Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea

Abstract

Plants respond to herbivore attack by rapidly inducing defenses that are mainly regulated by jasmonic acid (JA). Due to the systemic nature of induced defenses, attack by root herbivores can also result in a shoot response and vice versa, causing interactions between above- and belowground herbivores. However, little is known about the molecular mechanisms underlying these interactions. We investigated whether plants respond differently when roots or shoots are induced. We mimicked herbivore attack by applying JA to the roots or shoots of Brassica oleracea and analyzed molecular and chemical responses in both organs. In shoots, an immediate and massive change in primary and secondary metabolism was observed. In roots, the JA-induced response was less extensive and qualitatively different from that in the shoots. Strikingly, in both roots and shoots we also observed differential responses in primary metabolism, development as well as defense specific traits depending on whether the JA induction had been below- or aboveground. We conclude that the JA response is not only tissue-specific but also dependent on the organ that was induced. Already very early in the JA signaling pathway the differential response was observed. This indicates that both organs have a different JA signaling cascade, and that the signal eliciting systemic responses contains information about the site of induction, thus providing plants with a mechanism to tailor their responses specifically to the organ that is damaged.

Mechanisms and ecological implications of plant‐mediated interactions between belowground and aboveground insect herbivores

“…show organ-specificity for both the induction and the response. Interestingly, this organspecificity was observed for different response levels, such as transcriptome profiles of defense-related genes, specific classes of GLS and VOCs, that were induced after JA application or insect herbivory (van Dam et al 2004;Soler et al 2007;van Dam and Oomen 2008;Jansen et al 2009;van Dam et al 2010;Pierre et al 2011a;Tytgat et al 2013). Regarding GLS profiles, for example, BG JA application increased the expression of genes involved in the aliphatic GLS pathway and the levels of aliphatic GLS in B. oleracea shoots (van Dam et al 2004;van Dam and Oomen 2008;Tytgat et al 2013).…”

“…Interestingly, this organspecificity was observed for different response levels, such as transcriptome profiles of defense-related genes, specific classes of GLS and VOCs, that were induced after JA application or insect herbivory (van Dam et al 2004;Soler et al 2007;van Dam and Oomen 2008;Jansen et al 2009;van Dam et al 2010;Pierre et al 2011a;Tytgat et al 2013). Regarding GLS profiles, for example, BG JA application increased the expression of genes involved in the aliphatic GLS pathway and the levels of aliphatic GLS in B. oleracea shoots (van Dam et al 2004;van Dam and Oomen 2008;Tytgat et al 2013). In contrast, AG application increased mainly indole GLS levels and the expression of related genes in Table 1 Summary of a literature review on different inducible response levels (gene expression, phytohormones, glucosinolates (GLS), metabolome, volatile organic compounds (VOCs) and other) studied in belowground (BG) and aboveground (AG) tissues of different Brassica species after BG and/or AG treatments (insect herbivory or phytohormone application) and changes in the performance of AG herbivores Tytgat et al 2013).…”

“…is that BG insect herbivory or JA application increases total GLS levels in shoots (Griffiths et al 1994;van Dam et al 2004;Soler et al 2005;van Dam and Raaijmakers 2006;van Dam and Oomen 2008;Qiu et al 2009;Pierre et al 2012). In the few studies showing that BG induction results in a decrease or has a no effect (van Dam and Raaijmakers 2006;Pierre et al 2012;Tytgat et al 2013), GLS were either measured at earlier time points (less than 3 days) after BG induction or show a trend for an increase that is not statistically significant (yet). Thus, the observed differences may be mostly attributed to the timing of induction, at least for the different Brassica species that have been tested so far.…”

“…Regarding GLS profiles, for example, BG JA application increased the expression of genes involved in the aliphatic GLS pathway and the levels of aliphatic GLS in B. oleracea shoots (van Dam et al 2004;van Dam and Oomen 2008;Tytgat et al 2013). In contrast, AG application increased mainly indole GLS levels and the expression of related genes in Table 1 Summary of a literature review on different inducible response levels (gene expression, phytohormones, glucosinolates (GLS), metabolome, volatile organic compounds (VOCs) and other) studied in belowground (BG) and aboveground (AG) tissues of different Brassica species after BG and/or AG treatments (insect herbivory or phytohormone application) and changes in the performance of AG herbivores Tytgat et al 2013). This pattern was also observed in B. rapa plants, where only AG and not BG JA application increased indole GLS in shoots (Tytgat et al 2013).…”

“…In contrast, AG application increased mainly indole GLS levels and the expression of related genes in Table 1 Summary of a literature review on different inducible response levels (gene expression, phytohormones, glucosinolates (GLS), metabolome, volatile organic compounds (VOCs) and other) studied in belowground (BG) and aboveground (AG) tissues of different Brassica species after BG and/or AG treatments (insect herbivory or phytohormone application) and changes in the performance of AG herbivores Tytgat et al 2013). This pattern was also observed in B. rapa plants, where only AG and not BG JA application increased indole GLS in shoots (Tytgat et al 2013). Contrasting responses of aliphatic GLS (increase) and indole GLS (decrease) were also found in B. oleracea and B. napus leaves in response to BG herbivory by the turnip root fly Delia floralis (Birch et al 1992).…”