Oregano essential oil vapour prevents Plasmopara viticola infection in grapevine (Vitis Vinifera) and primes plant immunity mechanisms


Autoři: Markus Rienth aff001;  Julien Crovadore aff002;  Sana Ghaffari aff001;  François Lefort aff002
Působiště autorů: Changins, HES-SO University of Applied Sciences and Arts Western Switzerland, Nyon, Switzerland aff001;  Plants and Pathogens Group, Institute Land Nature and Environment, Hepia, HES-SO University of Applied Sciences and Arts Western Switzerland, Jussy, Geneva, Switzerland aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0222854

Souhrn

The reduction of synthetic fungicides in agriculture is necessary to guarantee a sustainable production that protects the environment and consumers’ health. Downy mildew caused by the oomycete Plasmopara viticola is the major pathogen in viticulture worldwide and responsible for up to 60% of pesticide treatments. Alternatives to reduce fungicides are thus utterly needed to ensure sustainable vineyard-ecosystems, consumer health and public acceptance. Essential oils (EOs) are amongst the most promising natural plant protection alternatives and have shown their antibacterial, antiviral and antifungal properties on several agricultural crops. However, the efficiency of EOs highly depends on timing, application method and the molecular interactions between the host, the pathogen and EO. Despite proven EO efficiency, the underlying processes are still not understood and remain a black box. The objectives of the present study were: a) to evaluate whether a continuous fumigation of a particular EO can control downy mildew in order to circumvent the drawbacks of direct application, b) to decipher molecular mechanisms that could be triggered in the host and the pathogen by EO application and c) to try to differentiate whether essential oils directly repress the oomycete or act as plant resistance primers. To achieve this a custom-made climatic chamber was constructed that enabled a continuous fumigation of potted vines with different EOs during long-term experiments. The grapevine (Vitis vinifera) cv Chasselas was chosen in reason of its high susceptibility to Plasmopara viticola. Grapevine cuttings were infected with P. viticola and subsequently exposed to continuous fumigation of different EOs at different concentrations, during 2 application time spans (24 hours and 10 days). Experiments were stopped when infection symptoms were clearly observed on the leaves of the control plants. Plant physiology (photosynthesis and growth rate parameters) were recorded and leaves were sampled at different time points for subsequent RNA extraction and transcriptomics analysis. Strikingly, the Oregano vulgare EO vapour treatment during 24h post-infection proved to be sufficient to reduce downy mildew development by 95%. Total RNA was extracted from leaves of 24h and 10d treatments and used for whole transcriptome shotgun sequencing (RNA-seq). Sequenced reads were then mapped onto the V. vinifera and P. viticola genomes. Less than 1% of reads could be mapped onto the P. viticola genome from treated samples, whereas up to 30% reads from the controls mapped onto the P. viticola genome, thereby confirming the visual observation of P. viticola absence in the treated plants. On average, 80% of reads could be mapped onto the V. vinifera genome for differential expression analysis, which yielded 4800 modulated genes. Transcriptomic data clearly showed that the treatment triggered the plant’s innate immune system with genes involved in salicylic, jasmonic acid and ethylene synthesis and signaling, activating Pathogenesis-Related-proteins as well as phytoalexin synthesis. These results elucidate EO-host-pathogen interactions for the first time and indicate that the antifungal efficiency of EO is mainly due to the triggering of resistance pathways inside the host plants. This is of major importance for the production and research on biopesticides, plant stimulation products and for resistance-breeding strategies.

Klíčová slova:

Downy mildew – Gene expression – Grapevine – Leaves – Oils – Plant fungal pathogens – Plant pathogens – Vapors


Zdroje

1. Gisi U, Sierotzki HJEJoPP. Fungicide modes of action and resistance in downy mildews. European Journal of Plant Pathology. 2008;122(1):157–67. doi: 10.1007/s10658-008-9290-5

2. Kim K-H, Kabir E, Jahan SA. Exposure to pesticides and the associated human health effects. Science of The Total Environment. 2017;575:525–35. doi: 10.1016/j.scitotenv.2016.09.009 27614863

3. Gessler C, Pertot I, Perazzolli M. Plasmopara viticola: a review of knowledge on downy mildew of grapevine and effective disease management. Phytopathologia Mediterranea. 2011;50(1).

