Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 49, 2012, Pages 20124-20129

  Bleeker, Petra M ^a   Mirabella, Rossana ^a   Diergaarde, Paul J ^b   VanDoorn, Arjen ^b   Tissier, Alain ^c   Kant, Merijn R ^d   Prins, Marcel ^b   De Vos, Martin ^b   Haring, Michel A ^a   Schuurink, Robert C ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b KEYGENE N V   (Netherlands)

^c LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Metabolic engineering; Promoter; Spider mite; Terpenoid; White fly

Indexed keywords

7 EPIZINGIBERENE SYNTHASE; FARNESYL DIPHOSPHATE; SESQUITERPENE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVITY; HERBIVORE; NONHUMAN; PEST RESISTANCE; PLANT BREEDING; PLANT CELL; PLANT LEAF; PLASTID; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPECIES CULTIVATION; TOMATO; TRICHOME;

ALKYL AND ARYL TRANSFERASES; ANALYSIS OF VARIANCE; ANIMALS; BIOSYNTHETIC PATHWAYS; BREEDING; CLONING, MOLECULAR; FEEDING BEHAVIOR; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; HEMIPTERA; HERBIVORY; LYCOPERSICON ESCULENTUM; METABOLIC ENGINEERING; POLYISOPRENYL PHOSPHATES; REAL-TIME POLYMERASE CHAIN REACTION; SESQUITERPENES; TETRANYCHIDAE;

LYCOPERSICON ESCULENTUM; TETRANYCHIDAE;

EID: 84870613786     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1208756109     Document Type: Article

References (35)

