Evolutionary trade-offs in plant immunity: prioritizing antiviral priming by herbivore-induced plant volatiles over defense against herbivores

Abstract

Plants respond to insect herbivory by producing and releasing distinctive blends of volatile compounds. These herbivore-induced plant volatiles (HIPVs) serve several roles, including direct defense through toxic or repellent effects on herbivores and indirect defense by attracting the herbivores’ natural enemies (Bleeker et al. 2009; Veyrat et al. 2016). HIPVs also act as warning signals, informing undamaged tissues within the same plant and nearby plants of a pending insect attack (Heil and Bueno 2007). HIPVs are mostly composed of terpenes, fatty acid-derived compounds, and shikimic acid pathway metabolites. In response to certain HIPVs, neighboring plants enter a primed state, preparing for a future attack. As a result, when these primed plants are later attacked by the same herbivore, they can mount a faster and stronger defense response (Arimura et al. 2009). However, many specialized herbivores and pathogens can overcome, and often manipulate, these defenses to thrive on their specific host plants. Some insect vectors have evolved mutualisms with their viruses, e.g., some begomoviruses suppress terpenoid emissions that negatively affect their whitefly vectors (Bleeker et al. 2009). HIPV emissions vulnerable to manipulation include the generalist whitefly Bemisia tabaci-induced volatile blend (composed of the monoterpenes β-myrcene and ρ-cymene, and the sesquiterpene β-caryophyllene). These whitefly-induced volatiles prime salicylic acid-dependent defenses against pathogens in tomato plants while suppressing jasmonic acid-dependent defenses against herbivores, thus rendering neighboring tomato plants more susceptible to whiteflies (Zhang et al. 2019). This appears to be paradoxical and warrants further investigation.