4. Burruano S. The life-cycle of Plasmopara viticola, cause of downy mildew of vine. Mycologist. 2000;14:179–82.

5. Furuya S, Mochizuki M, Saito S, Kobayashi H, Takayanagi T, Suzuki S. Monitoring of QoI fungicide resistance in Plasmopara viticola populations in Japan. Pest management science. 2010;66(11):1268–72. Epub 2010/08/28. doi: 10.1002/ps.2012 20799246.

6. Chen W-J, Delmotte F, Cervera SR, Douence L, Greif C, Corio-Costet M-F. At Least Two Origins of Fungicide Resistance in Grapevine Downy Mildew Populations. Appl Environ Microbiol. 2007;73(16):5162–72. doi: 10.1128/AEM.00507-07 J Applied and Environmental Microbiology. 17586672

7. Ballabio C, Panagos P, Lugato E, Huang J-H, Orgiazzi A, Jones A, et al. Copper distribution in European topsoils: An assessment based on LUCAS soil survey. Science of The Total Environment. 2018;636:282–98. doi: 10.1016/j.scitotenv.2018.04.268 29709848

8. Flemming CA, Trevors JT, Pollution S. Copper toxicity and chemistry in the environment: a review. J Water, Air,. 1989;44(1):143–58. doi: 10.1007/bf00228784

9. Salmon JM, Friedl MA, Frolking S, Wisser D, Douglas EM. Global rain-fed, irrigated, and paddy croplands: A new high resolution map derived from remote sensing, crop inventories and climate data. International Journal of Applied Earth Observation and Geoinformation. 2015;38:321–34. doi: 10.1016/j.jag.2015.01.014

10. Viret O, Spring JL, Gindro K. Stilbenes: biomarkers of grapevine resistance to fungal diseases. OENO One. 2018;52(3):235–41.

11. Yobrégat O. Introduction to resistant vine types: a brief history and overview of the situation. OENO One. 2018;52:241–6. https://doi.org/10.20870/oeno-one.2018.52.3.2220.

12. De la Fuente Lloreda M. Use of hybrids in viticulture. A challenge for the OIV. OENO One. 2018;52(3):231–4. https://doi.org/10.20870/oeno-one.2018.52.3.2312.

13. Peressotti E, Wiedemann-Merdinoglu S, Delmotte F, Bellin D, Di Gaspero G, Testolin R, et al. Breakdown of resistance to grapevine downy mildew upon limited deployment of a resistant variety. BMC Plant Biology. 2010;10(1):147–. doi: 10.1186/1471-2229-10-147 20633270

14. Boller T, Felix G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol. 2009;60:379–406. Epub 2009/04/30. doi: 10.1146/annurev.arplant.57.032905.105346 19400727.

15. Yi SY, Shirasu K, Moon JS, Lee S-G, Kwon S-Y. The activated SA and JA signaling pathways have an influence on flg22-triggered oxidative burst and callose deposition. PloS one. 2014;9(2):e88951–e. doi: 10.1371/journal.pone.0088951 24586453.

16. Gomès E, Coutos-Thévenot P. Molecular Aspects of Grapevine-Pathogenic Fungi Interactions. In: Roubelakis-Angelakis KA, editor. Grapevine Molecular Physiology & Biotechnology. Dordrecht: Springer Netherlands; 2009. p. 407–28.

17. Bektas Y, Eulgem T. Synthetic plant defense elicitors. Frontier in Plant Science. 2015;5(804). doi: 10.3389/fpls.2014.00804 25674095

18. Hamiduzzaman MM, Jakab G, Barnavon L, Neuhaus JM, Mauch-Mani B. beta-Aminobutyric acid-induced resistance against downy mildew in grapevine acts through the potentiation of callose formation and jasmonic acid signaling. Molecular plant-microbe interactions: MPMI. 2005;18(8):819–29. Epub 2005/09/02. doi: 10.1094/MPMI-18-0819 16134894.

19. Aziz A, Trotel-Aziz P, Dhuicq L, Jeandet P, Couderchet M, Vernet G. Chitosan oligomers and copper sulfate induce grapevine defense reactions and resistance to gray mold and downy mildew. Phytopathology. 2006;96(11):1188–94. Epub 2008/10/24. doi: 10.1094/PHYTO-96-1188 18943955.