1. Navas-Castillo J, Fiallo-Olivé E, Sánchez-Campos S (2011) Emerging virus diseases transmitted by whiteflies. Annu Rev Phytopathol 49:219-248.
2. McCaskill D, Croteau R (1999) Strategies for bioengineering the development and metabolism of glandular tissues in plants. Nat Biotechnol 17(1):31-36. (Pubitemid 29037206)
3. Eigenbrode SD, Trumble JT, Millar JG, White KK (1994) Topical toxicity of tomato sesquiterpenes to the beet armyworm and the role of these compounds in resistance derived from an accession of Lycopersicon hirsutum f. typicum. J Agric Food Chem 42:807-810.
4. Frelichowski JE, Jr., Juvik JA (2001) Sesquiterpene carboxylic acids from a wild tomato species affect larval feeding behavior and survival of Helicoverpa zea and Spodoptera exigua (Lepidoptera: Noctuidae). J Econ Entomol 94(5):1249-1259.
5. Snyder JC, Guo Z, Thacker R, Goodman JP, Pyrek JST (1993) 2,3-Dihydrofarnesoic acid, a unique terpene from trichomes of Lycopersicon hirsutum repels spider mites. J Chem Ecol 19:2981-2997. (Pubitemid 2031946)
6. Sallaud C, et al. (2009) A novel pathway for sesquiterpene biosynthesis from Z,Z-farnesyl pyrophosphate in the wild tomato Solanum habrochaites. Plant Cell 21(1):301-317.
7. Gonzales-Vigil E, Hufnagel DE, Kim J, Last RL, Barry CS (2012) Evolution of TPS20-related terpene synthases influences chemical diversity in the glandular trichomes of the wild tomato relative Solanum habrochaites. Plant J 71(6):921-935.
8. Schilmiller AL, et al. (2009) Monoterpenes in the glandular trichomes of tomato are synthesized from a neryl diphosphate precursor rather than geranyl diphosphate. Proc Natl Acad Sci USA 106(26):10865-10870.
9. Koyama T (1999) Molecular analysis of prenyl chain elongating enzymes. Biosci Biotechnol Biochem 63(10):1671-1676.
10. Maluf WR, Campos GA, Cardoso MG (2001) Relationships between trichome types and spider mites (Tetranychus evansi) repellence in tomatoes with respect to foliar zingiberene content. Euphytica 121:73-80. (Pubitemid 33028077)
11. Freitas JA, Maluf WR, Graças-Cardoso M, Gomes LAA, Bearzotti E (2002) Inheritance of foliar zingiberene contents and their relationship to trichome densities and whitefly resistance in tomatoes. Euphytica 127:275-287. (Pubitemid 35211629)
12. Muigai SG, et al. (2002) Mechanisms of resistance in Lycopersicon germplasm to the whitefly Bemisia argentifolii. Phytoparasitica 30:347-360. (Pubitemid 35008325)
13. de Azevedo SM, et al. (2003) Zingiberene-mediated resistance to the South American tomato pinworm derived from Lycopersicon hirsutum var. hirsutum. Euphytica 134:347-351.
14. Zhang W, McAuslane HJ, Schuster DJ (2004) Repellency of ginger oil to Bemisia argentifolii (Homoptera: Aleyrodidae) on tomato. J Econ Entomol 97(4):1310-1318. (Pubitemid 39174988)
15. Bleeker PM, et al. (2011) Tomato-produced 7-epizingiberene and R-curcumene act as repellents to whiteflies. Phytochemistry 72(1):68-73.
16. Iijima Y, et al. (2004) The biochemical and molecular basis for the divergent patterns in the biosynthesis of terpenes and phenylpropenes in the peltate glands of three cultivars of basil. Plant Physiol 136(3):3724-3736.
17. Davidovich-Rikanati R, et al. (2008) Overexpression of the lemon basil α-zingiberene synthase gene increases both mono- and sesquiterpene contents in tomato fruit. Plant J 56(2):228-238.
18. Zhuang X, et al. (2012) Dynamic evolution of herbivore-induced sesquiterpene biosynthesis in sorghum and related grass crops. Plant J 69(1):70-80.
19. Chen F, Tholl D, Bohlmann J, Pichersky E (2011) The family of terpene synthases in plants: A mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J 66(1):212-229.
20. Falara V, et al. (2011) The tomato terpene synthase gene family. Plant Physiol 157(2):770-789.
21. Köllner TG, et al. (2008) A maize (E)-β-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20(2):482-494. (Pubitemid 352844026)
22. Greenhagen BT, O'Maille PE, Noel JP, Chappell J (2006) Identifying and manipulating structural determinates linking catalytic specificities in terpene synthases. Proc Natl Acad Sci USA 103(26):9826-9831. (Pubitemid 43993582)
23. Yu G, et al. (2010) Enzymatic functions of wild tomato methylketone synthases 1 and 2. Plant Physiol 154(1):67-77.
24. van Schie CC, Haring MA, Schuurink RC (2007) Tomato linalool synthase is induced in trichomes by jasmonic acid. Plant Mol Biol 64(3):251-263. (Pubitemid 46663193)
25. Quesada-Ocampo LM, Hausbeck MK (2010) Resistance in tomato and wild relatives to crown and root rot caused by Phytophthora capsici. Phytopathology 100(6):619-627.
26. Rodríguez-López MJ, et al. (2011) Whitefly resistance traits derived from the wild tomato Solanum pimpinellifolium affect the preference and feeding behavior of Bemisia tabaci and reduce the spread of Tomato yellow leaf curl virus. Phytopathology 101(10):1191-1201.
27. Martin DM, et al. (2010) Functional annotation, genome organization and phylogeny of the grapevine (Vitis vinifera) terpene synthase gene family based on genome assembly, FLcDNA cloning, and enzyme assays. BMC Plant Biol 10:226-248.
28. Wu S, et al. (2006) Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants. Nat Biotechnol 24(11):1441-1447. (Pubitemid 44722109)
29. Besser K, et al. (2009) Divergent regulation of terpenoid metabolism in the trichomes of wild and cultivated tomato species. Plant Physiol 149(1):499-514.
30. Rahimi FR, Carter CD (1993) Inheritance of zingiberene in Lycopersicon. Theor Appl Genet 87:593-597. (Pubitemid 2028932)
31. Rodríguez-López MJ, et al. (2012) Acylsucrose-producing tomato plants forces Bemisia tabaci to shift its preferred settling and feeding site. PLoS ONE 7(3):e33064.
32. Weinhold A, Baldwin IT (2011) Trichome-derived O-acyl sugars are a first meal for caterpillars that tags them for predation. Proc Natl Acad Sci USA 108(19):7855-7859.
33. Sarmento RA, et al. (2011) A herbivore that manipulates plant defence. Ecol Lett 14(3):229-236.
34. Luckwill LC (1943) The genus Lycopersicon: An historical, biological and taxonomic survey of the wild and cultivated tomatoes (Aberdeen Univ Press, Aberdeen, UK).
35. Kang J-H, et al. (2010) The tomato odorless-2 mutant is defective in trichome-based production of diverse specialized metabolites and broad-spectrum resistance to insect herbivores. Plant Physiol 154(1):262-272.