Somatic epigenetic mosaicism within Pistacia terebinthus (Anacardiaceae) trees leaves signature in reproductive cells

Propagation of epimutations over the branching topology of individuals often produces epigenetic mosaicism in long-lived plants, but whether such epigenetic mosaics can bear some evolutionary relevance remains largely unknown. We test here whether epigenetic reprogramming during gametogenesis completely erases intraplant epigenetic variation or, alternatively, some “signature” of the somatic mosaicism persists into reproductive cells. Intraplant variation in global cytosine methylation of leaf and pollen DNA samples was studied in five adult males of the dioecious tree Pistacia terebinthus (Anacardiaceae). Paired samples of fresh expanding leaves and pollen grains were taken from five different twigs in each tree, and percent cytosine methylation estimated using HPLC. Trees were internally heterogeneous in global cytosine methylation of both leaf and pollen. Within-tree variance accounted for 49.7% and 30.5% of population-wide variance in methylation for leaves and pollen, respectively. Tree means and within-tree variances in pollen methylation were directly correlated, respectively, with tree means and within-tree variances in leaf methylation. As a consequence of the epigenetic variability accumulated in somatic tissues over the individual plants’ lifetimes being only weakly eroded by gametogenesis, intraplant epigenetic heterogeneity became a natural source of epigenetic gametic diversity in the wild-growing population of P. terebinthus trees studied.