20. Trouvelot S, Varnier AL, Allegre M, Mercier L, Baillieul F, Arnould C, et al. A beta-1,3 glucan sulfate induces resistance in grapevine against Plasmopara viticola through priming of defense responses, including HR-like cell death. Molecular plant-microbe interactions: MPMI. 2008;21(2):232–43. Epub 2008/01/11. doi: 10.1094/MPMI-21-2-0232 18184067.

21. Allegre M, Heloir MC, Trouvelot S, Daire X, Pugin A, Wendehenne D, et al. Are grapevine stomata involved in the elicitor-induced protection against downy mildew? Molecular plant-microbe interactions: MPMI. 2009;22(8):977–86. Epub 2009/07/11. doi: 10.1094/MPMI-22-8-0977 19589073.

22. Delaunois B, Farace G, Jeandet P, Clement C, Baillieul F, Dorey S, et al. Elicitors as alternative strategy to pesticides in grapevine? Current knowledge on their mode of action from controlled conditions to vineyard. Environmental science and pollution research international. 2013;21(7):4837–46. Epub 2013/05/31. doi: 10.1007/s11356-013-1841-4 23719689.

23. Godard S, Slacanin I, Viret O, Gindro K. Induction of defence mechanisms in grapevine leaves by emodin- and anthraquinone-rich plant extracts and their conferred resistance to downy mildew. Plant Physiol Biochem. 2009;47(9):827–37. Epub 2009/05/19. doi: 10.1016/j.plaphy.2009.04.003 19447634.

24. Dagostin S, Formolo T, Giovannini O, Pertot I. Salvia officinalis Extract Can Protect Grapevine Against Plasmopara viticola. PLANT DISEASE n°5. 2010;94(36):575–80. doi: 10.1094/Pdis-94-5-0575 30754462

25. Soylu EM, Kurt Ş, Soylu S. In vitro and in vivo antifungal activities of the essential oils of various plants against tomato grey mould disease agent Botrytis cinerea. International Journal of Food Microbiology. 2010;143(3):183–9. doi: 10.1016/j.ijfoodmicro.2010.08.015 20826038

26. Pina-Vaz C, Goncalves Rodrigues A, Pinto E, Costa-de-Oliveira S, Tavares C, Salgueiro L, et al. Antifungal activity of Thymus oils and their major compounds. J Eur Acad Dermatol Venereol. 2004;18(1):73–8. Epub 2003/12/18. 14678536.

27. Soylu S, Yigitbas H, Soylu EM, Kurt S. Antifungal effects of essential oils from oregano and fennel on Sclerotinia sclerotiorum. Journal of applied microbiology. 2007;103(4):1021–30. Epub 2007/09/28. doi: 10.1111/j.1365-2672.2007.03310.x 17897206.

28. Soylu EM, Kurt S, Soylu S. In vitro and in vivo antifungal activities of the essential oils of various plants against tomato grey mould disease agent Botrytis cinerea. Int J Food Microbiol. 2010;143(3):183–9. Epub 2010/09/10. doi: 10.1016/j.ijfoodmicro.2010.08.015 20826038.

29. Dagostin S, Formolo T, Giovannini O, Pertot I, Schmitt A. Salvia officinalis Extract Can Protect Grapevine Against Plasmopara viticola. Plant Disease. 2010;94(5):575–80. doi: 10.1094/PDIS-94-5-0575 30754462

30. Turek C, Stintzing FC. Stability of Essential Oils: A Review. 2013;12(1):40–53. doi: 10.1111/1541-4337.12006

31. Janatova A, Bernardos A, Smid J, Frankova A, Lhotka M, Kourimská L, et al. Long-term antifungal activity of volatile essential oil components released from mesoporous silica materials. Industrial Crops and Products. 2015;67:216–20. https://doi.org/10.1016/j.indcrop.2015.01.019.

32. Oliveira Fialho R, Stradioto Papa MdF, Rodrigo Panosso A, Rodrigues Cassiolato A. Fungitoxicity of essential Oils on Plasmopora viticola, causal agent of grapevine downy mildew. Rev Bras Frutic,. 2017;39(4).

33. Burketova L, Trda L, Ott PG, Valentova O. Bio-based resistance inducers for sustainable plant protection against pathogens. Biotechnol Adv. 2015;33(6 Pt 2):994–1004. Epub 2015/01/27. doi: 10.1016/j.biotechadv.2015.01.004 25617476.

