Great granny still ruling from the grave: Phenotypical response of plant performance and seed functional traits to salt stress affects multiple generations of a halophyte

Environmental changes, for example, in rainfall and land use, lead to changes in the environment experienced by subsequent generations of plant species. Environmental conditions of maternal plants can influence the fitness and phenotypes of subsequent generations via non-genetic mechanisms: transgenerational plasticity (TGP). However, relevant empirical evidence remains scarce and ambiguous. What are the adaptive consequences of TGP for plants in the face of environmental change? For how many generations does the TGP effect remain? We tried to answer these questions by measuring life-history traits and reproductive characteristics of progeny plants of the diaspore-heteromorphic annual halophyte Atriplex centralasiatica in a 3-year TGP experiment covering F0, F1 and F2 and partly F3. Plants from diaspore types A (low dispersal and high germination ability) and C (high dispersal and low germination ability) were grown in favourable versus stressful salinities over three generations in a fully factorial design. Transgenerational plasticity of plants grown in favourable versus stressful salinities decreased from F2 → F1 → F0. Compared to the favourable condition, the stressful condition decreased the length of the vegetative period, increased the length of reproductive time, reproductive allocation and progeny diaspore size. Salinity tolerance and phenotypic plasticity were higher in plants from diaspore A than in those from diaspore C. In the stressful condition, plants produced less plant biomass, larger diaspores, a higher proportion of diaspore C, but lower proportion of diaspore A. Production of the proportion of diaspore C increased with increase in number of previous generations that experienced stress. The stress experience of the great-great grandmother (F0) continued into the lower A:C ratio of the F3 diaspores. Synthesis. Our findings provide evidence for the ‘escape strategy’ of A. centralasiatica: TGP could spread the risk of environmental adversity by delaying seed germination temporally and broadening seed dispersal spatially, thus allowing plants to cope with environmental heterogeneity. Specifically, the trade-off in reproductive allocation between diaspores A and C enables plants to develop divergent strategies. New research should reveal the extent to which wide-ranging taxa can benefit from TGP and whether even (great)-great grandmother might be the starting point of TGP.