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Abstract

Fitness benefits of trypsin proteinase inhibitor expression in AbstractBackground: The commonly invoked cost-benefit paradigm, central to most of functional biology, explains why one phenotype cannot be optimally fit in all environments; yet it is rarely tested. Trypsin proteinase inhibitors (TPIs) expression in Nicotiana attenuata is known to decrease plant fitness when plants compete with unattacked conspecifics that do not produce TPIs and also to decrease the performance of attacking herbivores. Results:In order to determine whether the putative benefits of TPI production outweigh its cost, we transformed N. attenuata to silence endogenous TPI production or restore it in a natural mutant that was unable to produce TPIs. We compared the lifetime seed production of N. attenuata genotypes of the same genetic background with low or no TPI to that of genotypes with high TPI levels on which M. sexta larvae were allowed to feed freely. Unattacked low TPI-producing genotypes produced more seed capsules than did plants with high TPI levels. Caterpillar attack reduced seed capsule production in all genotypes and reversed the pattern of seed capsule production among genotypes. M. sexta larvae attacking genotypes with high TPI activity consumed more TPI, less protein, and move later to the young leaves. Larval masses were negatively correlated (R 2 = 0.56) with seed capsule production per plant.Conclusions: Our results demonstrate that the fitness benefits of TPI production outweigh their costs in greenhouse conditions, when plants are attacked and that despite the ongoing evolutionary interactions between plant and herbivore, TPI-mediated decreases in M. sexta performance translates into a fitness benefit for the plant.

Piriformospora indica and Sebacina vermifera increase growth performance at the expense of herbivore resistance in Nicotiana attenuata

“…Zavala and Baldwin (2004) studied the costs and benefits of TPI production in two ecotypes of N. attenuata, both of which were transformed to silence or enhance TPI production (Zavala et al 2004b). They showed that plants with low TPI production had a higher fitness than TPIexpressing genotypes when plants were not attacked, but when attacked, plants with high TPI production had an advantage over TPI-silenced plants (Zavala and Baldwin 2004).…”

“…This species and its specialist herbivore Manduca sexta (Sphingidae) have been developed as a model system for the study of plant-herbivore interactions (Baldwin and Preston 1999;Kessler and Baldwin 2002). In response to attack from M. sexta larvae, which is recognized when larval oral secretions (OS) are introduced into wounds during feeding (McCloud and Baldwin 1997;Halitschke et al 2001;Schittko et al 2001;Roda et al 2004), the plant dramatically increases the accumulation of trypsin proteinase inhibitors (TPI) which slow the growth of larvae (Zavala et al 2004a;Zavala and Baldwin 2004), presumably by inhibiting the function of larval digestive proteases. TPI production, however, comes at a significant fitness cost for the plant as TPI-producing genotypes are out-competed and produce less seed than genotypes in which TPI production has been genetically silenced (Glawe et al 2003;Zavala et al 2004b).…”

Herbivore induction of jasmonic acid and chemical defences reduce photosynthesis in Nicotiana attenuata

“…Suppression of trypsin protease inhibitors (TPIs) in Nicotiana attenuata Torr. ex Watson increases growth and fitness (Zavala et al ., 2004), but plants silenced in nicotine production function similarly to wild-type plants (Steppuhn et al ., 2004). As such, TPIs may incur greater resource costs than nicotine.…”

Evolutionary community ecology of plant‐associated arthropods in terrestrial ecosystems

“…Thus, these findings suggest that plants have a potential for continued evolution of induced response. Furthermore, several studies have shown the fitness costs of maintaining inducibility in the absence of herbivores and the benefits of induction in the presence of herbivores (Baldwin 1998;Agrawal et al 2002;Tian et al 2003;Zavala and Baldwin 2004;Go´mez et al 2007; but see Karban 1993). These results suggest that herbivore-induced plant responses are likely to be adaptive under the environment with herbivores.…”