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Journal of Plant Growth Regulation

, Volume 38, Issue 2, pp 723–738 | Cite as

Elevated α-Linolenic Acid Content in Extra-plastidial Membranes of Tomato Accelerates Wound-Induced Jasmonate Generation and Improves Tolerance to the Herbivorous Insects Heliothis peltigera and Spodoptera littoralis

  • Meng Zhang
  • Yonatan Demeshko
  • Rita Dumbur
  • Tim Iven
  • Ivo Feussner
  • Galina Lebedov
  • Murad Ganim
  • Rivka BargEmail author
  • Gozal Ben-HayyimEmail author
Article
  • 142 Downloads

Abstract

In tomato, desaturation of linoleic acid (18:2) to α-linolenic acid (18:3) is mediated in the plastidial membranes by the ω-3 fatty acid desaturases 7 (FAD7), and in the ER membrane by its paralog FAD3. According to the prevalent model, the hormone jasmonic acid isoleucine (JA-Ile), which plays a key role in the plant response to various stresses, including wounding and herbivores attack, is derived from 18:3 which is released from the plastidial membrane glycerolipids. The current work aimed at assessing in tomato the effects of ectopic FAD3 over-expression or SlFAD7 silencing on herbivore tolerance and on wound response. The tomato SlFAD7 gene encoding for the plastidial-residing FAD7 was silenced by RNA interference, and enhanced expression of the extra-plastidial ER-residing FAD3 was induced by ectopic expression of BnFAD3. Over-expression of BnFAD3 led to increase, whereas SlFAD7 silencing led to decrease in 18:3 content in the extra-plastidial and plastidial membrane, respectively. As anticipated, silencing SlFAD7 attenuated the accumulation of JA-Ile following wounding, and enhanced susceptibility to two important pest insects: the chewing herbivores Spodoptera littoralis and Heliothis peltigera. Unexpected was the finding that ectopic over-expression of the extra-plastidial ER-residing FAD3 accelerated both wound-induced JA-Ile accumulation and expression of wound-response marker genes. Furthermore, BnFAD3 over-expression significantly improved the tomato tolerance to these two chewing herbivores. The presented information supports the notion that 18:3 derived from extra-plastidial membranes may serve as a substrate for, or as a source for a cue triggering, JA-Ile biosynthesis in response to wounding and insect chewing.

Keywords

FAD Solanum lycopersicon Fatty acid Wounding Herbivory Jasmonate 

Notes

Acknowledgements

We thank Dr. Yehiam Salts, ARO, Israel, for assistance in primers design, and Prof. Yuval Eshed, Weizmann Institute of Science, Rehovot, Israel, for the pRNA69 and pART27 plasmids. The technical assistance of Sabine Freitag, (Georg-August-University, Göttingen, Germany), Chen Klap, and Sara Shabtai (ARO, Israel) is greatly appreciated.

Funding

This work was supported by the United States-Israel Binational Agricultural Research and Development BARD fund (Grant No. TB-8050-08), and by the Chief Scientist Fund, Ministry of Agriculture, Israel (Grant No. 204-442-01).

Compliance with Ethical Standards

Conflict of interest

We declare that there is no conflict of interest in this research.

