Advertisement

Planta

, Volume 250, Issue 1, pp 391–393 | Cite as

Commentary on Grandellis et al. 2019: suggesting endogenous DNA as further player in the plant immune response to DOTAP

  • Martin HeilEmail author
Short Communication

Successful immunity requires the perception of exogenous and endogenous factors that indicate threats for homeostasis. Over the past years, it has become evident that plants, fungi and mammals share multiple elements of their innate immune system, including the perception of ‘damage-associated molecular patterns’ (DAMPs): endogenous molecules that have an ‘all-day job’ in the intact cell but serve as danger signals when present—as entire molecules or as fragments—in aberrant compartments (Heil and Land 2014). Examples of well-studied mammalian DAMPs that play the same role in plants or fungi include small signalling peptides (Pearce et al. 2010; Hander et al. 2019), extracellular ATP (Choi et al. 2014; Castellanos et al. 2018), and the high-mobility group box protein 3 (Choi et al. 2016). Even cancer drugs can trigger plant immune responses (Hadwiger and Tanaka 2018).

The most recent milestone in this development comes from the recent publication by Grandellis et al. (2019). In the...

Keywords

Damage-associated molecular patterns (DAMPs) Extracellular DNA DNA transfection Induced resistance Plant innate immunity 

Abbreviations

eDNA

Extracellular DNA

DAMP

Damage-associated molecular pattern

DOTAP

1,2-Dioleoyl-3-trimethylammonium-propane

PPR

Pattern recognition receptor

Notes

Acknowledgements

I thank Professor Dr. Dorothea Bartels for inviting this commentary, two anonymous referees for very helpful comments and Dr. Caroline Woods for correcting an earlier version of this manuscript. The research of MH is supported by CONACYT Grant 278283.

