Although certain acquired nongenetic (i.e., epigenetic) traits are known to be heritable in plants, little is known currently about whether environmental parameters can induce adaptive epigenetic responses in plants and whether such effects can persist through generations. We used an experimental design based on classical genetics principles to assess whether plants respond to the environmental conditions of their ancestors in an adaptive epigenetic manner. An extensive examination of genetically identical Arabidopsis thaliana (L.) Heynh lines exposed to mild heat (30 °C) or cold (16 °C) treatments in the parental and F1 generations revealed that the prior elevated temperature regime lead to a greater than fivefold improvement in fitness (seed production per individual) for plants exposed to heat in a later generation (F3). The heat-specific fitness improvements among F3 plants were observed even though the heat-treated parental and F1 generations were followed by a generation grown at a normal temperature (F2) and point towards a temperature-induced adaptive epigenetic phenomenon. No such adaptive responses were detected for cold-treated plants, indicating that there are distinctive biological processes inherent to these two temperature regimes. Overall, the data are consistent with the existence of an environmentally induced epigenetic and heritable adaptive response in plants.

One of the main goals of molecular evolutionary biology is to determine the factors that influence the evolutionary rate of selectively neutral DNA, but much remains unknown, especially for plants. Key factors that could alter the mutation rate include environmental tolerances (because they reflect a plants vulnerability to changes in habitat), the pollen : ovule ratio (as it is associated with the number of mitotic divisions) and seed longevity (because this influences the number of generations per unit time in plants). This is the first study to demonstrate that seed bank persistence and drought tolerance are positively associated with molecular evolutionary rates in plants and that pollen : ovule ratio, shade tolerance and salinity tolerance have no detectable relationship. The implications of the findings to our understanding of the impact of environmental agents, the number of cell divisions and cell aging on neutral DNA sequence evolution are discussed.

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