Abstract
Folivory is the best studied plant-herbivore interaction, but it is unclear whether the signaling and resistance traits important for the defense of leaves are also important for other plant parts. Larvae of the tobacco stem weevil, Trichobaris mucorea, burrow into stems of Nicotiana attenuata and feed on the pith. Transgenic N. attenuata lines silenced in signaling and foliar defense traits were evaluated in a 2-year field study for resistance against attack by naturally occurring T. mucorea larva. Plants silenced in early jasmonic acid (JA) biosynthesis (antisense [as]-lipoxygenase3 [lox3]; inverted repeat [ir]-allene oxide cyclase), JA perception (as-coronatine insensitive1), proteinase inhibitors (ir-pi), and nicotine (ir-putrescine methyl-transferase) direct defenses and lignin (ir-cad) biosynthesis were infested more frequently than wild-type plants. Plants unable to emit C(6) aldehydes (as-hpl) had lower infestation rates, while plants silenced in late steps in JA biosynthesis (ir-acyl-coenzyme A oxidase, ir-opr) and silenced in diterpene glycoside production (ir-geranylgeranyl pyrophosphate synthase) did not differ from wild type. Pith choice assays revealed that ir-putrescine methyl-transferase, ir-coronatine insensitive1, and ir-lox3 pith, which all had diminished nicotine levels, were preferred by larvae compared to wild-type pith. The lack of preference for ir-lox2 and ir-cad piths, suggest that oviposition attraction and vascular defense, rather than pith palatability accounts for the higher attack rates observed for these plants. We conclude that traits that influence a plant's apparency, stem hardness, and pith direct defenses all contribute to resistance against this herbivore whose attack can be devastating to N. attenuata's fitness.
Highlights
Folivory is the best studied plant-herbivore interaction, but it is unclear whether the signaling and resistance traits important for the defense of leaves are important for other plant parts
The life cycles of most organisms are constrained by the seasonality of resources and the timing of N. attenuata’s initiation of stem growth and flowering represents a strong phenological constraint for the tobacco stem weevil
Since T. mucorea larvae do not survive very long when removed from stems, it is very unlikely that they can move from one plant to another
Summary
Folivory is the best studied plant-herbivore interaction, but it is unclear whether the signaling and resistance traits important for the defense of leaves are important for other plant parts. Weevils are classified in the superfamily, Curculionoidea, which contains about 62,000 species and approximately 6,000 described genera (Thompson, 1992; Kuschel, 1995), and as such, they represent one of the most specious groups of herbivorous beetles with the broadest geographical range They occur in the humid tropics, subaquatic, desert, tundra, and other environments at most latitudes and altitudes with all vegetation types (Arnett et al, 2002). Stem tissues, which are thought to be nutritionally deficient as a result of their high cellulose and lignin contents, may be low in defenses (Zangerl and Bazzaz, 1992) but this does not take into account the large negative fitness effects commonly associated with the attack of stems and other structural parts of a plant (Strong et al, 1984; Karban and Baldwin, 1997). Other studies have found stemassociated terpenoids to function as feeding deterrents or repellants (Nordlander, 1990; Lindgren et al, 1996) or toxins (Cook and Hain, 1988; Raffa and Smalley, 1995; Werner, 1995) to bark beetles and pine weevils
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