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ARS Home » Southeast Area » Gainesville, Florida » Center for Medical, Agricultural and Veterinary Entomology » Chemistry Research » Research » Publications at this Location » Publication #288353

Title: European corn borer (Ostrinia nubilalis) induced defenses in maize enhance susceptibility in maize

item Dafoe, Nicole
item Thomas, James
item Shirk, Paul
item Legaspi, Michelle
item Vaughan, Martha
item Huffaker, Alisa
item Teal, Peter
item Schmelz, Eric

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/1/2013
Publication Date: 9/11/2013
Citation: Dafoe, N.J., Thomas, J.D., Shirk, P.D., Legaspi, M.E., Vaughan, M.M., Huffaker, A., Teal, P.E., Schmelz, E.A. 2013. European corn borer (Ostrinia nubilalis) induced defenses in maize enhance susceptibility in maize. PLoS One. 8(9):1-18.

Interpretive Summary: In contrast to leaf feeding pests, stem boring larvae are hidden from sight resulting in significant and insidious crop damage. Prior to transgenic control measures, the European corn borer (Ostrinia nubilalis) was responsible for severe yearly losses in US maize production. While maize defense mechanisms that protect against borer damage have been examined, less is known about the physiological mechanisms that mediate plant susceptibility to attack. By examining the interactions of European corn borer larvae with maize stems, scientists at the Center for Medical, Agricultural and Veterinary Entomology in Gainesville, FL, have discovered that insect-induced plant responses are linked with increased susceptibility to larval attack. This relationship strongly contrasts the expectation of induced plant resistance. Improved larval growth on previously attacked stem tissues is attributable to greatly increased total protein levels and large scale metabolic changes despite increased levels of phytochemical defenses. Unlike other Lepidoptera pests examined, European corn borer larvae excrete high levels of the phytohormone indole-3-acetic acid (IAA) into the feeding tunnel through frass contact. While maize plants rapidly conjugate and remove exogenous IAA, stem tissue levels remain elevated during European corn borer attack. Consistent with a physiological role, single applications of stable IAA analogs were able trigger significant increases in stem protein levels. These results provide evidence that European corn borer larvae use IAA as an effector to promote plant susceptibility. An understanding of how European corn borer larvae produce IAA has significant potential to result in targeted strategies inhibiting this process and reducing the pests ability to negatively manipulate crops.

Technical Abstract: Herbivore-induced plant defenses have been widely described following attack on leaves; however, less attention has been paid to analogous local processes that occur in stems. Early studies of maize responses to stem boring by European corn borer (ECB, Ostrinia nubilalis) larvae revealed the presence of inducible acidic diterpenoid phytoalexins, termed kauralexins, and increases in the benzoxazinoid 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one-glucose (HDMBOA-glc) after 24 h of herbivory. Despite these rapidly activated defenses, larval growth was not altered in short-term feeding assays. Unexpectedly, in assays using stem tissue preconditioned by 48 h of herbivory, larval growth significantly improved. Correspondingly, measures of total soluble protein increased over 2.6-fold in 48 h ECB challenged tissue and were accompanied by elevated levels of sucrose and free linoleic acid. While microarray analyses revealed up-regulation of over 1100 transcripts, fewer individual protein increases were demonstrable using iTRAQ. Consistent with induced endoreduplication, both wounding and ECB stem attack resulted in significant expansion of the nucleus, nucleolus and levels of extractable DNA from challenged tissues. While some responses are triggered by wounding alone, biochemical changes occurring principally in response to ECB may be due to larval secreted effectors. Unlike other Lepidoptera examined, ECB excrete exceedingly high levels of indole-3-acetic acid (IAA) into the surrounding feeding tunnel through contamination with frass. Stem exposure to a metabolically stable auxin, such as 2,4-dichlorophenoxyacetic acid (2,4-D), promoted significant protein accumulation above wounding alone. We propose ECB-derived IAA as a candidate herbivore effector that promotes the increased nutritional content of maize stems.