Introduction
Phenotypic plasticity allows organisms to modify their biochemical, physiological or morphological traits to survive in changing environments (Schlichting, 1986). (Lämke & Bäurle, 2017; Bošković & Rando, 2018). These epigenetic responses have the potential to provide adaptive benefits to progeny, thereby enhancing evolutionary fitness of the parents. When facing environmental changes, organisms can adopt various transgenerational strategies to optimise their fitness. When environments change frequently and are unpredictable, parents may adopt a bet-hedging strategy to increase the variability within their progeny (Crean & Marshall, 2009). By contrast, when environments undergo directional and stable changes, which present a more predictable cue about future environmental conditions, parents could enhance reproductive fitness by transmitting specific adaptive traits to their progeny (Marshall & Uller, 2007; Proulx & Teotonio, 2017).
Transgenerational responses to stress have been reported in both plants and animals; ranging from maladaptive pathological effects of environmental pollutants, to adaptive immunological traits that increase resistance against pests and diseases (Holeski et al., 2012; Luna et al., 2012; Rasmann et al., 2012; Perez & Lehner, 2019; Tetreau et al., 2019). In plants, transgenerational induced resistance to disease is often referred to as ‘transgenerational acquired resistance’ (TAR), which is typically based on a sensitisation, or ‘priming’, of the immune system, mediating a faster and/or stronger immune response (Wilkinson et al., 2019). We have previously demonstrated that bacterial speck disease, caused by the hemi-biotrophic pathogen Pseudomonas syringae pv. tomato (Pst), elicits TAR that can be maintained over two stress-free generations in the self-fertilising annual plant Arabidopsis (Arabidopsis thaliana) (Luna et al., 2012; Stassen et al., 2018). Although the exact epigenetic mechanisms underpinning TAR are still under investigation, the induction and/or transmission of the resistance requires DNA demethylation at transposable elements, and is associated with genome-wide changes in DNA methylation (Luna & Ton, 2012; Lopez Sanchez et al., 2016; Stassen et al., 2018; Furci et al., 2019). These results are supported by numerous other studies reporting transgenerational changes in DNA methylation in response to environmental stress (Lämke & Bäurle, 2017; Wilkinson et al., 2019).
Despite the fact that epigenetic modifications are attracting much attention as a mechanism for transgenerational phenotypic plasticity, there is still controversy over whether such responses are adaptive (Herman & Sultan, 2011; Uller et al., 2013; Burggren, 2015; Crisp et al., 2016). Transgenerational phenotypic plasticity to abiotic conditions, such as light and water availability, have been shown to provide improved fitness when the environments of parents and progeny are matched (Galloway & Etterson, 2007; Herman et al., 2012). However, when parent and progeny environments are mismatched, transgenerational effects can be maladaptive, which may explain why many epigenetic modifications are erased during sexual reproduction (Iwasaki & Paszkowski, 2014; Crisp et al., 2016; Gehring, 2019). For TAR to be genuinely adaptive, theory provides three key predictions. First, TAR should be elicited by specific stresses that the parents can recover from and that generate corresponding specific phenotypic changes in their progeny. Secondly, since TAR is an inducible response, there should be associated costs that may only become apparent in mismatched environments. Finally, parents should have the ability to distinguish strong, reliable cues with high predictive value about future environments. There is limited evidence to support some of these predictions. For instance, while progeny from P. syringae-infected Arabidopsis exhibit TAR against another biotrophic pathogen, Hyaloperonospora arabidopsidis (Hpa), this same progeny showed enhanced susceptibility to the necrotrophic fungus Alternaria brassicicola (Luna et al., 2012). Similarly, progeny from spider mite-infested Arabidopsis were primed for defence against both spider mites and aphids but suffered increased susceptibility to P. syringae (Singh et al., 2017). However, none of these studies employed reciprocal designs to systematically test predictions relating to specificity and costs within a single experimental framework. Moreover, it remains unknown whether plants can perceive stress intensity as an environmental proxy to estimate the likelihood that the same stress is still present in the progeny environment and adjust the strength and/or durability of TAR accordingly.
Here, we have addressed the above hypotheses by characterising TAR responses of Arabidopsis to different types and intensities of biotic and abiotic stress. Using a full factorial reciprocal experimental design, we have examined the specificity of TAR by quantifying the impacts of three parental stresses in both matched and mismatched progeny environments. We show that TAR elicited by biotrophic and necrotrophic pathogens is not associated with reductions in reproductive fitness and provides resistance benefits to progeny in matched environments. However, these specific TAR responses were associated with ecological costs that become apparent in mismatched environments from enhanced susceptibility to other stresses. By contrast, abiotic stress by soil salinity failed to elicit TAR against salt but elicited non-specific resistance in mismatched environments against biotrophic and necrotrophic pathogens, which was offset by major reproductive costs from dramatically reduced seed production and viability. Finally, we demonstrate that the transgenerational stability and costs of pathogen-elicited TAR are proportional to the disease intensity experienced by the parents and discuss these results in context of current evolutionary theory about transgenerational phenotypic plasticity.
Results
Dose-dependent effects of biotic and abiotic stresses on plant fitness parameters.
To test our central hypotheses, we produced populations of Arabidopsis progeny that in the parental generation had been exposed to three different stresses: the (hemi)biotrohic pathogen Pseudomonas syringae pv. tomato DC3000 (Pst), the necrotrophic pathogen Plectosphaerella cucumerina (Pc), and salt stress (Fig. 1). All parents came from a single common ancestor to minimise (epi)genetic variation. For each stress type, we applied four severity levels (mock plus three increasing levels of the stress) and estimated their effects on different fitness parameters (Fig. 2).