34. Sakkas H, Papadopoulou C. Antimicrobial Activity of Basil, Oregano, and Thyme Essential Oils. Journal of microbiology and biotechnology. 2017;27(3):429–38. Epub 2016/12/21. doi: 10.4014/jmb.1608.08024 27994215.

35. Rienth M, Torregrosa L, Ardisson M, De Marchi R, Romieu C. Versatile and efficient RNA extraction protocol for grapevine berry tissue, suited for next generation RNA sequencing. Australian Journal of Grape and Wine Research. 2014;20(2):247–54. doi: 10.1111/ajgw.12077

36. Leinonen R, Sugawara H, Shumway M. The sequence read archive. Nucleic Acids Res. 2011;39(Database issue):D19–21. Epub 2010/11/11. doi: 10.1093/nar/gkq1019 21062823; PubMed Central PMCID: PMC3013647.

37. Yin L, An Y, Qu J, Li X, Zhang Y, Dry I, et al. Genome sequence of Plasmopara viticola and insight into the pathogenic mechanism. Scientific Reports. 2017;7:46553. doi: 10.1038/srep46553 https://www.nature.com/articles/srep46553#supplementary-information. 28417959

38. Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015;12(4):357–60. Epub 2015/03/10. doi: 10.1038/nmeth.3317 25751142; PubMed Central PMCID: PMC4655817.

39. Anders S, Pyl PT, Huber W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31(2):166–9. Epub 2014/09/28. doi: 10.1093/bioinformatics/btu638 25260700; PubMed Central PMCID: PMC4287950.

40. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology. 2014;15(12):550. doi: 10.1186/s13059-014-0550-8 25516281

41. Al-Shahrour F, Diaz-Uriarte R, Dopazo J. FatiGO: a web tool for finding significant associations of Gene Ontology terms with groups of genes. Bioinformatics. 2004;20(4):578–80. Epub 2004/03/03. doi: 10.1093/bioinformatics/btg455 14990455.

42. Grimplet J, Van Hemert J, Carbonell-Bejerano P, Diaz-Riquelme J, Dickerson J, Fennell A, et al. Comparative analysis of grapevine whole-genome gene predictions, functional annotation, categorization and integration of the predicted gene sequences. BMC Research Notes. 2012;5(1):213. doi: 10.1186/1756-0500-5-213 22554261

43. Teixeira B, Marques A, Ramos C, Serrano C, Matos O, Neng NR, et al. Chemical composition and bioactivity of different oregano (Origanum vulgare) extracts and essential oil. J Sci Food Agric. 2013;93(11):2707–14. Epub 2013/04/05. doi: 10.1002/jsfa.6089 23553824.

44. Bozin B, Mimica-Dukic N, Simin N, Anackov G. Characterization of the Volatile Composition of Essential Oils of Some Lamiaceae Spices and the Antimicrobial and Antioxidant Activities of the Entire Oils. Journal of Agricultural and Food Chemistry. 2006;54(5):1822–8. doi: 10.1021/jf051922u 16506839

45. Bisht D, Chanotiya CS, Rana M, Semwal M. Variability in essential oil and bioactive chiral monoterpenoid compositions of Indian oregano (Origanum vulgare L.) populations from northwestern Himalaya and their chemotaxonomy. Industrial Crops and Products. 2009;30(3):422–6. https://doi.org/10.1016/j.indcrop.2009.07.014.

46. Boruga O, Jianu C, Misca C, Golet I, Gruia AT, Horhat FG. Thymus vulgaris essential oil: chemical composition and antimicrobial activity. Journal of medicine and life. 2014;7 Spec No. 3:56–60. Epub 2014/01/01. 25870697; PubMed Central PMCID: PMC4391421.

47. Mohamed A., Hamza A., A D. Recent approaches for controlling downy mildew of cucumber under greenhouse conditions., 52: 1–9. Plant Protect Sci. 2016;52:1–9.

48. Nazzaro F, Fratianni F, Coppola R, Feo VD. Essential Oils and Antifungal Activity. Pharmaceuticals (Basel, Switzerland). 2017;10(4):86. doi: 10.3390/ph10040086 29099084.

