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Background Plants are able to optimize defense responses induced by various herbivores, which have different feeding strategies. Local and systemic responses within a plant after herbivory are essential to modulate herbivore-specific plant responses. For instance, leaf-chewing herbivores elicit jasmonic acid signaling, which result in the inductions of toxic chemicals in the attacked leaf (tissue-specific responses) and also in the other unattacked parts of the plant (systemic responses). Root herbivory induces toxic metabolites in the attacked root and alters the levels of transcripts and metabolites in the unattacked shoot. However, we have little knowledge of the local and systemic responses against stem-boring herbivores. In this study, we examined the systemic changes in metabolites in the wild tobacco  Nicotiana attenuata , when the stem-boring herbivore  Trichobaris mucorea  attacks. Results To investigate the systemic responses of  T. mucorea  attacks, we measured the levels of jasmonic acid (JA), JA-dependent secondary metabolites, soluble sugars, and free amino acids in 7 distinct tissues of  N. attenuata : leaf lamina with epidermis (LLE), leaf midrib (LM), stem epidermis (SE), stem pith (SP), stem vascular bundle (SV), root cortex with epidermis (RCE), and root vascular bundle (RV). The levels of JA were increased in all root tissues and in LM by  T. mucorea  attacks. The levels of chlorogenic acids (CGAs) and nicotine were increased in all stem tissues by  T. mucorea . However, CGA was systematically induced in LM, and nicotine was systematically induced in LM and RCE. We further tested the resource allocation by measuring soluble sugars and free amino acids in plant tissues.  T. mucorea  attacks increased the level of free amino acids in all tissues except in LLE. The levels of soluble sugars were significantly decreased in SE and SP, but increased in RV. Conclusions The results reveal that plants have local- and systemic-specific responses in response to attack from a stem-boring herbivore. Interestingly, the level of induced secondary metabolites was not consistent with the systemic inductions of JA. Spatiotemporal resolution of plant defense responses against stem herbivory will be required to understand how a plant copes with attack from herbivores from different feeding guilds.

Tissue-specific systemic responses of the wild tobacco Nicotiana attenuata against stem-boring herbivore attack