Experience and memory of environmental stimuli that indicate future stress can prepare (prime) organismic stress responses even in species lacking a nervous system. The process through which such organisms prepare their phenotype for an improved response to future stress has been termed ‘priming’. However, other terms are also used for this phenomenon, especially when considering priming in different types of organisms and when referring to different stressors. Here we propose a conceptual framework for priming of stress responses in bacteria, fungi and plants which allows comparison of priming with other terms, e.g. adaptation, acclimation, induction, acquired resistance and cross protection. We address spatial and temporal aspects of priming and highlight current knowledge about the mechanisms necessary for information storage which range from epigenetic marks to the accumulation of (dormant) signalling molecules. Furthermore, we outline possible patterns of primed stress responses. Finally, we link the ability of organisms to become primed for stress responses (their ‘primability’) with evolutionary ecology aspects and discuss which properties of an organism and its environment may favour the evolution of priming of stress responses.

Plants produce metabolites that directly decrease herbivore performance, and as a consequence, herbivores are selected for resistance to these metabolites. To determine whether these metabolites actually function as defenses requires measuring the performance of plants that are altered only in the production of a certain metabolite. To date, the defensive value of most plant resistance traits has not been demonstrated in nature. We transformed native tobacco(Nicotiana attenuata) with a consensus fragment of its two putrescine N-methyl transferase (pmt) genes in either antisense or inverted-repeat (IRpmt) orientations. Only the latter reduced (by greater than 95%) constitutive and inducible nicotine. With D₄-nicotinic acid (NA), we demonstrate that silencing pmt inhibits nicotine production, while the excess NA dimerizes to form anatabine. Larvae of the nicotine-adapted herbivore Manduca sexta (tobacco hornworm) grew faster and, like the beetle Diabrotica undecimpunctata, preferred IRpmt plants in choice tests. When planted in their native habitat, IRpmt plants were attacked more frequently and, compared to wild-type plants, lost 3-fold more leaf area from a variety of native herbivores, of which the beet armyworm, Spodoptera exigua, and Trimerotropis spp. grasshoppers caused the most damage. These results provide strong evidence that nicotine functions as an efficient defense in nature and highlights the value of transgenic techniques for ecological research.

Significance: When hornworm ( Manduca sexta ) larvae feed on Nicotiana attenuata plants in native habitats, more disappear at night when they feed on transgenic, nicotine-free N. attenuata plants because wolf spiders ( Camptocosa parallela ) selectively prey on nicotine-free larvae. When larvae consume nicotine-replete plants, their midgut-expressed cytochrome P450 6B46 ( CYP6B46 ) is upregulated. The larvae in which CYP6B46 is silenced by plant-mediated RNAi excrete more of their ingested nicotine. Silencing CYP6B46 impairs the mechanisms of passing ingested nicotine from the midgut to the hemolymph to be exhaled from the spiracles during spider attack. Spiders are deterred by this nicotine-rich halitosis. Thus, the CYP6B46 -silenced larvae exhale less nicotine and become ready spider prey, demonstrating that CYP6B46 functions to repurpose the normally excreted nicotine for defense.

Many predatory insects that prey on herbivores also feed on the plant, but it is unknown whether plants affect the performance of herbivores by responding to this phytophagy with defence induction. We investigate whether the prior presence of the omnivorous predator Macrolophus pygmaeus (Rambur) on tomato plants affects plant resistance against two different herbivore species. Besides plant-mediated effects of M. pygmaeus on herbivore performance, we examined whether a plant defence trait that is known to be inducible by herbivory, proteinase inhibitors (PI), may also be activated in response to the interactions of this predator with the tomato plant. We show that exposing tomato plants to the omnivorous predator M. pygmaeus reduced performance of a subsequently infesting herbivore, the two-spotted spider mite Tetranychus urticae Koch, but not of the greenhouse whitefly Trialeurodes vaporariorum (Westwood). The spider-mite infested tomato plants experience a lower herbivore load, i.e., number of eggs deposited and individuals present, when previously exposed to the zoophytophagous predator. This effect is not restricted to the exposed leaf and persists on exposed plants for at least two weeks after the removal of the predators. The decreased performance of spider mites as a result of prior exposure of the plant to M. pygmaeus is accompanied by a locally and systemically increased accumulation of transcripts and activity of proteinase inhibitors that are known to be involved in plant defence. Our results demonstrate that zoophytophagous predators can induce plant defence responses and reduce herbivore performance. Hence, the suppression of populations of certain herbivores via consumption may be strengthened by the induction of plant defences by zoophytophagous predators.