European Corn Borer (Ostrinia nubilalis) Induced Responses Enhance Susceptibility in Maize

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, 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, 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.

Impacts of insect oral secretions on defoliation-induced plant defense

“…For nutrient poor tissues, increased protein content, even if defense related, could facilitate growth of adapted insects. For example, stem herbivory in maize by the European corn borer (Ostrinia nubilalis) results in elicitation of defense responses, OSderived and frass-derived larval deposition of auxin (indole-3-acetic acid), doubling of protein levels and improved insect growth [32 ]. Thus a combination of wounding, HAMPs and candidate effectors could potentially be used by Lepidoptera larvae to promote plant susceptibility.…”

Auxin Is Rapidly Induced by Herbivore Attack and Regulates a Subset of Systemic, Jasmonate-Dependent Defenses

“…Several studies suggest that the auxin indole-3-acetic acid (IAA) also regulates gall formation, since some gall-forming herbivores contain high levels of IAA Davies, 2001a, 2001b;Tooker and de Moraes, 2011a;Straka et al, 2010;Dorchin et al, 2009;Yamaguchi et al, 2012;Tanaka et al, 2013), IAA pools and signaling are enhanced in parasitized plant tissue (Yamaguchi et al, 2012;Tooker and de Moraes, 2011b), and direct application of IAA can result in the formation of gallresembling structures (Hamner and Kraus, 1937;Guiscafrearrillaga, 1949;Schäller, 1968;Bartlett and Connor, 2014;Connor et al, 2012). In the context of chewing insects, however, our understanding is more limited (Dafoe et al, 2013). IAA levels seem to remain unaltered in goldenrod (Solidago altissima) and wheat (Triticum aestivum) attacked by Heliothis virescens caterpillars de Moraes, 2011a, 2011b) and to be reduced in Helicoverpa zea attacked maize (Zea mays; Schmelz et al, 2003) and Manduca sexta-challenged Nicotiana attenuata leaves (Onkokesung et al, 2010;Woldemariam et al, 2012).…”

Cytochrome P₄₅₀, CYP93A1, as defense marker in soybean

“…In maize stems, it was also observed that mechanical damage alone did not result in an increase of JA, but feeding by the Ostrinia nubilalis did (Dafoe et al 2011). This correlated with a higher expression of certain defense-related genes and higher content of defensive compounds in tissue damaged by the Ostrinia nubilalis (Dafoe et al 2011(Dafoe et al , 2013. This would be consistent with the notion that the stems may also receive mechanical damage from the wind and under such circumstances the plant would not want to waste too much energy on induction of defenses in the absence of an insect herbivore or pathogen infection (Howe and Jander 2008).…”