Supplementary material

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References

  1. Abe H, Ohnishi J, Narusaka M, Seo S, Narusaka Y, Tsuda S, Kobayashi M (2008) Function of jasmonate in response and tolerance of Arabidopsis to thrip feeding. Plant Cell Physiol 49:68–80CrossRefGoogle Scholar
  2. Ameye M, Allmann S, Verwaeren J, Smagghe G, Haesaert G, Schuurink RC, Audenaert K (2017) Green leaf volatile production by plants: a meta-analysis. New Phytol.  https://doi.org/10.1111/nph.14671 Google Scholar
  3. Andreu V, Collados R, Testillano PS, Risueño MC, Picorel R, Alfonso M (2007) In situ molecular identification of the plastid omega3 fatty acid desaturase FAD7 from soybean: evidence of thylakoid membrane localization. Plant Physiol 145:1336–1344CrossRefGoogle Scholar
  4. Awai K, Xu C, Tamot B, Benning C (2006) A phosphatidic acid-binding protein of the chloroplast inner envelope membrane involved in lipid trafficking. Proc Natl Acad Sci USA 103:10817–10822CrossRefGoogle Scholar
  5. Barg R, Sobolev I, Eilon T, Gur A, Chmelnitsky I, Shabtai S, Grotewold E, Salts Y (2005) The tomato early fruit specific gene Lefsm1 defines a novel class of plant-specific SANT/MYB domain proteins. Planta 221:197–211CrossRefGoogle Scholar
  6. Bargmann BO, Laxalt AM, ter Riet B, Testerink C, Merquiol E, Mosblech A, Leon-Reyes A, Pieterse CM, Haring MA, Heilmann I, Bartels D, Munnik T (2009) Reassessing the role of phospholipase D in the Arabidopsis wounding response. Plant Cell Environ 32:837–850CrossRefGoogle Scholar
  7. Berberich T, Harada M, Sugawara K, Kodama H, Iba K, Kusano T (1998) Two maize genes encoding omega-3 fatty acid desaturase and their differential expression to temperature. Plant Mol Biol 36:297–306CrossRefGoogle Scholar
  8. Bergey DR, Howe GA, Ryan CA (1996) Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. Proc Natl Acad Sci USA 93:12053–12058CrossRefGoogle Scholar
  9. Browse J, McConn M, James D, Miquel M (1993) Mutants of Arabidopsis deficient in the synthesis of a-linolenate: biological and genetic characterization of the endoplasmic reticulum linoleoyl desaturase. J Biol Chem 268:16345–16351Google Scholar
  10. Bruckhoff V, Haroth S, Feussner K, König S, Brodhun F, Feussner I (2016) Functional characterization of cyp94-genes and identification of a novel jasmonate catabolite in flowers. PLoS ONE 11:e0159875CrossRefGoogle Scholar
  11. Caarls L, Pieterse CM, Van Wees SC (2015) How salicylic acid takes transcriptional control over jasmonic acid signaling. Front Plant Sci 6:170CrossRefGoogle Scholar
  12. Carmi N, Salts Y, Dedicova B, Shabtai S, Barg R (2003) Induction of parthenocarpy in tomato via specific expression of the rolB gene in the ovary. Planta 217:726–735CrossRefGoogle Scholar
  13. Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA (2005) Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proc Natl Acad Sci USA 102:19237–19242CrossRefGoogle Scholar
  14. Chini A, Monte I, Zamarreño AM, Hamberg M, Lassueur S, Reymond P, Weiss S, Stintzi A, Schaller A, Porzel A, García-Mina JM, Solano R (2018) Identification of an OPR3-independent pathway for jasmonate biosynthesis. Nat Chem Biol 14:171–178CrossRefGoogle Scholar
  15. Christensen SA, Nemchenko A, Borrego E, Murray I, Sobhy IS, Bosak L, DeBlasio S, Erb M, Robert CA, Vaughn KA, Herrfurth C, Tumlinson J, Feussner I, Jackson D, Turlings TC, Engelberth J, Nansen C, Meeley R, Kolomiets MV (2013) The maize lipoxygenase, ZmLOX10, mediates green leaf volatile, jasmonate and herbivore-induced plant volatile production for defense against insect attack. Plant J 74:59–73CrossRefGoogle Scholar
  16. Collados R, Andreu V, Picorel R, Alfonso M (2006) A light-sensitive mechanism differently regulates transcription and transcript stability of x3 fatty-acid desaturases (FAD3, FAD7 and FAD8) in soybean photosynthetic cell suspensions. FEBS Lett 580:4934–4940CrossRefGoogle Scholar
  17. Conconi A, Miquel M, Browse JA, Ryan CA (1996) Intracellular levels of free linolenic and linoleic acids increase in tomato leaves in response to wounding. Plant Physiol 111:797–803CrossRefGoogle Scholar
  18. Conrath U, Beckers GJ, Flors V, García-Agustín P, Jakab G, Mauch F, Newman MA, Pieterse CM, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19:1062–1071CrossRefGoogle Scholar
