Transgenerational plasticity is sex-dependent and persistent in yellow monkeyflower (Mimulus guttatus)

Abstract

Transgenerational phenotypic plasticity, whereby environmental cues experienced by parents alter the phenotype of their progeny, has now been documented in diverse organisms. Transmission of environmentally determined responses is known to occur through both maternal and paternal gametes, but the underlying mechanisms have rarely been compared. In addition, the persistence of induction over multiple generations appears to vary widely, but has been characterized for relatively few systems. Yellow monkeyflower (Mimulus guttatus) is known to exhibit transgenerational induction of increased glandular trichome production in response to simulated insect damage. Here, we test for differences between maternal and paternal transmission of this response and examine its persistence over five generations following damage. Maternal and paternal damage resulted in similar and apparently additive increases in progeny trichome production. Treatment of germinating seeds with the genome-wide demethylating agent 5-azacytidine erased the effect of maternal but not paternal damage. The number of glandular trichomes remained elevated for three generations following damage. These results indicate that transgenerational transmission occurs through both maternal and paternal germ lines, but that they differ in the proximate mechanism of epigenetic inheritance. Our results also indicate that a wounding response can persist for multiple generations in the absence of subsequent damage.

Keywords: Mimulus; epigenetic inheritance; induced defense; transgenerational plasticity; trichome.

Figure 1

Number of glandular trichomes produced along a mid-leaf transect across the underside of both leaves in the 5th leaf pair. Bars represent marginal means for each combination of maternal and paternal damage, for control plants and plants treated with 5-azacytidine at germination. Letters indicate significant differences measured via pairwise comparisons within control or 5-azacytidine treated plants (α = 0.05). Error bars show ± 1 SE. N = 1314.

Figure 2

Number of glandular trichomes along a mid-leaf transect for 5 generations of plants originating from either control or damaged Generation 0 ancestors and produced by self-pollination. Bars represent marginal means for each combination of generation and ancestral damage treatment. Error bars show 95% credible intervals. N = 670.