References

  1. 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). Int J Mol Sci 17:1659.  https://doi.org/10.3390/ijms17101659 CrossRefGoogle Scholar
  2. Bhat A, Ryu C-M (2016) Plant perceptions of extracellular DNA and RNA. Mol Plant 9(7):956–958.  https://doi.org/10.1016/j.molp.2016.05.014 CrossRefGoogle Scholar
  3. 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 Signal Behav 11(4):e1158381.  https://doi.org/10.1080/15592324.2016.1158381 CrossRefGoogle Scholar
  4. Castellanos E, Herrera-Estrella A et al (2018) Danger signals activate a putative innate immune system during regeneration in a filamentous fungus. PLoS Genet 14(11):e1007390.  https://doi.org/10.1371/journal.pgen.1007390 CrossRefGoogle Scholar
  5. 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(6168):290–294.  https://doi.org/10.1126/science.343.6168.290 CrossRefGoogle Scholar
  6. Choi HW, Manohar M, Manosalva P, Tian MY, 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(3):e1005518.  https://doi.org/10.1371/journal.ppat.1005518 CrossRefGoogle Scholar
  7. Duran-Flores D, Heil M (2015) Growth inhibition by self-DNA: a phenomenon and its multiple explanations. New Phytol 207(3):482–485.  https://doi.org/10.1111/nph.13542 CrossRefGoogle Scholar
  8. 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.  https://doi.org/10.1016/j.bbi.2017.10.010 CrossRefGoogle Scholar
  9. Gallucci S, Maffei M (2017) DNA sensing across the tree of life. Trends Immunol 38(10):719–732.  https://doi.org/10.1016/j.it.2017.07.012 CrossRefGoogle Scholar
  10. Grandellis C, Garavaglia BS, Gottig N, Lonez C, Ruysschaert JM, Ottado J (2019) DOTAP, a lipidic transfection reagent, triggers Arabidopsis plant defense responses. Planta 249(2):469–480.  https://doi.org/10.1007/s00425-018-3014-7 CrossRefGoogle Scholar
  11. Hadwiger LA (2015) Nonhost resistance: self-inflicted DNA damage by fungal DNase accumulation is a major factor in terminating fungal growth in the pea-Fusarium solani f. sp phaseoli interaction. Physiol Mol Plant Pathol 92:79–87.  https://doi.org/10.1016/j.pmpp.2015.08.003 CrossRefGoogle Scholar
  12. Hadwiger LA, Tanaka K (2017) Non-host resistance: DNA damage is associated with SA signaling for induction of PR genes and contributes to the growth suppression of a pea pathogen on pea endocarp tissue. Front Plant Sci 8:446.  https://doi.org/10.3389/fpls.2017.00446 CrossRefGoogle Scholar
  13. Hadwiger LA, Tanaka K (2018) DNA damage and chromatin conformation changes confer nonhost resistance: a hypothesis based on effects of anti-cancer agents on plant defense responses. Front Plant Sci 9:1056.  https://doi.org/10.3389/fpls.2018.01056 CrossRefGoogle Scholar
  14. Hander T, Fernández-Fernández ÁD, Kumpf RP, Willems P, Schatowitz H, Rombaut D, Staes A, Nolf J, Pottie R, Yao P, Gonçalves A, Pavie B, Boller T, Gevaert K, Van Breusegem F, Bartels S, Stael S (2019) Damage on plants activates Ca2+-dependent metacaspases for release of immunomodulatory peptides. Science 363(6433):eaar7486.  https://doi.org/10.1126/science.aar7486 CrossRefGoogle Scholar
  15. Heil M, Land WG (2014) Danger signals—damaged-self recognition across the tree of life. Front Plant Sci 5:579.  https://doi.org/10.3389/fpls.2014.00578 CrossRefGoogle Scholar
  16. Heil M, Vega-Muñoz I (2019) Nucleic acid sensing in mammals and plants: facts and caveats. Int Rev Cell Mol Biol 345:225–285.  https://doi.org/10.1016/bs.ircmb.2018.10.003 CrossRefGoogle Scholar
  17. Huang H-J, Cui J-R, Xia X, Chen J, Ye Y-X, Zhang C-X, Hong X-Y (2019) Salivary DNase II from Laodelphax striatellus acts as an effector that suppresses plant defense. New Phytol.  https://doi.org/10.1111/nph.15792 Google Scholar
  18. Kopfnagel V, Wagenknecht S, Harder J, Hofmann K, Kleine M, Buch A, Sodeik B, Werfel T (2018) RNase 7 strongly promotes TLR9-mediated DNA sensing by human plasmacytoid dendritic cells. J Invest Dermatol 138(4):872–881.  https://doi.org/10.1016/j.jid.2017.09.052 CrossRefGoogle Scholar
  19. Lonez C, Vandenbranden M, Ruysschaert JM (2012) Cationic lipids activate intracellular signaling pathways. Adv Drug Deliver Rev 64(15):1749–1758.  https://doi.org/10.1016/j.addr.2012.05.009 CrossRefGoogle Scholar
  20. Lonez C, Bessodes M, Scherman D, Vandenbranden M, Escriou V, Ruysschaert JM (2014) Cationic lipid nanocarriers activate Toll-like receptor 2 and NLRP3 inflammasome pathways. Nanomed Nanotechnol Biol Med 10(4):775–782.  https://doi.org/10.1016/j.nano.2013.12.003 CrossRefGoogle Scholar
  21. Mazzoleni S, Bonanomi G, Incerti G, Chiusano ML, Termolino P, Mingo A, Senatore M, Giannino F, Cartenì F, Rietkerk M, Lanzotti V (2015a) Inhibitory and toxic effects of extracellular self-DNA in litter: a mechanism for negative plant–soil feedbacks? New Phytol 205(3):1195–1210.  https://doi.org/10.1111/nph.13121 CrossRefGoogle Scholar
  22. Mazzoleni S, Cartenì 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 Phytol 206(1):127–132.  https://doi.org/10.1111/nph.13306 CrossRefGoogle Scholar
  23. Pearce G, Yamaguchi Y, Barona G, Ryan CA (2010) A subtilisin-like protein from soybean contains an embedded, cryptic signal that activates defense-related genes. Proc Natl Acad Sci USA 107(33):14921–14925.  https://doi.org/10.1073/pnas.1007568107 CrossRefGoogle Scholar
  24. 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 defence-related responses in Lactuca sativa. Funct Plant Biol 45(10):1065–1072.  https://doi.org/10.1071/FP18011 CrossRefGoogle Scholar
  25. Wasungu L, Hoekstra D (2006) Cationic lipids, lipoplexes and intracellular delivery of genes. J Control Release 116(2):255–264.  https://doi.org/10.1016/j.jconrel.2006.06.024 CrossRefGoogle Scholar
  26. Yan S, Wang W, Marqués J, Mohan R, Saleh A, Durrant Wendy E, Song J, Dong X (2013) Salicylic acid activates DNA damage responses to potentiate plant immunity. Mol Cell 52(4):602–610.  https://doi.org/10.1016/j.molcel.2013.09.019 CrossRefGoogle Scholar
  27. Zebell SG, Dong X (2015) Cell-cycle regulators and cell death in immunity. Cell Host Microbe 18(4):402–407.  https://doi.org/10.1016/j.chom.2015.10.001 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Departmento de Ingeniería GenéticaCentro de Investigación y de Estudios Avanzados (CINVESTAV) Unidad IrapuatoIrapuatoMexico

Personalised recommendations