Costs and benefits of priming for defense in Arabidopsis

Abstract

Induced resistance protects plants against a wide spectrum of diseases; however, it can also entail costs due to the allocation of resources or toxicity of defensive products. The cellular defense responses involved in induced resistance are either activated directly or primed for augmented expression upon pathogen attack. Priming for defense may combine the advantages of enhanced disease protection and low costs. In this study, we have compared the costs and benefits of priming to those of induced direct defense in Arabidopsis. In the absence of pathogen infection, chemical priming by low doses of ␤-aminobutyric acid caused minor reductions in relative growth rate and had no effect on seed production, whereas induction of direct defense by high doses of ␤-aminobutyric acid or benzothiadiazole strongly affected both fitness parameters. These costs were defense-related, because the salicylic acid-insensitive defense mutant npr1-1 remained unaffected by these treatments. Furthermore, the constitutive priming mutant edr1-1 displayed only slightly lower levels of fitness than wild-type plants and performed considerably better than the constitutively activated defense mutant cpr1-1. Hence, priming involves less fitness costs than induced direct defense. Upon infection by Pseudomonas syringae or Hyaloperonospora parasitica, priming conferred levels of disease protection that almost equaled the protection in benzothiadiazole-treated wild-type plants and cpr1 plants. Under these conditions, primed plants displayed significantly higher levels of fitness than noninduced plants and plants expressing chemically or cpr1-induced direct defense. Collectively, our results indicate that the benefits of priming-mediated resistance outweigh the costs in environments in which disease occurs.induced resistance ͉ innate immunity ͉ plant defense

Plant immune responses triggered by beneficial microbes

“…This is not illogical, because activation of inducible defenses involves major costs that affect plant growth and reproduction [57], and this is inconsistent with the beneficial nature of these plant-microbe interactions. Through the study of the costs and benefits of priming in Arabidopsis, it was recently shown that the fitness costs of priming are lower than those of constitutively activated defenses, such as those expressed in the constitutive SAR-expressing mutant cpr1 [58 ]. Intriguingly, the fitness benefits of priming outweighed its costs under pathogen pressure, which suggests that priming functions as an ecological adaptation of the plant to respond faster to its hostile environment.…”

Systemic acquired resistance: the elusive signal(s)

“…A recent field study confirmed that SAR increases the fitness of plants exposed to pathogens, which translates into enhanced crop yield [52]. However, unlike the fitness cost of constitutive resistance that associated with inducible resistance generally appears to outweigh the cost of pathogen infection, although this might depend on additional environmental factors [53,54 ]. In the era of metabolomics, large-scale surveys might reveal additional candidate compounds involved in SAR induction (e.g.…”

Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests

“…Priming for defence against pathogens has been shown to involve considerably fewer costs than the induction of direct defence, and the benefits derived from this priming outweigh the costs under conditions of disease pressure [12]. The phenomenon of volatile-induced priming against insects also fits in this ecological context of costs and benefits.…”

“…In addition, we address the recent studies that point to a priming effect in plants that are exposed to certain HIPVs, conferring an enhanced defensive capacity against future insect attack [6 ,7-11]. We conclude, with some reservations, that there is not only reason for optimism that manipulation of HIPVs emissions can indeed lead to enhanced repulsion of pests and attraction of their natural enemies but, moreover, that enhanced volatile information transfer between plants might, if exploited appropriately, improve the efficiency of the plant's direct and indirect defence strategies through priming [4,12]. Figures 1 and 2 summarize the various interactions in which HIPVs are implicated as we have studied them for maize plants.…”

“…This so-called priming for defence has proven to be an important mechanism behind induced resistance against pathogens [28], and has now also been reported as a likely mechanism behind volatile-induced resistance [6 ,24 ]. Priming through volatiles might also be important in enhancing indirect defences [6 ,7,29].Priming for defence against pathogens has been shown to involve considerably fewer costs than the induction of direct defence, and the benefits derived from this priming outweigh the costs under conditions of disease pressure [12]. The phenomenon of volatile-induced priming against insects also fits in this ecological context of costs and benefits.…”