Transgenerational imprint of subindividual variation: somatic epigenetic divergence within trees cascades into epigenetic and phenotypic pollen divergence

The evolutionary significance of somatic mosaicism created within plants by random epigenetic drift or localized responses to the environment will rest on its transgenerational implications. This paper tests whether the epigenetic mosaicism exhibited by individuals of a long-lived tree leaves some discernible "imprint" in the next gametophytic generation. Paired samples of leaves and pollen from five distinct branches within each of five wild-growing Pistacia terebinthus (Anacardiaceae) trees were characterized epigenetically using genome-wide DNA cytosine methylation level and multivariate epigenetic fingerprinting. Pollen grains were also characterized phenotypically by size and shape. Individual trees were somatically heterogeneous with regard to both cytosine methylation level and multilocus epigenetic fingerprints of leaf tissue, and within-tree variance in leaf epigenetic features exceeded among-tree variance. Phenotypic and epigenetic features of pollen differed significantly among branches of individual trees, and intraplant variation in phenotype and epigenetic fingerprints of pollen was predicted by intraplant variation in epigenetic features of leaves. Results provide evidence that intraindividual epigenetic heterogeneity arising in long-lived plants can leave its imprint into subsequent sporophyte generations via the production of epigenetically and phenotypically heterogeneous haploid gametophytes. Testable hypotheses for future epigenetic research on wild populations of non-model plants are suggested.