  19. De Domenico S, Tsesmetzis N, Di Sansebastiano GP, Hughes RK, Casey R, Santino A (2007) Subcellular localisation of Medicago truncatula 9/13-hydroperoxide lyase reveals a new localisation pattern and activation mechanism for CYP74C enzymes. BMC Plant Biol 7:58CrossRefGoogle Scholar
  20. Demchenko K, Zdyb A, Feussner I, Pawlowski K (2012) Analysis of the subcellular localisation of lipoxygenase in legume and actinorhizal nodules. Plant Biol 14:56–63Google Scholar
  21. Domínguez T, Hernández ML, Pennycooke JC, Jiménez P, Martínez-Rivas JM, Sanz C, Stockinger EJ, Sánchez-Serrano JJ, Sanmartín M (2010) Increasing ω-3 desaturase expression in tomato results in altered aroma profile and enhanced resistance to cold stress. Plant Physiol 153:655–665CrossRefGoogle Scholar
  22. Dunkelblum E, Kehat M (1989) Female sex pheromone components of Heliothis peltigera (Lepidoptera: Noctuidae) chemical identification from gland extracts and male response. ‎J Chem Ecol 15:2233–2245CrossRefGoogle Scholar
  23. Dyer JM, Mullen RT (2001) Immunocytological localization of two plant fatty acid desaturases in the endoplasmic reticulum. FEBS Lett 494:44–47CrossRefGoogle Scholar
  24. Ellinger D, Stingl N, Kubigsteltig II, Bals T, Juenger M, Pollmann S, Berger S, Schuenemann D, Mueller MJ (2010) DONGLE and DEFECTIVE IN ANTHER DEHISCENCE1 lipases are not essential for wound- and pathogen-induced jasmonate biosynthesis: redundant lipases contribute to jasmonate formation. Plant Physiol 153:14–127CrossRefGoogle Scholar
  25. Farmer EE, Ryan CA (1990) Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci USA 87:7713–7716CrossRefGoogle Scholar
  26. Farmer EE, Ryan CA (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4:129–134CrossRefGoogle Scholar
  27. Farmer EE, Johnson RR, Ryan CA (1992) Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic Acid. Plant Physiol 98:995–1002CrossRefGoogle Scholar
  28. Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol 53:275–297CrossRefGoogle Scholar
  29. Froehlich JE, Itoh A, Howe GA (2001) Tomato allene oxide synthase and fatty acid hydroperoxide lyase, two cytochrome P450s involved in oxylipin metabolism, are targeted to different membranes of chloroplast envelope. Plant Physiol 125:306–317CrossRefGoogle Scholar
  30. Frost CJ, Mescher MC, Carlson JE, De Moraes CM (2008) Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol 146:818–824CrossRefGoogle Scholar
  31. Gfeller A, Dubugnon L, Liechti R, Farmer EE (2010) Jasmonate biochemical pathway. Sci Signal 3:cm4Google Scholar
  32. Ghanim M, Lebedev G, Kontsedalov S, Ishaaya I (2011) Flufenerim, a novel insecticide acting on diverse insect pests: biological mode of action and biochemical aspects. J Agric Food Chem 59:2839–2844CrossRefGoogle Scholar
  33. Gibson S, Arondel V, Iba K, Somerville C (1994) Cloning of a temperature-regulated gene encoding a chloroplast omega-3 desaturase from Arabidopsis thaliana. Plant Physiol 106:1615–1621CrossRefGoogle Scholar
  34. Goetz S, Hellwege A, Stenzel I, Kutter C, Hauptmann V, Forner S, McCaig B, Hause G, Miersch O, Wasternack C, Hause B (2012) Role of cis-12-oxo-phytodienoic acid in tomato embryo development. Plant Physiol 158:1715–1727CrossRefGoogle Scholar
  35. Goossens J, Ferna´ndez-Calvo P, Schweizer F, Goossens A (2016) Jasmonates: signal transduction components and their roles in environmental stress responses. Plant Mol Biol 91:673–689CrossRefGoogle Scholar
  36. Halitschke R, Baldwin IT (2005) Jasmonates and related compounds in plant-insect interactions. J Plant Growth Reg 23:238–245CrossRefGoogle Scholar
  37. Horowitz AR, Weintraub PG, Ishaaya I (1998) Status of pesticide resistance in arthropod pests in Israel. Phytoparasitica 26:231–240CrossRefGoogle Scholar
  38. Hou Q, Ufer G, Bartels D (2016) Lipid signalling in plant responses to abiotic stress. Plant Cell Environ 39:1029–1048CrossRefGoogle Scholar
  39. Howe GA (2018) Metabolic end run to jasmonate. Nature Chem Biol 14:109–110CrossRefGoogle Scholar
  40. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66CrossRefGoogle Scholar
  41. Ishiguro S, Kawai-Oda A, Ueda J, Nishida I, Okada K (2001) The DEFECTIVE IN ANTHER DEHISCIENCE gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13:2191–2209CrossRefGoogle Scholar
