The role of abscisic acid and water stress in root herbivore‐induced leaf resistance

Abstract

Summary• Herbivore-induced systemic resistance occurs in many plants and is commonly assumed to be adaptive. The mechanisms triggered by leaf-herbivores that lead to systemic resistance are largely understood, but it remains unknown how and why root herbivory also increases resistance in leaves.• To resolve this, we investigated the mechanism by which the root herbivore Diabrotica virgifera induces resistance against lepidopteran herbivores in the leaves of Zea mays.• Diabrotica virgifera infested plants suffered less aboveground herbivory in the field and showed reduced growth of Spodoptera littoralis caterpillars in the laboratory. Root herbivory did not lead to a jasmonate-dependent response in the leaves, but specifically triggered water loss and abscisic acid (ABA) accumulation. The induction of ABA by itself was partly responsible for the induction of leaf defenses, but not for the resistance against S. littoralis. Root-herbivore induced hydraulic changes in the leaves, however, were crucial for the increase in insect resistance.• We conclude that the induced leaf resistance after root feeding is the result of hydraulic changes, which reduce the quality of the leaves for chewing herbivores. This finding calls into question whether root-herbivore induced leaf-resistance is an evolved response.

Influence of drought on plant performance through changes in belowground tritrophic interactions

“…In addition, to what extent the increased concentrations are the result of reduced root water contents is currently unclear. As BXDs have an important role in plant defense and protection against herbivores and pathogens (Ahmad et al., 2011; Glauser et al., 2011; Maag et al., 2016), the drought‐induced concentration increase may also alter plant interactions with other plant‐associated organisms (Erb et al., 2011; Robert et al., 2012). …”

“…The fact that WCR attack further accentuated the delay in silk emergence points to a further increase in drought stress in WCR‐attacked plants. Small maize seedlings were shown previously to suffer from increased leaf water loss upon combined drought and WCR attack (Erb et al., 2011). Potential interactive effects between water deficit and WCR attack have also been noted episodically in the field (Godfrey, Meinke, & Wright, 1993; Urías‐López, Meinke, Higley, & Haile, 2000).…”

“…Second, soil moisture can alter the performance of root herbivores and their natural enemies indirectly via changes in plant chemistry (Khan, Ulrichs, & Mewis, 2010; Vaughan, Block, Christensen, Allen, & Schmelz, 2017). Third, root herbivores can alter the impact of soil moisture on plant performance, for instance by accentuating the negative impact of drought via the removal of roots by root herbivores (Erb et al., 2011). …”

Oviposition by a moth suppresses constitutive and herbivore-induced plant volatiles in maize

“…As the production of many HIPVs, particularly terpenoids, depends on plant photosynthesis (Paré and Tumlinson 1997), it is possible that the observed phenomenon is not adaptive per se, but simply the result of a physiological constraint, as has been observed for other aspects of plant-insect interactions (Erb et al 2010). The fact that linalool was also suppressed during the night, however, suggests that the suppression also occurs independently of the plant's photosynthetic activity.…”

Facilitation and inhibition: changes in plant nitrogen and secondary metabolites mediate interactions between above-ground and below-ground herbivores

“…For example, tannins are considered especially important in defence against specialist insects as digestibility-reducing compounds [9,10]. Damage by above-ground and/or below-ground herbivores may affect the levels of primary and secondary metabolites in plants, and changes in these chemicals can mediate the interactions of above-ground and below-ground herbivores [11][12][13][14][15]. For instance, Kaplan et al [11] found in tobacco that root-feeding nematodes increased the performance of folivorous caterpillars by blocking synthesis of alkaloids that are transported to leaves, but caterpillars increased nematode performance by increasing nitrogen transport to roots.…”