Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Exogenous fragmented DNA acts as a damage-associated molecular pattern (DAMP) inducing changes in CpG DNA methylation and defence-related responses in Lactuca sativa

I. Vega-Muñoz A , Ana A. Feregrino-Pérez A , I. Torres-Pacheco A and R. G. Guevara-González A B
+ Author Affiliations
- Author Affiliations

A Biosystems Engineering Group, School of Engineering, Autonomous University of Queretaro, Campus Amazcala. Carr. Chichimequillas-Amazcala Km 1 S/N. Amazcala, C.P.76265, El Marques, Querétaro, México.

B Corresponding author. Email: ramon.guevara@uaq.mx

Functional Plant Biology 45(10) 1065-1072 https://doi.org/10.1071/FP18011
Submitted: 11 January 2018  Accepted: 10 April 2018   Published: 9 May 2018

Abstract

Damage-associated molecular patterns (DAMPs) have been studied recently to understand plant self–nonself recognition in response to attack by biotic and abiotic stresses. Extracellular DNA has emerged as a possible DAMP. As a DAMP DNA seems to function depending on the phylogenetic scale and has been tested in a few plant species. This study aimed to evaluate the possible role of self DNA (sDNA) as a DAMP by analysing changes in CpG DNA methylation and defence-related responses in lettuce (Lactuca sativa L.) as a model plant. sDNA and nonself DNA (nsDNA) from Capsicum chinense Murray (both species belong to the same clade, Asterids) stimulated aberrant seed germination and root growth in lettuce seedlings. Similar resultswere obtained with nsDNA obtained from Acaciella angustissima (Mill.) Britton & Rose plants (belonging to the clade Rosids I), although at significantly higher concentrations. Moreover, in most cases, this behaviour was correlated with hypomethylation of CpG DNA as well as defence responses measured as altered gene expression associated with oxidative burst and production of secondary metabolites (phenylpropanoids) related to coping with stress conditions. Our results suggested that extracellular and fragmented DNA has a role as a DAMP depending on phylogenetic closeness in plants as lettuce, inducing epigenetic, genetic and biochemical changes within the plant. The importance of our results is that, for the first time, they demonstrate that sDNA acts as a DAMP in plants, changing CpG DNA methylation levels as well as increasing the production of secondary metabolites associated with defence responses to stress.

Additional keywords: elicitor, epigenetics, immune system, lettuce, sonication.


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. Current Opinion in Plant Biology 26, 80–86.
Cues from chewing insects – the intersection of DAMPs, HAMPs, MAMPs and effectors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXpsVWktr4%3D&md5=d24835cd0c3a491fe81d1aa46f628d32CAS |

Aroca R, Ruiz-Lozano JM, Zamarreño AM, Paz JA, Garcia-Mina JM, Pozo MJ, Lopez-Raez JA (2013) Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. Journal of Plant Physiology 170, 47–55.
Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFKns7bJ&md5=14feb7a02077b6a070c3c57db544382bCAS |

Barbero F, Guglielmotto M, Capuzzo A, Maffei ME (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). International Journal of Molecular Sciences 17, 1659
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).Crossref | GoogleScholarGoogle Scholar |

Bianchi ME (2007) DAMPs, PAMPs and alarmins: all we need to know about danger. Journal of Leukocyte Biology 81, 1–5.
DAMPs, PAMPs and alarmins: all we need to know about danger.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktVaisg%3D%3D&md5=1855fe2f08b670f553b931c928e897f7CAS |

Böhm H, Albert I, Fan L, Reinhard A, Nürnberger T (2014) Immune receptor complexes at the plant cell surface. Current Opinion in Plant Biology 20, 47–54.
Immune receptor complexes at the plant cell surface.Crossref | GoogleScholarGoogle Scholar |

Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annual Review of Plant Biology 60, 379–406.
A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntFGlsL0%3D&md5=14b060658a49fb11b67701c7dfddf11cCAS |

Cartenì F, Bonanomi G, Giannino F, Incerti G, Vincenot CE, Chiusano ML, Mazzoleni S (2016) Self-DNA inhibitory effects: underlying mechanisms and ecological implications. Plant Signaling & Behavior 11, e1158381
Self-DNA inhibitory effects: underlying mechanisms and ecological implications.Crossref | GoogleScholarGoogle Scholar |

Choi HW, Klessig DF (2016) DAMPs, MAMPs, and NAMPs in plant innate immunity. BMC Plant Biology 16, 232
DAMPs, MAMPs, and NAMPs in plant innate immunity.Crossref | GoogleScholarGoogle Scholar |

Clarke JD (2009) Cetyltrimethyl ammonium bromide (CTAB) DNA miniprep for plant DNA isolation. Cold Spring Harbor Protocols 4, 5177–5179.