  42. Iven T, König S, Singh S, Braus-Stromeyer SA, Bischoff M, Tietze LF, Braus GH, Lipka V, Feussner I, Dröge-Laser W (2012) Transcriptional activation and production of tryptophan-derived secondary metabolites in Arabidopsis roots contributes to the defense against the fungal vascular pathogen Verticillium longisporum. Mol Plant 5:1389–1402CrossRefGoogle Scholar
  43. Kang JH, Wang L, Giri A, Baldwin IT (2006) Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairs jasmonic acid-isoleucine-mediated defenses against Manduca sexta. Plant Cell 18:3303–3320CrossRefGoogle Scholar
  44. Karimzadeh J, Mohammadipou A (2011) Studies on population dynamics and regulatory factors (biotic vs. abiotic and bottom-up vs. top-down) of the pest species belonging to genera Helicoverpa and Heliothis (Lepidoptera: Noctuidae) on cotton, chickpea and tomato [2011]. http://agris.fao.org/agris-search/search.do?recordID=IR2012014242
  45. Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328CrossRefGoogle Scholar
  46. Koo AJ, Thireault C, Zemelis S, Poudel AN, Zhang T, Kitaoka N, Brandizzi F, Matsuura H, Howe GA (2014) Endoplasmic reticulum-associated inactivation of the hormone jasmonoyl-L-isoleucine by multiple members of the cytochrome P450 94 family in Arabidopsis. J Biol Chem 289:29728–29738CrossRefGoogle Scholar
  47. Lebedev G, Gafni G, Ben-Yakir D, Ghanim M (2012) High-level of resistance to spinosad, emamectin benzoate and carbosulfan in populations of Thrips tabaci collected in Israel. Pest Manag Sci 69:274–277CrossRefGoogle Scholar
  48. Lee KR, Lee Y, Kim EH, Lee SB, Roh KH, Kim JB, Kang HC, Kim HU (2016) Functional identification of oleate 12-desaturase and ω-3 fatty acid desaturase genes from Perilla frutescens var. frutescens. Plant Cell Rep 35:2523–2537CrossRefGoogle Scholar
  49. León J (2013) Role of plant peroxisomes in the production of jasmonic acid-based signals. Subcell Biochem 69:299–313CrossRefGoogle Scholar
  50. Li L, Li C, Lee GI, Howe GA (2002) Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc Natl Acad Sci USA 99:6416–6421CrossRefGoogle Scholar
  51. Li C, Liu G, Xu C, Lee GI, Bauer P, Ling H-Q, Gana 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 15:1646–1661CrossRefGoogle Scholar
  52. Li XR, Li HJ, Yuan L, Liu M, Shi DQ, Liu J, Yang WC (2014) Arabidopsis DAYU/ABERRANT PEROXISOME MORPHOLOGY9 is a key regulator of peroxisome biogenesis and plays critical roles during pollen maturation and germination in planta. Plant Cell 26:619–635CrossRefGoogle Scholar
  53. Machemer K, Shaiman O, Salts Y, Shabtai S, Sobolev I, Belausov E, Grotewold E, Barg R (2011) Interplay of MYB factors in differential cell expansion, and consequences for tomato fruit development. Plant J 68:337–350CrossRefGoogle Scholar
  54. Matsuda O, Sakamoto H, Hashimoto T, Iba K (2005) A temperature-sensitive mechanism that regulates post-translational stability of a plastidial omega-3 fatty acid desaturase (FAD8) in Arabidopsis leaf tissues. J Biol Chem 280:3597–3604CrossRefGoogle Scholar
  55. Matsui K, Kurishita S, Hisamitsu A, Kajiwara T (2000) A lipid-hydrolysing activity involved in hexenal formation. Biochem Soc Trans 28:857–860CrossRefGoogle Scholar
  56. Matsui K, Sugimoto K, Mano J, Ozawa R, Takabayashi J (2012) Differential metabolisms of green leaf volatiles in injured and intact parts of a wounded leaf meet distinct ecophysiological requirements. PLoS ONE 7:e36433CrossRefGoogle Scholar
  57. McCartney AW, Dyer JM, Dhanoa PK, Kim PK, Andrews DW, McNew JA, Mullen RT (2004) Membrane-bound fatty acid desaturases are inserted co-translationally into the ER and contain different ER retrieval motifs at their carboxy termini. Plant J 37:156–173CrossRefGoogle Scholar
  58. McConn M, Browse J (1996) The critical requirement for linolenic acid is pollen development, not photosynthesis, in an arabidopsis mutant. Plant Cell 8:403–416CrossRefGoogle Scholar
  59. McConn M, Creelman RA, Bell E, Mullet JE, Browse J (1997) Jasmonate is essential for insect defense in Arabidopsis. Proc Natl Acad Sci USA 94:5473–5477CrossRefGoogle Scholar
  60. Miquel M, Browse J (1992) Arabidopsis mutants deficient in polyunsaturated fatty acid synthesis. J Biol Chem 267:1502–1509Google Scholar
