When environments mismatch - The limits of transgenerational climate memory in Scots pine

A long-term irrigation experiment in the dry Rhône Valley of Switzerland provides a unique opportunity to examine transgenerational environmental memory effects of persistent drought and irrigation in Scots pine (Pinus sylvestris). Previous work in this system showed that offspring from mother trees exposed to chronic drought (non-irrigated control) versus long-term irrigation differed markedly in growth and survival. Offspring from irrigated mothers grew faster under irrigated conditions but performed poorly under drought, whereas offspring from drought-exposed mothers showed higher growth and survival under drought conditions. While these responses suggested transgenerational environmental memory, the relative contributions of maternal provisioning versus epigenetic mechanisms could not be fully resolved. Notably, mother trees did not differ in genotype, and seed mass did not vary between treatments, indicating a limited role of maternal effects. Here, we tested whether transgenerational environmental memory effects persist after offspring were grown for three years under non-experimental conditions before being re-exposed to experimental hot-drought and irrigation treatments. In contrast to the earlier study, offspring from irrigated mothers did not show higher growth performance under irrigated conditions, indicating that irrigation-related memory weakened during the intervening non-treated phase. Conversely, seedlings originating from drought-exposed mothers consistently exhibited higher carbon assimilation and stem growth than those from irrigated mothers, irrespective of experimental treatment. Gene expression analyses showed differences in the number and identity of differentially expressed genes between offspring of drought- and irrigation-exposed mothers, although we lack data on DNA methylation, histone modifications, or small RNAs. Patterns in primary metabolites broadly mirrored the results of gene expression, with modest differences in osmoprotectants and stress-related compounds. Overall, our results indicate that transgenerational environmental memory effects in P. sylvestris can diminish over time and, depending on the parental and offspring environments, may even result in mismatch and maladjustments.