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). Frontiers in Plant Science 5, 585
Damaged-self recognition in common bean (Phaseolus vulgaris) shows taxonomic specificity and triggers signaling via reactive oxygen species (ROS).Crossref | GoogleScholarGoogle Scholar |

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

Duran-Flores D, Heil M (2016) Sources of specificity in plant damaged-self recognition. Current Opinion in Plant Biology 32, 77–87.
Sources of specificity in plant damaged-self recognition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtFanu7zM&md5=b867f8b640a8761a160ec8efd95abab5CAS |

Duran-Flores D, Heil M (2017) Extracellular self-DNA as a damage-associated molecular pattern (DAMP) that triggers self-specific immunity induction in plants. Brain, Behavior, and Immunity
Extracellular self-DNA as a damage-associated molecular pattern (DAMP) that triggers self-specific immunity induction in plants.Crossref | GoogleScholarGoogle Scholar |

Gallucci S, Maffei ME (2017) DNA sensing across the tree of life. Trends in Immunology 38, 719–732.
DNA sensing across the tree of life.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhtlGrs7bF&md5=9cdec1af674d96743ba10e1b29a48f9fCAS |

Gust AA, Pruitt R, Nürnberger T (2017) Sensing danger: key to activating plant immunity. Trends in Plant Science 22, 779–791.
Sensing danger: key to activating plant immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXht1entb%2FN&md5=59dc4323eea7268ed757e06144b08aa1CAS |

Heil M (2012) Damaged-self recognition as a general strategy for injury detection. Plant Signaling & Behavior 7, 576–580.
Damaged-self recognition as a general strategy for injury detection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVKhtr%2FN&md5=3d8e2a4ebf08a3317cdbdc5ba138ac76CAS |

Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Reviews. Genetics 11, 204–220.
Establishing, maintaining and modifying DNA methylation patterns in plants and animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitFCrsLk%3D&md5=24dddd906174e68a5750a4baa67660ddCAS |

Macho AP, Zipfel C (2014) Plant PRRs and the activation of innate immune signaling. Molecular Cell 54, 263–272.
Plant PRRs and the activation of innate immune signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXntFGht78%3D&md5=56d0d466c7aec691dc49beafec6a42a0CAS |

Mazzoleni S, Bonanomi G, Incerti G, Chiusano ML, Termolino P, Mingo A, Senatore M, Giannino F, Carteni F, Rietkerk M, Lanzotti V (2015a) Inhibitory and toxic effects of extracellular self-DNA in litter: a mechanism for negative plant–soil feedbacks? New Phytologist 205, 1195–1210.
Inhibitory and toxic effects of extracellular self-DNA in litter: a mechanism for negative plant–soil feedbacks?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXnslaguw%3D%3D&md5=973c1e1712bdc6d04013dba20bf68681CAS |

Mazzoleni S, Carteni F, Bonanomi G, Senatore M, Termolino P, Giannino F, Incerti G, Rietkerk M, Lanzotti V, Chiusano ML (2015b) Inhibitory effects of extracellular self-DNA: a general biological process? New Phytologist 206, 127–132.
Inhibitory effects of extracellular self-DNA: a general biological process?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjtF2qsLY%3D&md5=c472a0f9173d88b4db2c3cd18bdc1ee1CAS |

Mejía-Teniente L, Torres-Pacheco I, González-Chavira MM, Ocampo-Velazquez RV, Herrera-Ruiz G, Chapa-Oliver AM, Guevara Gonzalez RG (2010) Use of elicitors as an approach for sustainable agriculture. African Journal of Biotechnology 9, 9155–9162.

