European corn borer (Ostrinia nubilalis) induced responses enhance susceptibility in maize

PLoS One. 2013 Sep 2;8(9):e73394. doi: 10.1371/journal.pone.0073394. eCollection 2013.

Abstract

Herbivore-induced plant responses 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 (Zea mays) responses to stem boring by European corn borer (ECB, Ostrinianubilalis) 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, ECB growth significantly improved in assays using stem tissue preconditioned by 48 h of larval tunneling. Correspondingly, measures of total soluble protein increased over 2.6-fold in these challenged tissues 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. Consistent with induced endoreduplication, both wounding and ECB stem attack resulted in similar significant expansion of the nucleus, nucleolus and levels of extractable DNA from challenged tissues. While many of these responses are triggered by wounding alone, biochemical changes further enhanced in response to ECB may be due to larval secreted effectors. Unlike other Lepidoptera examined, ECB excrete exceedingly high levels of the auxin indole-3-acetic acid (IAA) in their frass which is likely to contact and contaminate the surrounding feeding tunnel. Stem exposure to a metabolically stable auxin, such as 2,4-dichlorophenoxyacetic acid (2,4-D), promoted significant protein accumulation above wounding alone. As a future testable hypothesis, we propose that ECB-associated IAA may function as a candidate herbivore effector promoting the increased nutritional content of maize stems.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 2,4-Dichlorophenoxyacetic Acid / pharmacology
  • Animals
  • Cell Nucleus / drug effects
  • Cell Nucleus / metabolism
  • Disease Susceptibility / metabolism*
  • Disease Susceptibility / pathology
  • Herbivory*
  • Indoleacetic Acids / metabolism
  • Larva / growth & development
  • Lepidoptera / growth & development
  • Lepidoptera / physiology*
  • Plant Diseases*
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Plant Stems / cytology
  • Plant Stems / drug effects
  • Plant Stems / genetics
  • Plant Stems / metabolism
  • Time Factors
  • Up-Regulation / drug effects
  • Zea mays / cytology
  • Zea mays / drug effects
  • Zea mays / genetics
  • Zea mays / metabolism*

Substances

  • Indoleacetic Acids
  • Plant Proteins
  • 2,4-Dichlorophenoxyacetic Acid
  • indoleacetic acid

Grants and funding

This work was supported by the United States Department of Agriculture, Agricultural Research Service base funds directed to CRIS project number 6615-22430-002-00D. The funders had no role in data collection and analysis, decision to publish, or preparation of the manuscript.