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.
Highlights
Induced defense responses often protect plants against insect herbivory, but in some cases insects modify these responses by manipulating the plant to produce more optimal feeding sites [1,2,3,4]
While HDMBOA-Glc was undetectable in control tissue, approximately 3.6 μg g-1 FW was present in larval conditioned tissues (LCT)
In leaves of young maize plants, the benzoxazinoid DIMBOA-Glc is closely associated with resistance to ECB herbivory while in mature stems, resistance appears to be associated with cell wall composition [35]
Summary
Induced defense responses often protect plants against insect herbivory, but in some cases insects modify these responses by manipulating the plant to produce more optimal feeding sites [1,2,3,4]. Within 24 h, maize stem feeding by the European corn borer (ECB, Ostrinia nubilalis) rapidly induces the local accumulation of defensive compounds such as benzoxazinoids and the kauralexin family of diterpenoid phytoalexins [5]. These defenses do not appear to affect the short-term growth of ECB, which are one of the most devastating pests of maize [5,6]. The long-term accumulation of inducible biochemical defenses has the potential to deter ECB feeding [8]. It is possible that ECB larvae possess mechanisms to overcome defense responses and flourish in nutrient poor tissue
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