Ngom B, Sarr I, Kimatu J, Mamati E, Kane NA (2017) Genome-wide analysis of cytosine DNA methylation revealed salicylic acid promotes defense pathways over seedling development in pearl millet. Plant Signaling & Behavior 12, e1356967
Genome-wide analysis of cytosine DNA methylation revealed salicylic acid promotes defense pathways over seedling development in pearl millet.Crossref | GoogleScholarGoogle Scholar |

Paludan SR, Bowie AG (2013) Immune sensing of DNA. Immunity 38, 870–880.
Immune sensing of DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXotF2ntbo%3D&md5=d6034ba018b88d582612bffdc7fba28dCAS |

Reyes-Chin-Wo S, Wang Z, Yang X, Kozik A, Arikit S, Song C, Xia L, Froenicke L, Lavelle DO, Truco M-J, Xia R, Zhu S, Xu C, Xu H, Xu X, Cox K, Korf I, Meyerz BC, Michelmore RW (2017) Genome assembly with in vitro proximity ligation data and whole-genome triplication in lettuce. Nature Communications 8, 14953
Genome assembly with in vitro proximity ligation data and whole-genome triplication in lettuce.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXmtFCrsLk%3D&md5=079f4ab7ec984241782dbc8c3c7c7631CAS |

Segonzac C, Zipfel C (2011) Activation of plant pattern-recognition receptors by bacteria. Current Opinion in Microbiology 14, 54–61.
Activation of plant pattern-recognition receptors by bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvV2qt7w%3D&md5=b04df73b33255d3b5fa0840b7b50c8f7CAS |

Seybold H, Trempel F, Ranf S, Scheel D, Romeis T, Lee J (2014) Ca2+ signalling in plant immune response: from pattern recognition receptors to Ca2+ decoding mechanisms. New Phytologist 204, 782–790.
Ca2+ signalling in plant immune response: from pattern recognition receptors to Ca2+ decoding mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVOgurnL&md5=59b7a1d8e4648ea4346f56cfbe962f87CAS |

Tanaka K, Choi J, Cao Y, Stacey G (2014) Extracellular ATP acts as a damage-associated molecular pattern (DAMP) signal in plants. Frontiers in Plant Science 5, 446
Extracellular ATP acts as a damage-associated molecular pattern (DAMP) signal in plants.Crossref | GoogleScholarGoogle Scholar |

Tierranegra-García N, Salinas-Soto P, Torres-Pacheco I, Ocampo-Velázquez RV, Rico-García E, Mendoza-Diaz SO, Feregrino-Pérez AA, Mercado-Luna A, Vargas-Hernandez M, Soto-Zarazúa GM, Guevara-González RG (2011) Effect of foliar salicylic acid and methyl jasmonate applications on protection against pill-bugs in lettuce plants (Lactuca sativa). Phytoparasitica 39, 137–144.
Effect of foliar salicylic acid and methyl jasmonate applications on protection against pill-bugs in lettuce plants (Lactuca sativa).Crossref | GoogleScholarGoogle Scholar |

Vargas-Hernandez M, Macias-Bobadilla I, Guevara-Gonzalez RG, Romero-Gomez SdJ, Rico-Garcia E, Ocampo-Velazquez RV, Alvarez-Arquieta LdL, Torres-Pacheco I (2017) Plant hormesis management with biostimulants of biotic origin in agriculture. Frontiers in Plant Science 8, 1762
Plant hormesis management with biostimulants of biotic origin in agriculture.Crossref | GoogleScholarGoogle Scholar |

Veresoglou SD, Aguilar-Trigueros CA, Mansour I, Rillig MC (2015) Self-DNA: a blessing in disguise? New Phytologist 207, 488–490.
Self-DNA: a blessing in disguise?Crossref | GoogleScholarGoogle Scholar |

Zipfel C (2009) Early molecular events in PAMP-triggered immunity. Current Opinion in Plant Biology 12, 414–420.
Early molecular events in PAMP-triggered immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsFyqtrg%3D&md5=36e3237a30951f19ad8b2e0b52c6bcc3CAS |

Zipfel C (2014) Plant pattern-recognition receptors. Trends in Immunology 35, 345–351.
Plant pattern-recognition receptors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpvFWltbk%3D&md5=66b4bdc9f1b086248b2ec5173dfbff58CAS |