49. Nobrega RO, Teixeira AP, Oliveira WA, Lima EO, Lima IO. Investigation of the antifungal activity of carvacrol against strains of Cryptococcus neoformans. Pharmaceutical biology. 2016;54(11):2591–6. Epub 2016/05/27. doi: 10.3109/13880209.2016.1172319 27225838.

50. Chavan PS, Tupe SG. Antifungal activity and mechanism of action of carvacrol and thymol against vineyard and wine spoilage yeasts. Food Control. 2014;46:115–20. https://doi.org/10.1016/j.foodcont.2014.05.007.

51. Broekaert WF, Delauré SL, Bolle MFCD, Cammue BPA. The Role of Ethylene in Host-Pathogen Interactions. 2006;44(1):393–416. doi: 10.1146/annurev.phyto.44.070505.143440 16602950.

52. Pieterse CMJ, Does DVd, Zamioudis C, Leon-Reyes A, Wees SCMV. Hormonal Modulation of Plant Immunity. 2012;28(1):489–521. doi: 10.1146/annurev-cellbio-092910-154055 22559264.

53. Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P, Pastor V, et al. Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. Plant Cell Rep. 2013;32(7):1085–98. Epub 2013/04/16. doi: 10.1007/s00299-013-1441-2 23584548.

54. Larrieu A, Vernoux T. Q&A: How does jasmonate signaling enable plants to adapt and survive? BMC biology. 2016;14:79–. doi: 10.1186/s12915-016-0308-8 27643853.

55. Boubakri H, Wahab MA, Chong J, Bertsch C, Mliki A, Soustre-Gacougnolle I. Thiamine induced resistance to Plasmopara viticola in grapevine and elicited host-defense responses, including HR like-cell death. Plant Physiol Biochem. 2012;57:120–33. Epub 2012/06/16. doi: 10.1016/j.plaphy.2012.05.016 22698755.

56. Pajerowska-Mukhtar KM, Emerine DK, Mukhtar MS. Tell me more: roles of NPRs in plant immunity. Trends Plant Sci. 2013;18(7):402–11. Epub 2013/05/21. doi: 10.1016/j.tplants.2013.04.004 23683896.

57. Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Van Pelt JA, Mueller MJ, et al. NPR1 Modulates Cross-Talk between Salicylate- and Jasmonate-Dependent Defense Pathways through a Novel Function in the Cytosol. 2003;15(3):760–70. doi: 10.1105/tpc.009159 J The Plant Cell. 12615947

58. Backer R, Naidoo S, van den Berg N. The NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1) and Related Family: Mechanistic Insights in Plant Disease Resistance. Front Plant Sci. 2019;10(102). doi: 10.3389/fpls.2019.00102 30815005

59. Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, et al. The JAZ family of repressors is the missing link in jasmonate signalling. Nature. 2007;448(7154):666–71. Epub 2007/07/20. doi: 10.1038/nature06006 17637675.

60. Kazan K, Manners JM. JAZ repressors and the orchestration of phytohormone crosstalk. Trends in Plant Science. 2012;17(1):22–31. doi: 10.1016/j.tplants.2011.10.006 22112386

61. Proietti S, Caarls L, Coolen S, Van Pelt JA, Van Wees SCM, Pieterse CMJ. Genome-wide association study reveals novel players in defense hormone crosstalk in Arabidopsis. Plant, cell & environment. 2018;41(10):2342–56. Epub 2018/07/03. doi: 10.1111/pce.13357 29852537.

62. Caarls L, Pieterse CMJ, Van Wees SCM. How salicylic acid takes transcriptional control over jasmonic acid signaling. Frontiers in plant science. 2015;6:170–. doi: 10.3389/fpls.2015.00170 25859250.

63. Zheng Z, Qamar SA, Chen Z, Mengiste T. Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J. 2006;48(4):592–605. Epub 2006/10/25. doi: 10.1111/j.1365-313X.2006.02901.x 17059405.

64. Li J, Brader G, Kariola T, Palva ET. WRKY70 modulates the selection of signaling pathways in plant defense. Plant J. 2006;46(3):477–91. Epub 2006/04/21. doi: 10.1111/j.1365-313X.2006.02712.x 16623907.

65. Wang D, Amornsiripanitch N, Dong X. A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog. 2006;2(11):e123. Epub 2006/11/14. doi: 10.1371/journal.ppat.0020123 17096590; PubMed Central PMCID: PMC1635530.