  61. Mita G, Quarta A, Fasano P, De Paolis A, Di Sansebastiano GP, Perrotta C, Iannacone R, Belfield E, Hughes R, Tsesmetzis N, Casey R, Santino A (2005) Molecular cloning and characterization of an almond 9-hydroperoxide lyase, a new CYP74 targeted to lipid bodies. J Exp Bot 56:2321–2333CrossRefGoogle Scholar
  62. Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970CrossRefGoogle Scholar
  63. Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521CrossRefGoogle Scholar
  64. Ryan CA (1990) Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annu Rev Phytopathol 28:425–449CrossRefGoogle Scholar
  65. Samach A, Hareven D, Gutfinger T, Ken-Dror S, Lifschitz E (1991) Biosynthetic threonine deaminase gene of tomato: isolation, structure, and upregulation in floral organs. Proc Natl Acad Sci USA 88:2678–2682CrossRefGoogle Scholar
  66. Sánchez-Hernández C, López MG, Délano-Frier JP (2006) Reduced levels of volatile emissions in jasmonate-deficient spr2 tomato mutants favour oviposition by insect herbivores. Plant Cell Environ 29:546–557CrossRefGoogle Scholar
  67. Shorey HH, Hale RL (1965) Mass-rearing of the larvae of nine noctuid species on a simple artificial Medium. J Econ Entomol 58:522–524CrossRefGoogle Scholar
  68. Stotz HU, Koch T, Biedermann A, Weniger K, Boland W, Mitchell-Olds T (2002) Evidence for regulation of resistance in Arabidopsis to Egyptian cotton worm by salicylic and jasmonic acid signaling pathways. Planta 214:648–652CrossRefGoogle Scholar
  69. ul Hassan MN, Zainal Z, Ismail I (2015) Green leaf volatiles: biosynthesis, biological functions and their applications in biotechnology. Plant Biotechnol J 13:727–739CrossRefGoogle Scholar
  70. Upchurch RG (2008) Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnol Lett 30:967–977CrossRefGoogle Scholar
  71. van de Ven WTG, LeVesque CS, Perring TM, Walling LL (2000) Local and systemic changes in squash gene expression in response to silverleaf whitefly feeding. Plant Cell 12:1409–1424CrossRefGoogle Scholar
  72. Vos IA, Pieterse CMJ, Van Wees SCM (2013) Costs and benefits of hormone-regulated plant defences. Plant Pathol 62:43–55CrossRefGoogle Scholar
  73. Walley JW, Kliebenstein DJ, Bostock RM, Dehesh K (2013) Fatty acids and early detection of pathogens. Curr Opi Plant Biol 16:520–526CrossRefGoogle Scholar
  74. Wallis JG, Browse J (2002) Mutants of Arabidopsis reveal many roles for membrane lipids. Prog Lipid Res 41:254–278CrossRefGoogle Scholar
  75. Wang C, Avdiushko S, Hildebrand DF (1999) Overexpression of a cytoplasm-localized allene oxide synthase promotes the wound-induced accumulation of jasmonic acid in transgenic tobacco. Plant Mol Biol 40:783–793CrossRefGoogle Scholar
  76. Wang HS, Yu C, Tang XF, Wang LY, Dong XC, Meng QW (2010) Antisense-mediated depletion of tomato endoplasmic reticulum omega-3 fatty acid desaturase enhances thermal tolerance. J Integr Plant Biol 52:568–577CrossRefGoogle Scholar
  77. Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review. Ann Bot 111:1021–1058CrossRefGoogle Scholar
  78. Wasternack C, Hause B (2018) A Bypass in jasmonate in biosynthesis—the OPR3-independent formation. Trends Plant Sci 23:276–279CrossRefGoogle Scholar
  79. Wasternack C, Strnad M (2016) Jasmonate signaling in plant stress responses and development—active and inactive compounds. New Biotechnol 33:604–613CrossRefGoogle Scholar
  80. Zhang M, Barg R, Yin M, Gueta-Dahan Y, Leikin-Frenkel A, Salts Y, Shabtai S, Ben-Hayyim G (2005) Modulated fatty acid desaturation via overexpression of two distinct ω-3 desaturases differentially alters tolerance to various abiotic stresses in transgenic tobacco cells and plants. Plant J 44:361–371CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.The Institute of Plant SciencesThe Volcani Center, Agricultural Research OrganizationRishon LeZionIsrael
  2. 2.College of AgronomyNorthwest A&F UniversityYanglingChina
  3. 3.Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant SciencesGeorg-August-UniversityGöttingenGermany
  4. 4.Department of Plant Biochemistry, Goettingen Center for Molecular Biosciences (GZMB)Georg-August-UniversityGöttingenGermany
  5. 5.Institute of Plant Protection, The Volcani CenterAgricultural Research OrganizationRishon LeZionIsrael

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