Abstract
Alteration and induction of plant secondary metabolites after herbivore attack have been shown in almost all the studied plant species. Induction can be at the local site of damage, or systemic, such as from roots to shoots. In addition to immediate induction, previous herbivore bouts have been shown to “prime” the plants for a stronger and faster response only after a subsequent attack happens. Whereas several studies revealed a link between root herbivory and increased resistance against aboveground (AG) herbivory, the evidence of root defense priming against subsequent AG herbivory is currently lacking. To address this gap, we induced Cardamine hirsuta roots by applying jasmonic acid (JA), and, after a time lag, we subjected both control and JA-treated plants to AG herbivory by the generalist herbivore Spodoptera littoralis. We addressed the effect of root JA addition on AG herbivore resistance by measuring larval weight gain and tested the effect of root induction on abundance and composition of glucosinolates (GSLs) in shoots, prior, and after subsequent herbivory. We observed a strong positive effect of root induction on the resistance against AG herbivory. The overall abundance and identity of GSLs was globally affected by JA induction and by herbivore feeding, independently, and we found a significant correlation between larval growth and the shoot GSL profiles only after AG herbivory, 11 days after induction in roots. Contrary to expectations of priming, we observed that JA induction in roots altered the GSLs profile in the leaves that was maintained through time. This initial modification was sufficient to maintain a lower caterpillar weight gain, even 11 days post-root induction. Altogether, we show that prior root defense induction increases AG insect resistance by modifying and maintaining variation in GSL profiles during insect feeding.
Highlights
Resistance to herbivory in plants is mediated by pre-existing, or herbivore-inducible, physical and chemical barriers (Karban and Baldwin, 1997)
We found no effect of plant biomass on larval weight gain (F1,76 = 0.01, p = 0.93)
The PERMANOVA showed that the abundance and diversity of GSLs were globally affected by jasmonic acid (JA) treatment and by one week of continuous damage by AG herbivores (Figure 3A and Table 1), we found no interaction between time and JA induction (Figure 3A)
Summary
Resistance to herbivory in plants is mediated by pre-existing, or herbivore-inducible, physical and chemical barriers (Karban and Baldwin, 1997). Other studies demonstrated that BG induction resulted in a decrease (van Dam et al, 2005), or had no effect on secondary metabolites levels (van Dam and Raaijmakers, 2006; Pierre et al, 2012; Tytgat et al, 2013) This suggests that plant defense induction in the roots could reduce herbivore pressure AG by immediately increasing shoot defenses, (van Dam et al, 2001, van Dam et al, 2004), or by priming the plants for a subsequent stronger response induction only after the shoot herbivore is on the plant
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