66. Pandey SP, Somssich IE. The Role of WRKY Transcription Factors in Plant Immunity. 2009;150(4):1648–55. doi: 10.1104/pp.109.138990 J Plant Physiology. 19420325

67. Paul PK, Sharma PD. Azadirachta indica leaf extract induces resistance in barley against leaf stripe disease. Physiological and Molecular Plant Pathology. 2002;61(1):3–13. https://doi.org/10.1006/pmpp.2002.0412.

68. Gao Q-M, Zhu S, Kachroo P, Kachroo A. Signal regulators of systemic acquired resistance. Frontiers in plant science. 2015;6:228–. doi: 10.3389/fpls.2015.00228 25918514.

69. Vergnes S, Ladouce N, Fournier S, Ferhout H, Attia F, Dumas B. Foliar treatments with Gaultheria procumbens essential oil induce defense responses and resistance against a fungal pathogen in Arabidopsis. 2014;5(477). doi: 10.3389/fpls.2014.00477 25295045

70. von Rad U, Mueller MJ, Durner J. Evaluation of natural and synthetic stimulants of plant immunity by microarray technology. New Phytol. 2005;165(1):191–202. Epub 2005/02/22. doi: 10.1111/j.1469-8137.2004.01211.x 15720633.

71. Gullner G, Komives T, Kiraly L, Schroder P. Glutathione S-Transferase Enzymes in Plant-Pathogen Interactions. Front Plant Sci. 2018;9:1836. Epub 2019/01/10. doi: 10.3389/fpls.2018.01836 30622544; PubMed Central PMCID: PMC6308375.

72. Suzuki N, Sejima H, Tam R, Schlauch K, Mittler R. Identification of the MBF1 heat-response regulon of Arabidopsis thaliana. The Plant Journal. 2011;66:844–51. doi: 10.1111/j.1365-313X.2011.04550.x 21457365

73. Suzuki N, Koussevitzky S, Mittler R, Miller G. ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ. 2012;35(2):259–70. Epub 2011/04/14. doi: 10.1111/j.1365-3040.2011.02336.x 21486305.

74. Rienth M, Torregrosa L, Sarah G, Ardisson M, Brillouet J-M, Romieu C. Temperature desynchronizes sugar and organic acid metabolism in ripening grapevine fruits and remodels their transcriptome. BMC Plant Biology. 2016;16(1):164. doi: 10.1186/s12870-016-0850-0 27439426

75. Rienth M, Torregrosa L, Kelly MT, Luchaire N, Pellegrino A, Grimplet Jrm, et al. Is Transcriptomic Regulation of Berry Development More Important at Night than During the Day? PLoS One. 2014;9(2):e88844. doi: 10.1371/journal.pone.0088844 24551177

76. Rienth M, Torregrosa L, Luchaire N, Chatbanyong R, Lecourieux D, Kelly M, et al. Day and night heat stress trigger different transcriptomic responses in green and ripening grapevine (vitis vinifera) fruit. BMC Plant Biology. 2014;14(1):108. doi: 10.1186/1471-2229-14-108 24774299

77. Torregrosa L, Rienth M, Romieu C, Pellegrino A. The microvine, a model for studies in grapevine physiology and genetics. OENO One. 2019;53(3). doi: 10.20870/oeno-one.2019.53.3.2409

78. Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. AP2/ERF family transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta (BBA)—Gene Regulatory Mechanisms. 2012;1819(2):86–96. https://doi.org/10.1016/j.bbagrm.2011.08.004.

79. Bahieldin A, Atef A, Edris S, Gadalla NO, Ali HM, Hassan SM, et al. Ethylene responsive transcription factor ERF109 retards PCD and improves salt tolerance in plant. 2016;16(1):216. doi: 10.1186/s12870-016-0908-z 27716054

80. Kumar M, Brar A, Yadav M, Chawade A, Vivekanand V, Pareek N. Chitinases—Potential Candidates for Enhanced Plant Resistance towards Fungal Pathogens. 2018;8(7):88. doi: 10.3390/agriculture8070088

81. Hakim, Ullah A, Hussain A, Shaban M, Khan AH, Alariqi M, et al. Osmotin: A plant defense tool against biotic and abiotic stresses. Plant Physiology and Biochemistry. 2018;123:149–59. doi: 10.1016/j.plaphy.2017.12.012 29245030

