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

Abstract

Tomato breeding has been tremendously efficient in increasing fruit quality and quantity but did not focus on improving herbivore resistance. The biosynthetic pathway for the production of 7-epizingiberene in a wild tomato was introduced into a cultivated greenhouse variety with the aim to obtain herbivore resistance. 7-Epizingiberene is a specific sesquiterpene with toxic and repellent properties that is produced and stored in glandular trichomes. We identified 7-epizingiberene synthase (ShZIS) that belongs to a new class of sesquiterpene synthases, exclusively using Z-Z-farnesyl-diphosphate (zFPP) in plastids, probably arisen through neo-functionalization of a common ancestor. Expression of the ShZIS and zFPP synthases in the glandular trichomes of cultivated tomato resulted in the production of 7-epizingiberene. These tomatoes gained resistance to several herbivores that are pests of tomato. Hence, introduction of this sesquiterpene biosynthetic pathway into cultivated tomatoes resulted in improved herbivore resistance.metabolic engineering | terpenoid | white fly | spider mite | promoter H erbivorous insects pose serious problems in agricultural production areas. On commercial tomato, whiteflies, spider mites, and aphids are major pests, not only by the feeding damage they cause, but also because they transmit devastating viruses that can cause losses up to 100% (1). Production of tomato, a crop with considerable economic importance, reached 145,751,507 tons worldwide in 2010, representing a value of 53.3 billion dollars (www.fao.org). In general, wild tomatoes are far less attractive to pests than cultivated tomatoes due to an elevated or qualitatively different production of an array of defense compounds such as alkaloids, phenolic compounds, and terpenes.Toxic and repellent compounds are mostly produced in glandular trichomes, autonomous epidermal protrusions specialized in efficient production, storage, and release of defense compounds (2). These glands have long been regarded as economically important and challenging targets for bioengineering (2). Confining metabolic changes to trichomes ensures that the plant metabolism and crop yield remains unaffected.Terpenes constitute the largest and most diverse class of plantproduced secondary compounds that maintain a variety of biological functions and applications, including anticancer (taxol) and antimalarial (artemisin) drugs, in flavor and fragrance industry, and for crop improvement through enhanced pest resistance. Wild tomato sesquiterpenes and derivatives have been implicated in defense against herbivores (3-5). Sesquiterpenes are C 15 -terpenes predominantly derived from precursors of the cytosolic mevalonate pathway where the C 5 -isoprene units isopentenyl diphosphate (IPP) and dimethylallyl diphosphate (DMAPP) are assembled into C 15 E-E-farnesyl diphosphate (FPP) by FPP synthase (FPS) and converted by specific sesquiterpene synthases. However, it was recently shown that some wild tomato species contain a sesquiterpene pathway that is confined to ...

Virulence Factors of Geminivirus Interact with MYC2 to Subvert Plant Resistance and Promote Vector Performance

“…7-Epizingiberene synthase, a key enzyme in the biosynthesis of the sesquiterpene 7-epizingiberene in wild tomato, is a major factor in the resistance of wild tomatoes (Solanum habrochaites LA1777) to whiteflies (Bleeker et al, 2012). TPS-silenced Arabidopsis or tobacco plants were more susceptible to whiteflies ( Figure 2F; Luan et al, 2013).…”

“…Terpenoids confer effective resistance to whiteflies (Bleeker et al, 2009(Bleeker et al, , 2012Luan et al, 2013), and some terpene biosynthesis genes have been identified to be involved in this process. 7-Epizingiberene synthase, a key enzyme in the biosynthesis of the sesquiterpene 7-epizingiberene in wild tomato, is a major factor in the resistance of wild tomatoes (Solanum habrochaites LA1777) to whiteflies (Bleeker et al, 2012).…”

Recent progress in secondary metabolism of plant glandular trichomes

“…Bleeker et al introduced the biosynthesis pathway of 7-epizingiberene in the glandular trichomes of tomato cultivar 'Moneymaker' by coexpressing ShZIS (7-epizingiberene synthase) and zFPP synthase driven by trichome-specific promoters. The transgenic cultivated tomato re-gained resistance to several tomato pests without observed penalties in growth or development (Bleeker et al 2011;Bleeker et al 2012).…”

Characterization of Trichome-Expressed BAHD Acyltransferases in Petunia axillaris Reveals Distinct Acylsugar Assembly Mechanisms within the Solanaceae

“…Glandular trichomes are epidermal cell appendages present on the surface of many plant species that serve as the location for the synthesis, storage, and secretion of diverse classes of specialized metabolites, including phenylpropanoids, terpenoids, and acylsugars (Schilmiller et al, 2008;Tissier, 2012). These compounds act directly as toxins or repellants to deter herbivory or serve as signaling molecules in tritrophic interactions to attract predators and also have been coopted by humans for use as medicines, narcotics, aromatics, and flavorings (Schilmiller et al, 2008;Weinhold and Baldwin, 2011;Bleeker et al, 2012). The glandular trichomes of members of the Solanaceae family are structurally and chemically diverse and synthesize specialized metabolites that are often restricted to individual species or specific accessions (Luckwill, 1943;Shapiro et al, 1994;Fridman et al, 2005;Gonzales-Vigil et al, 2012;Kim et al, 2012Kim et al, , 2014a.…”