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Planta

, Volume 247, Issue 5, pp 1217–1227 | Cite as

Induction of systemic resistance in tomato against Botrytis cinerea by N-decanoyl-homoserine lactone via jasmonic acid signaling

  • Zhangjian Hu
  • Shujun Shao
  • Chenfei Zheng
  • Zenghui Sun
  • Junying Shi
  • Jingquan Yu
  • Zhenyu Qi
  • Kai Shi
Original Article

Abstract

Main conclusion

N-decanoyl-homoserine lactone activates plant systemic resistance against Botrytis cinerea in tomato plants, which is largely dependent on jasmonic acid biosynthesis and signal transduction pathways.

Rhizosphere bacteria secrete N-acylated-homoserine lactones (AHLs), a type of specialized quorum-sensing signal molecule, to coordinate their population density during communication with their eukaryotic hosts. AHLs behave as low molecular weight ligands that are sensed by plants and promote the host’s resistance against foliar pathogens. In this study, we report on N-decanoyl-homoserine lactone (DHL), which is a type of AHL that induces systemic immunity in tomato plants and protects the host organism against the necrotrophic fungus Botrytis cinerea. Upon DHL treatment, tomato endogenous jasmonic acid (JA) biosynthesis (rather than salicylic acid biosynthesis) and signal transduction were significantly activated. Strikingly, the DHL-induced systemic resistance against B. cinerea was blocked in the tomato JA biosynthesis mutant spr2 and JA signaling gene-silenced plants. Our findings highlight the role of DHL in systemic resistance against economically important necrotrophic pathogens and suggest that DHL-induced immunity against B. cinerea is largely dependent on the JA signaling pathway. Manipulation of DHL-induced resistance is an attractive disease management strategy that could potentially be used to enhance disease resistance in diverse plant species.

Keywords

N-decanoyl-homoserine lactone Induced systemic resistance Jasmonic acid Salicylic acid Solanum lycopersicum Virus-induced gene silencing 

Abbreviations

AHLs

N-acylated-homoserine lactones

DHL

N-decanoyl-homoserine lactone

dpi/hpi

Day/hour post infection

HHL

N-hexanoyl-homoserine lactone

JA

Jasmonic acid

OHHL

N-3-oxo-hexanoyl-homoserine lactone

PI

Proteinase inhibitor

SA

Salicylic acid

ФPSII

The photochemical quantum efficiency of PSII

Notes

Acknowledgements

This work was supported by the National Key Research and Development Program of China (2017YFD0200600) and the National Natural Science Foundation of China (31772355).

Supplementary material

425_2018_2860_MOESM1_ESM.pdf (822 kb)
Supplementary material 1 (PDF 821 kb)

