Phytohormone Mediation of Interactions Between Herbivores and Plant Pathogens

Abstract

Induced plant defenses against either pathogens or herbivore attackers are regulated by phytohormones. These phytohormones are increasingly recognized as important mediators of interactions between organisms associated with plants. In this review, we discuss the role of plant defense hormones in sequential tri-partite interactions among plants, pathogenic microbes, and herbivorous insects, based on the most recent literature. We discuss the importance of pathogen trophic strategy in the interaction with herbivores that exhibit different feeding modes. Plant resistance mechanisms also affect plant quality in future interactions with attackers. We discuss exemplary evidence for the hypotheses that (i) biotrophic pathogens can facilitate chewing herbivores, unless plants exhibit effector-triggered immunity, but (ii) facilitate or inhibit phloem feeders. (iii) Necrotrophic pathogens, on the other hand, can inhibit both phloem feeders and chewers. We also propose herbivore feeding mode as predictor of effects on pathogens of different trophic strategies, providing evidence for the hypotheses that (iv) phloem feeders inhibit pathogen attack by increasing SA induction, whereas (v) chewing herbivores tend not to affect necrotrophic pathogens, while they may either inhibit or facilitate biotrophic pathogens. Putting these hypotheses to the test will increase our understanding of phytohormonal regulation of plant defense to sequential attack by plant pathogens and insect herbivores. This will provide valuable insight into plant-mediated ecological interactions among members of the plant-associated community.

Ecophysiological aspects of the interaction between Cameraria ohridella and Guignardia aesculi on Aesculus hippocastanum

“…In turn, in control plants where both insect and leaf blotch disease were co-existing induced synthesis of secondary metabolites was observed. In concordance with the phytohormonal theory (Lazebnik et al, 2014) it may be the effect of different pathways of phytohormones, i.e. jasmonic acid and salicylic acid that are involved when both insect and pathogen are colonising the leaf tissue separately or simultaneously (Thaler et al, 2002).…”

“…The way plants recognise and respond depends on the type of consumer and their strategy for accessing their food (Kessler & Baldwin, 2002). Interaction between both the insect feeding mode (chewing/phloem feeding) and pathogen trophic strategy (bio-, necro-and hemibiotrophic) results in different mechanisms of plant defence (Lazebnik et al, 2014). Chemical defence in plants, constitutive as well as induced, can influence intruders directly (by lowering quality of sustenance) or indirectly (by attraction of other organisms that could protect the plant) and plenty of biochemical compounds were found to play this role (Mithöfer & Boland, 2012).…”

Trichoderma gamsii affected herbivore feeding behaviour on Arabidopsis thaliana by modifying the leaf metabolome and phytohormones

“…ABA is a major regulator of abiotic stress responses caused by drought, salt, cold and wounding (Christmann et al ., 2006; Raghavendra et al ., 2010), and also plays a prominent role in plant resistance to biotic stresses such as pathogen attack (Ton et al ., 2009; Denance et al ., 2013) and herbivorous insects (Bodenhausen and Reymond, 2007; Verhage et al ., 2011; Pineda et al ., 2012; Lazebnik et al ., 2014). In our study, ABA content was increased in the Arabidopsis leaves when it was inoculated with T. gamsii F18.…”

“…Phytohormones, including JA, ethylene (ET), salicylic acid(SA), abscisic acid (ABA), auxin, cytokinins (CK), brassinosteroids (BR) and gibberllins (GB), have been reported to play important roles in both plant‐insect and plant‐microbe interactions (Erb et al ., 2012; Lazebnik et al ., 2014). These phytohormones function as signal transducers in plant‐induced defence pathways.…”

Plants under dual attack : consequences for plant chemistry and parasitoid behavior

“…This research takes the field of multiple attack and tritrophic interactions into a relatively new and unexplored direction that would benefit from greater attention. Typically, the effects of pathogen challenge in relation to herbivory have been fairly well studied in the context of plant-mediated effects on herbivore or pathogen performance, or changes to the defense signaling pathways at the molecular level (Cui et al, 2002;De Vos et al, 2006;Stout et al, 2006;Lazebnik et al, 2014). In terms of research on pathogen-induced volatiles, some work has been done on the induction of pathogen-specific compounds, mostly in the context of early disease detection in crops or their inhibitory effects on future pathogen colonization, and even less has been done in terms of effects on tritrophic interactions (Cardoza et al, 2003b;Rostás et al, 2006).…”