Herbivore-induced ethylene burst reduces fitness costs of jasmonate- and oral secretion-induced defenses in Nicotiana attenuata

Abstract

Specialist herbivores are known to alter their host's wound-induced responses but the beneficiaries of these alterations are unknown. Nicotiana attenuata plants release a burst of ethylene specifically in response to feeding by Manduca sexta larvae, which is known to suppress wound- and methyl jasmonate (MeJA)-inducible nicotine accumulation. The ethylene burst may be a mechanism by which M. sexta larvae feed "stealthily" on their host plants or, alternatively, it may allow the plant to optimize its defense response against this specialist herbivore by reducing costs of induction. We examined the impact of the ethylene burst on defense-related fitness costs that are readily observed when plants are treated with MeJA and grown in competition with untreated plants. We elicited nicotine induction (with MeJA), the ethylene burst (with the ethylene releasing compound, ethephon) and inhibited the plant's ability to perceive ethylene (with applications of an antagonist of ethylene receptors, 1-methylcyclopropene, 1-MCP). By simultaneously applying MeJA and ethephon we mimicked the plant's hormonal response to larval attack. We hypothesized that if the ethylene burst benefited the plant, the fitness costs of MeJA induction should be reduced by ethephon and restored if the plants were additionally treated with 1-MCP. In a second experiment, we applied larval oral secretion (OS) to elicit endogenous hormone production and predicted that the 1-MCP treatment should reduce the fitness of OS-treated plants. Our measures of plant fitness, namely the rate of stalk elongation and lifetime capsule production, supported these predictions. We conclude that the ethylene burst elicited by this specialist herbivore can reduce MeJA-induced fitness costs and increase the competitive strength of OS-treated plants. Suppressed nicotine production is likely to contribute to, but is not sufficient to explain, the observed fitness outcomes. The intensity of intra-specific competition and herbivore attack will likely determine the adaptive value of the M. sexta-elicited ethylene response.

Consistency of Nicotiana attenuata's Herbivore- and Jasmonate-Induced Transcriptional Responses in the Allotetraploid Species Nicotiana quadrivalvis and Nicotiana clevelandii

“…This observation is consistent with a more general response to stress in which the remobilization of limiting resources can minimize the fitness consequences of losing tissues to herbivores, or activate metabolically demanding defense responses in all three species (Karban and Baldwin, 1997;Voelckel et al, 2001;Heil and Baldwin, 2002;Strauss et al, 2002;Zangerl et al, 2002;Hui et al, 2003;Zavala et al, 2004).…”

“…PIs act as direct defenses, slowing the growth of the larvae and keeping them at a size which is vulnerable to generalist predators, while VOCs, as an indirect defense, attract generalist predators to the feeding larvae (Pohnert et al, 1999;Baldwin, 2001, 2002;Glawe et al, 2003). In addition, a large-scale transcriptional reorganization (Schittko et al, 2000Hermsmeier et al, 2001;Voelckel et al, 2001;Halitschke et al, 2003;Hui et al, 2003;Voelckel and Baldwin, 2003) accompanies the up-regulation of direct and indirect defenses elicited by M. sexta attack. The available evidence suggests that many of the responses are adaptive, increasing the fitness of plants attacked by M. sexta larvae.…”

The HERBIVORE ELICITOR-REGULATED1 Gene Enhances Abscisic Acid Levels and Defenses against Herbivores in Nicotiana attenuata Plants

“…SA, ethylene, brassinosteroids, and their signaling pathways have already been shown to act both synergistically and antagonistically with JA during herbivore attack in N. attenuata (Voelckel et al, 2001;Rayapuram and Baldwin, 2007;Onkokesung et al, 2010;Yang et al, 2011); a similar level of complex interactions has been shown for ethylene with all other known phytohormones (Chang et al, 2013). The multifaceted role of ABA also suggests that it may fine-tune biotic stress responses (Ton et al, 2009;Atkinson and Urwin, 2012).…”

“…Most of these interactions are modulated by insect-derived FACs (Voelckel et al, 2001;Rayapuram and Baldwin, 2007;von Dahl et al, 2007;Onkokesung et al, 2010;Gilardoni et al, 2011;Yang et al, 2011;Heinrich et al, 2013). Therefore, phytohormone cross talk and FACs have important roles in the organization and execution of optimal defense responses in natural ecosystems in this plant.…”

A Comparison of Two Nicotiana attenuata Accessions Reveals Large Differences in Signaling Induced by Oral Secretions of the Specialist Herbivore Manduca sexta

“…Nicotine is a potent chemical defense that has a strong negative effect on M. sexta and on many other herbivores and has been previously shown to be a critical component of JA-mediated direct defense in AZ as well as in UT (Steppuhn et al, 2004). Nicotine biosynthesis is both up-regulated by JA and down-regulated by OS-induced ET (Baldwin, 1998;Voelckel et al, 2001;von Dahl et al, 2007). Thus, higher nicotine levels in AZ could indicate that decreased negative regulation by ET plays a greater role than decreased positive regulation by JA in nicotine accumulation after herbivory.…”