82. Gauthier A, Trouvelot S, Kelloniemi J, Frettinger P, Wendehenne D, Daire X, et al. 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. 2014;9(2):e88145. doi: 10.1371/journal.pone.0088145 24516597

83. Rasmussen M, Roux M, Petersen M, Mundy J. MAP Kinase Cascades in Arabidopsis Innate Immunity. 2012;3(169). doi: 10.3389/fpls.2012.00169 22837762

84. Tsuda K, Mine A, Bethke G, Igarashi D, Botanga CJ, Tsuda Y, et al. Dual regulation of gene expression mediated by extended MAPK activation and salicylic acid contributes to robust innate immunity in Arabidopsis thaliana. PLoS Genet. 2013;9(12):e1004015. Epub 2013/12/19. doi: 10.1371/journal.pgen.1004015 24348271; PubMed Central PMCID: PMC3861249 adherence to all PLoS Genetics policies on sharing data and materials.

85. Su J, Yang L, Zhu Q, Wu H, He Y, Liu Y, et al. Active photosynthetic inhibition mediated by MPK3/MPK6 is critical to effector-triggered immunity. PLOS Biology. 2018;16(5):e2004122. doi: 10.1371/journal.pbio.2004122 29723186

86. Shoresh M, Gal-On A, Leibman D, Chet I. Characterization of a Mitogen-Activated Protein Kinase Gene from Cucumber Required for Trichoderma-Conferred Plant Resistance. Plant Physiol. 2006;142(3):1169–79. doi: 10.1104/pp.106.082107 J Plant Physiology. 16950863

87. Genot B, Lang J, Berriri S, Garmier M, Gilard F, Pateyron S, et al. Constitutively Active Arabidopsis MAP Kinase 3 Triggers Defense Responses Involving Salicylic Acid and SUMM2 Resistance Protein. Plant Physiology. 2017;174(2):1238–49. doi: 10.1104/pp.17.00378 28400495

88. Kwaaitaal M, Huisman R, Maintz J, Reinstädler A, Panstruga R. Ionotropic glutamate receptor (iGluR)-like channels mediate MAMP-induced calcium influx in Arabidopsis thaliana. 2011;440(3):355–73. doi: 10.1042/BJ20111112 J Biochemical Journal. 21848515

89. CyanoBase.

90. Zhu X, Caplan J, Mamillapalli P, Czymmek K, Dinesh-Kumar SP. Function of endoplasmic reticulum calcium ATPase in innate immunity-mediated programmed cell death. Embo j. 2010;29(5):1007–18. Epub 2010/01/16. doi: 10.1038/emboj.2009.402 20075858; PubMed Central PMCID: PMC2837167.

91. Lam E, Kato N, Lawton M. Programmed cell death, mitochondria and the plant hypersensitive response. Nature. 2001;411(6839):848–53. Epub 2001/07/19. doi: 10.1038/35081184 11459068.

92. Stael S, Kmiecik P, Willems P, Van Der Kelen K, Coll NS, Teige M, et al. Plant innate immunity—sunny side up? Trends in plant science. 2015;20(1):3–11. Epub 2014/10/29. doi: 10.1016/j.tplants.2014.10.002 25457110.

93. Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, et al. Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell. 2004;16(12):3460–79. doi: 10.1105/tpc.104.025833 15548743.

94. Vanlerberghe GC. Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. Int J Mol Sci. 2013;14(4):6805–47. Epub 2013/03/28. doi: 10.3390/ijms14046805 23531539; PubMed Central PMCID: PMC3645666.

95. Piasecka A, Jedrzejczak-Rey N, Bednarek P. Secondary metabolites in plant innate immunity: conserved function of divergent chemicals. New Phytol. 2015;206(3):948–64. Epub 2015/02/11. doi: 10.1111/nph.13325 25659829.

96. Scholasch T, Rienth M. Review of water deficit mediated changes in vine and berry physiology; Consequences for the optimization of irrigation strategies. OENO One. 2019;53(3). https://doi.org/10.20870/oeno-one.2019.53.3.2407.

