Submitted to: Journal of Chemical Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/24/2004
Publication Date: 3/20/2005
Citation: Huang, J., Schmelz, E.A., Alborn, H., Engelberth, J., and Tumlinson, J.H. 2005. Phytohormones mediate volatile emissions during the interaction of compatible and incompatible pathogens: The role of ethylene in Pseudomonas syringae infected tobacco. Journal of Chemical Ecology. 31(3):439-459. Interpretive Summary: Plants often respond to pathogen attack by rapidly inducing biochemical changes that reduce further growth of the offending microbes. One commonly occurring plant response is increased emission of low molecular weight terpenoid volatiles. Clearly, plant hormones regulate insect-induced plant volatile emission yet how plants regulate volatile emission during bacterial pathogen attack has remained uncertain. Scientists at the Center for Medical, Agricultural and Veterinary Entomology in Gainesville, FL, have discovered that during the interaction of multiple pathogens on the same plant, the plant hormone ethylene can greatly influence the amount and ratios of plant volatiles released during infection. Surprisingly, key plant defense related hormones, such as jasmonic acid, were not clearly implicated in the pathogen induced volatile emission. By examining both virulent and avirulent bacteria, the results indicated that virulent bacteria can suppress a plants volatile response by causing a large burst in ethylene production. These experiments provide important insight on how virulent bacteria may suppress plant defense responses aiding in their attack and colonization.
Technical Abstract: Interactions between the phytohormones ethylene, salicylic acid (SA), and jasmonic acid (JA) are thought to regulate the specificity of induced plant defenses against microbial pathogens and herbivores. However, the nature of these interactions leading to induced plant volatile emission during pathogen infection is unclear. We previously demonstrated that a complex volatile blend including (E)-'-ocimene, methyl salicylate (MeSA), and numerous sesquiterpenes was released by tobacco plants, Nicotiana tabacum K326, infected with an avirulent/incompatible strain of Pseudomonas syringae pv. tomato (Pst DC3000). In contrast, a volatile blend, mainly consisting of MeSA and two unidentified sesquiterpenes, was released by plants infected with P. syringae pv. tabaci (Pstb) in a virulent/compatible interaction. In this study, we examined the interaction of multiple pathogen stresses, phytohormone signaling, and induced volatile emissions in tobacco. Combined pathogen infection involved the inoculation of one leaf with Pst DC 3000 and on a second leaf, from the same plant, Pstb inoculation. Combined infection significantly reduced emission of ocimene and MeSA compared to plants infected with Pst DC3000 alone, but with no significant changes in total sesquiterpene emissions. In the compatible interaction, Pstb elicited a large ethylene burst with a peak emission occurring 3 days after inoculation. In contrast, the incompatible interaction involving Pst DC3000 displayed no such ethylene induction. Pstb-induced ethylene production was not significantly altered by Pst DC3000 in the combined infection. We postulated that Pstb-induced ethylene production may play an important regulatory role in altering the typical volatile emission in tobacco in response to Pst DC3000 infection. To clarify the role of ethylene, we dynamically applied ethylene to the headspace of tobacco plants following infection with Pst DC3000. Consistent with Pstb-induced ethylene, exogenous ethylene significantly reduced both ocimene and MeSA emissions, and selectively altered the ratios and amounts of induced sesquiterpenes emissions. Our findings strongly suggest that ethylene can regulate the magnitude and blend of induced volatile emissions during pathogen infection.