from a single polyprotein precursor. Nature 411:817–820

    CAS  PubMed  Google Scholar 

  • Petutschnig EK, Jones AM, Serazetdinova L, Lipka U, Lipka V (2010) The lysin motif receptor-like kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J Biol Chem 285:28902–28911

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pisetsky DS (2012) The origin and properties of extracellular DNA: from PAMP to DAMP. Clin Immunol 144:32–40

    CAS  PubMed  PubMed Central  Google Scholar 

  • Quintana-Rodriguez E, Duran-Flores D, Heil M, Camacho-Coronel X (2018) Damage-associated molecular patterns (DAMPs) as future plant vaccines that protect crops from pests. Sci Hortic 237:207–220

    CAS  Google Scholar 

  • Ramadan A, Land WG, Paczesny S (2017) Editorial: danger signals triggering immune response and inflammation. Front Immunol 8:979

    PubMed  PubMed Central  Google Scholar 

  • Ranf S, Gisch N, Schaffer M et al (2015) A lectin S-domain receptor kinase mediates lipopolysaccharide sensing in Arabidopsis thaliana. Nat Immunol 16:426–433

    CAS  PubMed  Google Scholar 

  • Ross A, Yamada K, Hiruma K, Yamashita-Yamada M, Lu X, Takano Y, Tsuda K, Saijo Y (2014) The Arabidopsis PEPR pathway couples local and systemic plant immunity. EMBO J 33:62–75

    CAS  PubMed  Google Scholar 

  • Saijo Y, Loo E (2020) Plant immunity in signal integration between biotic and abiotic stress responses. New Phytol 225:87–104

    PubMed  Google Scholar 

  • Saijo Y, Loo E, Yasuda S (2018) Pattern recognition receptors and signaling in plant–microbe interactions. Plant J 93:592–613

    CAS  PubMed  Google Scholar 

  • Scheer JM, Ryan CA (2002) The systemin receptor SR160 from Lycopersicon peruvianum is a member of the LRR receptor kinase family. Proc Natl Acad Sci USA 99:9585–9590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J, Chourey PS, Alborn HT, Teal PEA (2006) Fragments of ATP synthase mediate plant perception of insect attack. Proc Natl Acad Sci USA 103:8894–8899

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schmelz EA, LeClere S, Carroll MJ, Alborn HT, Teal PEA (2007) Cowpea chloroplastic ATP synthase is the source of multiple plant defense elicitors during insect herbivory. Plant Physiol 144:793–805

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schneider S, Ullrich WR (1994) Differential induction of resistance and enhanced enzyme-activities in cucumber and tobacco caused by treatment with various abiotic and biotic inducers. Physiol Mol Plant Pathol 45:291–304

    CAS  Google Scholar 

  • Smith A (2002) Screening for drug discovery: the leading question. Nature 418:453–455. https://doi.org/10.1038/418453a

    Article  CAS  PubMed  Google Scholar 

  • Souza CD, Li SD, Lin AZ, Boutrot F, Grossmann G, Zipfel C, Somerville SC (2017) Cellulose-derived oligomers act as damage-associated molecular patterns and trigger defense-like responses. Plant Physiol 173:2383–2398

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stegmann M, Monaghan J, Smakowska-Luzan E, Rovenich H, Lehner A, Holton N, Belkhadir Y, Zipfel C (2017) The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science 355:287–289

    CAS  PubMed  Google Scholar 

  • Stokes JM, Yang K, Swanson K, Jin W, Cubillos-Ruiz A, Donghia NM, MacNair CR, French S, Carfrae LA, Bloom-Ackerman Z, Tran VM, Chiappino-Pepe A, Badran AH, Andrews IW, Chory EJ, Church GM, Brown EB, Jaakkola TS, Barzilay R, Collins JJ (2020) A deep learning approach to antibiotic discovery. Cell 180:688–702

    CAS  PubMed  PubMed Central  Google Scholar 

  • Swinney DC, Anthony J (2011) How were new medicines discovered? Nat Rev Drug Discov 10:507–519

    CAS  PubMed  Google Scholar 

  • Szymański P, Markowicz M, Mikiciuk-Olasiknt E (2012) Adaptation of high-throughput screening in drug discovery—toxicological screening tests. J Mol Sci 13:427–452. https://doi.org/10.3390/ijms13010427

    Article  CAS  Google Scholar 

  • Tanaka K, Choi J, Cao Y, Stacey G (2014) Extracellular ATP acts as a damage-associated molecular pattern (DAMP) signal in plants. Front Plant Sci 5:446

