Herbivory in the Previous Generation Primes Plants for Enhanced Insect Resistance    

Abstract

Inducible defenses, which provide enhanced resistance after initial attack, are nearly universal in plants. This defense signaling cascade is mediated by the synthesis, movement, and perception of jasmonic acid and related plant metabolites. To characterize the long-term persistence of plant immunity, we challenged Arabidopsis (Arabidopsis thaliana) and tomato (Solanum lycopersicum) with caterpillar herbivory, application of methyl jasmonate, or mechanical damage during vegetative growth and assessed plant resistance in subsequent generations. Here, we show that induced resistance was associated with transgenerational priming of jasmonic acid-dependent defense responses in both species, caused caterpillars to grow up to 50% smaller than on control plants, and persisted for two generations in Arabidopsis. Arabidopsis mutants that are deficient in jasmonate perception (coronatine insensitive1) or in the biogenesis of small interfering RNA (dicer-like2 dicer-like3 dicer-like4 and nuclear RNA polymerase d2a nuclear RNA polymerase d2b) do not exhibit inherited resistance. The observation of inherited resistance in both the Brassicaceae and Solanaceae suggests that this trait may be more widely distributed in plants. Epigenetic resistance to herbivory thus represents a phenotypically plastic mechanism for enhanced defense across generations.

Next-Generation Systemic Acquired Resistance

“…Independently from our findings, two independent studies by Slaughter et al (2012) and Rasmann et al (2012) demonstrate similar transgenerational resistance phenomena in response to priming-inducing stimuli. Slaughter et al (2012) discovered that progeny of Arabidopsis that had been treated with b-aminobutyric acid or an avirulent isolate of PstDC3000 (PstavrRpt2) are primed for SA-dependent resistance against H. arabidopsidis and PstDC3000.…”

Epigenetic Variation, Inheritance, and Selection in Plant Populations

“…In several cases, plant responses to biotic stress, such as enhanced defense reactions to herbivore and plant pathogen attacks, persist in the next generation, indicating inherited resistance (Kathiria et al 2010;Luna et al 2012;Rasmann et al 2012;Slaughter et al 2012). The transmission of stress-induced stress tolerance to the progeny was impaired when the RdDM pathway was not functional (Boyko et al 2010;Rasmann et al 2012). The reported results suggest that the exposure of the mother plant to biotic and abiotic stresses has an influence on its progeny.…”

“…Furthermore, environmentally induced changes in DNA methylation patterns and gene expression are transmitted to unstressed offspring (Hauben et al 2009;Verhoeven et al 2010;Bilichak et al 2012). In several cases, plant responses to biotic stress, such as enhanced defense reactions to herbivore and plant pathogen attacks, persist in the next generation, indicating inherited resistance (Kathiria et al 2010;Luna et al 2012;Rasmann et al 2012;Slaughter et al 2012). The transmission of stress-induced stress tolerance to the progeny was impaired when the RdDM pathway was not functional (Boyko et al 2010;Rasmann et al 2012).…”

Mediation of seed provisioning in the transmission of environmental maternal effects in Maritime pine (Pinus pinaster Aiton)

“…Increasing evidence is accumulating that environmental maternal effects may be adaptive, enhancing the fitness of the offspring when established under environmental conditions that resemble the maternal environment (Galloway and Etterson, 2007;Herman and Sultan, 2011). This form of adaptive transgenerational plasticity has been reported in response to several biotic and abiotic environmental cues, including temperature (Yakovlev et al, 2010), drought (Herman et al, 2012), shade (Galloway and Etterson, 2007), nutrient availability (Kou et al, 2011), salinity (Boyko et al, 2010), herbivory (Rasmann et al, 2012) or viral infection (Kathiria et al, 2010). As a result of all these studies, environmental maternal effects are now recognized as a relevant source of phenotypic variation that may have an essential role in local adaptations (Herman and Sultan, 2011;Holeski et al, 2012).…”