Herbivorous caterpillars can utilize three mechanisms to alter green leaf volatile emission

Authors: JONES, ANNE - Pennsylvania State University; SEIDL-ADAMS, IRMGARD - Pennsylvania State University; ENGELBERTH, JURGEN - University Of Texas At San Antonio; Hunter, Charles; Alborn, Hans; TUMLINSON, JAMES - Pennsylvania State University

Submitted to: Environmental Entomology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/11/2018
Publication Date: 4/11/2019
Citation: Jones, A.C., Seidl-Adams, I., Engelberth, J., Hunter III, C.T., Alborn, H.T., Tumlinson, J.H. 2019. Herbivorous caterpillars can utilize three mechanisms to alter green leaf volatile emission. Environmental Entomology. 48(2):419–425. https://doi.org/10.1093/ee/nvy191.
DOI: https://doi.org/10.1093/ee/nvy191

Interpretive Summary: This work provides new information regarding an important plant-insect interaction where caterpillar regurgitant (spit) is capable of repressing the production of an important class of volatile (odors) defense compound call green leaf volatiles (GLVs). Normally when a plant is wounded, as occurs during herbivory, the plant emits GLVs and other volatile signals that induce defense priming (readying of chemical defense pathways of the plant for future attacks) and potentially attract wasp species that prey on caterpillars. ARS scientist from the Chemistry Research Unit in collaboration with Penn State University researchers who led the study characterized the capacity of regurgitant from five different caterpillar species to decrease GLV emission from corn leaf tissue, and showed that four of the five effectively suppress GLVs. The characterization of heat stability and precise origin of the suppressing activity showed three distinct GLV modifying or suppressing effectors, one in caterpillar gut contents and two in salivary glands. The widespread occurrence of GLV-suppression and the finding that multiple independent pathways target GLV emission indicates the importance of these insect strategies to bypass plant defense pathways. These findings provide important new information on GLV suppression by insects and may help researchers breed or engineer plants with the ability to circumvent the strategy, thus improving their ability to withstand insect attack.

Technical Abstract: While green plants emit green leaf volatiles (GLVs) as a general damage response when wounded, oral secretions from certain caterpillars, when applied to wounded leaves, significantly decrease these GLV emissions. We examined 5 different caterpillar species representing 3 different families for their capacity to decrease GLV emissions from Zea mays leaf tissue. We also investigated where in the alimentary tract of the various caterpillars the modifying effectors occurred. In Spodoptera exigua, S. frugiperda, Trichoplusia ni, and Manduca sexta, we found three distinct GLV modifying or suppressing effectors: a heat-stable effector in the gut, a heat-labile effector in salivary gland homogenate and an isomerase in the salivary gland homogenate, that catalyzes the conversion of (Z)-3-hexenal to (E)-2-hexenal – previously described in M. sexta. The exception to our findings was Malacosoma americanum oral secretions, which did not possess any detectible effectors modifying GLV emission in Z. mays leaf tissue. The wide-spread and multiple strategies employed by caterpillars to suppress GLV emission indicate the importance of the process and suggest a possibly detrimental role of GLVs to caterpillar fitness in plant-caterpillar interactions.