97. Mierziak J, Kostyn K, Kulma A. Flavonoids as important molecules of plant interactions with the environment. Molecules. 2014;19(10):16240–65. Epub 2014/10/14. doi: 10.3390/molecules191016240 25310150.

98. Fofana B, McNally DJ, Labbé C, Boulanger R, Benhamou N, Séguin A, et al. Milsana-induced resistance in powdery mildew-infected cucumber plants correlates with the induction of chalcone synthase and chalcone isomerase. Physiological and Molecular Plant Pathology. 2002;61(2):121–32. https://doi.org/10.1006/pmpp.2002.0420.

99. Richard T, Abdelli-Belhad A, Vitrac X, Waffo-Téguo P, Mérillon J-M. Vitis vinifera canes, a source of stilbenoids against downy mildew. OENO One. 2016;50(3). https://doi.org/10.20870/oeno-one.2016.50.3.1178.

100. Höll J, Vannozzi A, Czemmel S, D'Onofrio C, Walker AR, Rausch T, et al. The R2R3-MYB Transcription Factors MYB14 and MYB15 Regulate Stilbene Biosynthesis in Vitis vinifera. 2013;25(10):4135–49. doi: 10.1105/tpc.113.117127 J The Plant Cell. 24151295

101. Belhadj A, Telef N, Saigne C, Cluzet S, Barrieu F, Hamdi S, et al. Effect of methyl jasmonate in combination with carbohydrates on gene expression of PR proteins, stilbene and anthocyanin accumulation in grapevine cell cultures. Plant Physiol Biochem. 2008;46:493–9. doi: 10.1016/j.plaphy.2007.12.001 18294857

102. D'Onofrio C, Cox A, Davies C, Boss P. Induction of secondary metabolism in grape cell cultures by jasmonates. Funct Plant Biol. 2009;36:323–38.

103. Garde-Cerdan T, Gutiérrez-Gamboa G. P-Á, E. P., Rubio-Bretón P. Foliar application of methyl jasmonate to Graciano and Tempranillo vines: effects on grape amino acid content during two consecutive vintages. OENO One,. 2019; 53(1). https://doi.org/10.20870/oeno-one.2019.53.1.2163.

104. La Torre A, Mandalà C, Pezza L, Caradonia F, Battaglia V. Evaluation of essential plant oils for the control of Plasmopara viticola. Journal of Essential Oil Research. 2014;26(4):282–91. doi: 10.1080/10412905.2014.889049

105. Kordali S, Cakir A, Ozer H, Cakmakci R, Kesdek M, Mete E. Antifungal, phytotoxic and insecticidal properties of essential oil isolated from Turkish Origanum acutidens and its three components, carvacrol, thymol and p-cymene. Bioresource Technology. 2008;99(18):8788–95. doi: 10.1016/j.biortech.2008.04.048 18513954

106. de Almeida LFR, Frei F, Mancini E, De Martino L, De Feo V. Phytotoxic activities of Mediterranean essential oils. Molecules (Basel, Switzerland). 2010;15(6):4309–23. doi: 10.3390/molecules15064309 20657443.

107. Amri IS, Hamrouni L, Hananac M, Jamoussi B. REVIEWS ON PHYTOTOXIC EFFECTS OF ESSENTIAL OILS AND THEIR INDIVIDUAL COMPONENTS: NEWS APPROACH FOR WEEDS MANAGEMENT. International Journal of Applied Biology and Pharmaceutical Technology. 2012:96–114.

108. Duchêne E, Dumas V, Jaegli N, Merdinoglu D. Genetic variability of descriptors for grapevine berry acidity in Riesling, Gewürztraminer and their progeny. Australian Journal of Grape and Wine Research. 2014;20(1):91–9. doi: 10.1111/ajgw.12051

109. Merdinoglu D, Schneider C, Prado E, Wiedemann-Merdinoglu S, Mestre P. Breeding for durable resistance to downy and powdery mildew in grapevine. 52(3), 203–209. OENO One. 2018;52(3):103–209. https://doi.org/10.20870/oeno-one.2018.52.3.2116.

110. Torregrosa L, Bigard A, Doligez A, Lecourieux D, Rienth M, Luchaire N, et al. Developmental, molecular and genetic studies on grapevine response to temperature open breeding strategies for adaptation to warming. OENO One. 2017;51(2):155–65. https://doi.org/10.20870/oeno-one.2017.51.2.1587.


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