References

  1. Asai S, Mase K, Yoshioka H (2010) A key enzyme for flavin synthesis is required for nitric oxide and reactive oxygen species production in disease resistance. Plant J 62(6):911–924PubMedGoogle Scholar
  2. Birkenbihl RP, Diezel C, Somssich IE (2012) Arabidopsis WRKY33 is a key transcriptional regulator of hormonal and metabolic responses toward Botrytis cinerea infection. Plant Physiol 159(1):266–285CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bolton MD, Thomma BPHJ, Nelson BD (2006) Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Mol Plant Pathol 7(1):1–16CrossRefPubMedGoogle Scholar
  4. de Oliveira MVV, Xu GY, Li B, Vespoli LD, Meng XZ, Chen X, Yu X, de Souza SA, Intorne AC, Manhaes AMED, Musinsky AL, Koiwa H, de Souza GA, Shan LB, He P (2016) Specific control of Arabidopsis BAK1/SERK4-regulated cell death by protein glycosylation. Nat Plants 2(2):15218CrossRefPubMedPubMedCentralGoogle Scholar
  5. El Oirdi M, Abd El Rahman T, Rigano L, El Hadrami A, Rodriguez MC, Daayf F, Vojnov A, Bouarab K (2011) Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato. Plant Cell 23(6):2405–2421CrossRefPubMedPubMedCentralGoogle Scholar
  6. Ferrari S, Plotnikova JM, De Lorenzo G, Ausubel FM (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J 35(2):193–205CrossRefPubMedGoogle Scholar
  7. Ferrari S, Galletti R, Denoux C, De Lorenzo G, Ausubel FM, Dewdney J (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(1):367–379CrossRefPubMedPubMedCentralGoogle Scholar
  8. Fonseca S, Chico JM, Solano R (2009) The jasmonate pathway: the ligand, the receptor and the core signalling module. Curr Opin Plant Biol 12(5):539–547CrossRefPubMedGoogle Scholar
  9. Fu ZQ, Dong XN (2013) Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64(64):839–863CrossRefPubMedGoogle Scholar
  10. Gaida MM, Dapunt U, Hansch GM (2016) Sensing developing biofilms: the bitter receptor T2R38 on myeloid cells. Pathog Dis 74(3):ftw004CrossRefPubMedPubMedCentralGoogle Scholar
  11. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990(1):87–92CrossRefGoogle Scholar
  12. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227CrossRefPubMedGoogle Scholar
  13. Gonzalez JE, Keshavan ND (2006) Messing with bacterial quorum sensing. Microbiol Mol Biol Rev 70(4):859–875CrossRefPubMedPubMedCentralGoogle Scholar
  14. Gotz C, Fekete A, Gebefuegi I, Forczek ST, Fuksova K, Li X, Englmann M, Gryndler M, Hartmann A, Matucha M, Schmitt-Kopplin P, Schroder P (2007) Uptake, degradation and chiral discrimination of N-acyl-d/l-homoserine lactones by barley (Hordeum vulgare) and yam bean (Pachyrhizus erosus) plants. Anal Bioanal Chem 389(5):1447–1457CrossRefPubMedGoogle Scholar
  15. Govrin EM, Levine A (2002) Infection of Arabidopsis with a necrotrophic pathogen, Botrytis cinerea, elicits various defense responses but does not induce systemic acquired resistance (SAR). Plant Mol Biol 48(3):267–276CrossRefPubMedGoogle Scholar
  16. Karlsson T, Turkina MV, Yakymenko O, Magnusson KE, Vikstrom E (2012) The Pseudomonas aeruginosa N-acylhomoserine lactone quorum sensing molecules target IQGAP1 and modulate epithelial cell migration. PLoS Pathog 8(10):e1002953CrossRefPubMedPubMedCentralGoogle Scholar
  17. Lade H, Paul D, Kweon JH (2014) N-acyl homoserine lactone-mediated quorum sensing with special reference to use of quorum quenching bacteria in membrane biofouling control. Biomed Res Int 2014:16254CrossRefGoogle Scholar
  18. Li CY, Liu GH, Xu CC, Lee GI, Bauer P, Ling HQ, Ganal MW, Howe GA (2003) The tomato Suppressor of prosystemin-mediated responses2 gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemic wound signal for defense gene expression. Plant Cell 15(7):1646–1661CrossRefPubMedPubMedCentralGoogle Scholar
  19. Liu YL, Schiff M, Dinesh-Kumar SP (2002) Virus-induced gene silencing in tomato. Plant J 31(6):777–786CrossRefPubMedGoogle Scholar
  20. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408CrossRefPubMedGoogle Scholar
  21. Lopez-Millan AF, Sagardoy R, Solanas M, Abadia A, Abadia J (2009) Cadmium toxicity in tomato (Lycopersicon esculentum) plants grown in hydroponics. Environ Exp Bot 65(2–3):376–385CrossRefGoogle Scholar
  22. Mathesius U, Mulders S, Gao MS, Teplitski M, Caetano-Anolles G, Rolfe BG, Bauer WD (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci USA 100(3):1444–1449CrossRefPubMedPubMedCentralGoogle Scholar
  23. Morquecho-Contreras A, Mendez-Bravo A, Pelagio-Flores R, Raya-Gonzalez J, Ortiz-Castro R, Lopez-Bucio J (2010) Characterization of drr1, an alkamide-resistant mutant of Arabidopsis, reveals an important role for small lipid amides in lateral root development and plant senescence. Plant Physiol 152(3):1659–1673CrossRefPubMedPubMedCentralGoogle Scholar
  24. Ortiz-Castro R, Martinez-Trujillo M, Lopez-Bucio J (2008) N-acyl-l-homoserine lactones: a class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. Plant Cell Environ 31(10):1497–1509CrossRefPubMedGoogle Scholar
