Costs and Benefits of Transgenerational Induced Resistance in Arabidopsis.

Recent evidence suggests that stressed plants employ epigenetic mechanisms to transmit acquired resistance traits to their progeny. However, the evolutionary and ecological significance of transgenerational induced resistance (t-IR) is poorly understood because a clear understanding of how parents interpret environmental cues in relation to the effectiveness, stability, and anticipated ecological costs of t-IR is lacking. Here, we have used a full factorial design to study the specificity, costs, and transgenerational stability of t-IR following exposure of Arabidopsis thaliana to increasing stress intensities by a biotrophic pathogen, a necrotrophic pathogen, and salinity. We show that t-IR in response to infection by biotrophic or necrotrophic pathogens is effective against pathogens of the same lifestyle. This pathogen-mediated t-IR is associated with ecological costs, since progeny from biotroph-infected parents were more susceptible to both necrotrophic pathogens and salt stress, whereas progeny from necrotroph-infected parents were more susceptible to biotrophic pathogens. Hence, pathogen-mediated t-IR provides benefits when parents and progeny are in matched environments but is associated with costs that become apparent in mismatched environments. By contrast, soil salinity failed to mediate t-IR against salt stress in matched environments but caused non-specific t-IR against both biotrophic and necrotrophic pathogens in mismatched environments. However, the ecological relevance of this non-specific t-IR response remains questionable as its induction was offset by major reproductive costs arising from dramatically reduced seed production and viability. Finally, we show that the costs and transgenerational stability of pathogen-mediated t-IR are proportional to disease pressure experienced by the parents, suggesting that plants use disease severity as an environmental proxy to adjust investment in t-IR.

Chemical priming of immunity without costs to plant growth.

ß-Aminobutyric acid (BABA) induces broad-spectrum disease resistance, but also represses plant growth, which has limited its exploitation in crop protection. BABA perception relies on binding to the aspartyl-tRNA synthetase (AspRS) IBI1, which primes the enzyme for secondary defense activity. This study aimed to identify structural BABA analogues that induce resistance without stunting plant growth. Using site-directed mutagenesis, we demonstrate that the (l)-aspartic acid-binding domain of IBI1 is critical for BABA perception. Based on interaction models of this domain, we screened a small library of structural BABA analogues for growth repression and induced resistance against biotrophic Hyaloperonospora arabidopsidis (Hpa). A range of resistance-inducing compounds were identified, of which (R)-ß-homoserine (RBH) was the most effective. Surprisingly, RBH acted through different pathways than BABA. RBH-induced resistance (RBH-IR) against Hpa functioned independently of salicylic acid, partially relied on camalexin, and was associated with augmented cell wall defense. RBH-IR against necrotrophic Plectosphaerella cucumerina acted via priming of ethylene and jasmonic acid defenses. RBH-IR was also effective in tomato against Botrytis cinerea. Metabolic profiling revealed that RBH, unlike BABA, does not majorly affect plant metabolism. RBH primes distinct defense pathways against biotrophic and necrotrophic pathogens without stunting plant growth, signifying strong potential for exploitation in crop protection.

Costs and benefits of priming for defense in Arabidopsis.

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 beta-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 beta-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.