    PubMed  PubMed Central  Google Scholar 

  • Tang D, Kang R, Coyne CB, Lotze ZHJ (2012) PAMPs and DAMPs: signal 0s that spur autophagy and immunity. Immunol Rev 249:158–175

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tavormina P, De Coninck B, Nikonorova N, De Smet I, Cammue BPA (2015) The plant peptidome: an expanding repertoire of structural features and biological functions. Plant Cell 27:2095–2118

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas C, Nielsen K (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3:711–721

    CAS  PubMed  Google Scholar 

  • Tripathi D, Zhang T, Koo AJ, Stacey G, Tanaka K (2018) Extracellular ATP acts on jasmonate signaling to reinforce plant defense. Plant Physiol 176:511–523

    CAS  PubMed  Google Scholar 

  • Vega-Muñoz I, Feregrino-Pérez AA, Torres-Pacheco I, Guevara-González RG (2018) Exogenous fragmented DNA acts as a damage-associated molecular pattern (DAMP) inducing changes in CpG DNA methylation and defense-related responses in Lactuca sativa. Funct Plant Biol. https://doi.org/10.1071/FP18011

    Article  PubMed  Google Scholar 

  • Vénéreau E, Ceriotti C, Bianchi ME (2015) DAMPs from death to new life. Front Immunol 6:422

    PubMed  PubMed Central  Google Scholar 

  • Veresoglou SD, Aguilar-Trigueros CA, Mansour I, Rillig MC (2015) Self-DNA: a blessing in disguise? New Phytol 207:488–490. https://doi.org/10.1111/nph.13425

    Article  PubMed  Google Scholar 

  • Walters D, Heil M (2007) Costs and trade-offs associated with induced resistance. Physiol Mol Plant Pathol 71:3–17

    CAS  Google Scholar 

  • Wang L, Einig E, Almeida-Trapp M, Albert M, Fliegman J, Mithöfer A, Kalbacher H, Felix G (2018) The systemin receptor SYR1 enhances resistance of tomato against herbivorous insects. Nat Plants 4:152–156. https://doi.org/10.1038/s41477-018-0106-0

    Article  CAS  PubMed  Google Scholar 

  • Wen F, White GJ, VanEtten HD, Xiong Z, Hawes MC (2009) Extracellular DNA is required for root tip resistance to fungal infection. Plant Physiol 151:820–829

    CAS  PubMed  PubMed Central  Google Scholar 

  • Willmann R, Lajunen HM, Erbs G 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi Y, Huffaker A (2011) Endogenous peptide elicitors in higher plants. Curr Opin Plant Biol 14:351–357

    CAS  PubMed  Google Scholar 

  • Yamaguchi Y, Huffaker A, Bryan AC, Frans ET, Ryan CA (2010) PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22:508–522

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yatim N, Cullen S, Albert ML (2017) Dying cells actively regulate adaptive immune responses. Nat Rev Immunol 17:262–275

    CAS  PubMed  Google Scholar 

  • Yoshinaga N, Ishikawa C, Seidl-Adams I, Bosak E, Aboshi T, Tumlinson JH, Mori N (2014) N-(18-Hydroxylinolenoyl)-l-glutamine: a newly discovered analog of volicitin in Manduca sexta and its elicitor activity in plants. J Chem Ecol 40:484–490

    CAS  PubMed  Google Scholar 

  • Zhang W (2018) Global pesticide use: profile, trend, cost/benefit and more. Proc Int Acad Ecol Environ Sci 8(1):1–27

    Google Scholar 

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Acknowledgements

Author thanks to Sep-CONACYT (Consejo Nacional de Ciencia y Tecnología) Ciencia Básica 2016 (283259) for partial support. Moreover, N.I. F-J also acknowledges to CONACYT for grant support.

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  1. Biosystems Engineering Group, School of Engineering, Autonomous University of Querétaro, Querétaro, Mexico

    Noelia I. Ferrusquía-Jiménez, Gobinath Chandrakasan, Irineo Torres-Pacheco, Enrique Rico-Garcia, Ana A. Feregrino-Perez & Ramón G. Guevara-González

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  1. Noelia I. Ferrusquía-Jiménez
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Ferrusquía-Jiménez, N.I., Chandrakasan, G., Torres-Pacheco, I. et al. Extracellular DNA: A Relevant Plant Damage-Associated Molecular Pattern (DAMP) for Crop Protection Against Pests—A Review. J Plant Growth Regul 40, 451–463 (2021). https://doi.org/10.1007/s00344-020-10129-w

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