  25. Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5(5):308–316CrossRefPubMedGoogle Scholar
  26. Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375CrossRefPubMedGoogle Scholar
  27. Rehman S, Aziz E, Akhtar W, Ilyas M, Mahmood T (2017) Structural and functional characteristics of plant proteinase inhibitor-II (PI-II) family. Biotechnol Lett 39(5):647–666CrossRefPubMedGoogle Scholar
  28. Rowe HC, Walley JW, Corwin J, Chan EKF, Dehesh K, Kliebenstein DJ (2010) Deficiencies in jasmonate-mediated plant defense reveal quantitative variation in Botrytis cinerea pathogenesis. PLoS Pathog 6(4):e1000861CrossRefPubMedPubMedCentralGoogle Scholar
  29. Schenk ST, Hernandez-Reyes C, Samans B, Stein E, Neumann C, Schikora M, Reichelt M, Mithofer A, Becker A, Kogel KH, Schikora A (2014) N-acyl-homoserine lactone primes plants for cell wall reinforcement and induces resistance to bacterial pathogens via the salicylic acid/oxylipin pathway. Plant Cell 26(6):2708–2723CrossRefPubMedPubMedCentralGoogle Scholar
  30. Schikora A, Schenk ST, Stein E, Molitor A, Zuccaro A, Kogel KH (2011) N-acyl-homoserine lactone confers resistance toward biotrophic and hemibiotrophic pathogens via altered activation of AtMPK6. Plant Physiol 157(3):1407–1418CrossRefPubMedPubMedCentralGoogle Scholar
  31. Schuhegger R, Ihring A, Gantner S, Bahnweg G, Knappe C, Vogg G, Hutzler P, Schmid M, Van Breusegem F, Eberl L, Hartmann A, Langebartels C (2006) Induction of systemic resistance in tomato by N-acyl-l-homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ 29(5):909–918CrossRefPubMedGoogle Scholar
  32. Sun JQ, Jiang HL, Li CY (2011) Systemin/jasmonate-mediated systemic defense signaling in tomato. Mol Plant 4(4):607–615CrossRefPubMedGoogle Scholar
  33. Tejeda-Sartorius M, de la Vega OM, Delano-Frier JP (2008) Jasmonic acid influences mycorrhizal colonization in tomato plants by modifying the expression of genes involved in carbohydrate partitioning. Physiol Plant 133(2):339–353CrossRefPubMedGoogle Scholar
  34. van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483CrossRefPubMedGoogle Scholar
  35. Vannini A, Volpari C, Gargioli C, Muraglia E, Cortese R, De Francesco R, Neddermann P, Di Marco S (2002) The crystal structure of the quorum sensing protein TraR bound to its autoinducer and target DNA. EMBO J 21(17):4393–4401CrossRefPubMedPubMedCentralGoogle Scholar
  36. Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206CrossRefPubMedGoogle Scholar
  37. von Rad U, Klein I, Dobrev PI, Kottova J, Zazimalova E, Fekete A, Hartmann A, Schmitt-Kopplin P, Durner J (2008) Response of Arabidopsis thaliana to N-hexanoyl-dl-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere. Planta 229(1):73–85CrossRefGoogle Scholar
  38. Walters DR, Ratsep J, Havis ND (2013) Controlling crop diseases using induced resistance: challenges for the future. J Exp Bot 64(5):1263–1280CrossRefPubMedGoogle Scholar
  39. Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346CrossRefPubMedGoogle Scholar
  40. Waters CA, Lu WY, Rabinowitz JD, Bassler BL (2008) Quorum sensing controls biofilm formation in Vibrio cholerae through modulation of cyclic Di-GMT levels and repression of vpsT. J Bacteriol 190(7):2527–2536CrossRefPubMedPubMedCentralGoogle Scholar
  41. Williamson B, Tudzynsk B, Tudzynski P, van Kan JAL (2007) Botrytis cinerea: the cause of grey mould disease. Mol Plant Pathol 8(5):561–580CrossRefPubMedGoogle Scholar
  42. Withers H, Swift S, Williams P (2001) Quorum sensing as an integral component of gene regulatory networks in Gram-negative bacteria. Curr Opin Microbiol 4(2):186–193CrossRefPubMedGoogle Scholar
  43. Wu JQ, Hettenhausen C, Meldau S, Baldwin IT (2007) Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell 19(3):1096–1122CrossRefPubMedPubMedCentralGoogle Scholar
  44. Zabala MD, Zhai B, Jayaraman S, Eleftheriadou G, Winsbury R, Yang R, Truman W, Tang SJ, Smirnoff N, Grant M (2016) Novel JAZ co-operativity and unexpected JA dynamics underpin Arabidopsis defence responses to Pseudomonas syringae infection. New Phytol 209(3):1120–1134CrossRefGoogle Scholar
  45. Zhang S, Li X, Sun ZH, Shao SJ, Hu LF, Ye M, Zhou YH, Xia XJ, Yu JQ, Shi K (2015) Antagonism between phytohormone signalling underlies the variation in disease susceptibility of tomato plants under elevated CO2. J Exp Bot 66(7):1951–1963CrossRefPubMedPubMedCentralGoogle Scholar
  46. Zhu ZQ, An FY, Feng Y, Li PP, Xue L, Mu A, Jiang ZQ, Kim JM, To TK, Li W, Zhang XY, Yu Q, Dong Z, Chen WQ, Seki M, Zhou JM, Guo HW (2011) Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Natl Acad Sci USA 108(30):12539–12544CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of HorticultureZhejiang UniversityHangzhouPeople’s Republic of China
  2. 2.Experimental Station of Zhejiang UniversityHangzhouPeople’s Republic of China

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