Phenotypic plasticity at the molecular scale

Despite the abundance of studies investigating the phenotypes produced in response to changing environments, the molecular mechanisms underlying phenotypic variation remain still largely unknown in both plants and animals. Organisms need to process environmental signals and respond appropriately accordingly to their significance. They achieve this through a system common to all organisms based on signal reception, transduction and translation, and the resulting product(s). In particular, environmental stimuli are perceived and transmitted by different signal transduction pathways. These pathways switch on specific transcription factors, which activate genes, ultimately affecting the phenotype.

Notably, in some cases, this process driving phenotypic plasticity was affected by epigenetic mechanisms (Schlichting, 1986; Mirouze and Paszkowski, 2011). Epigenetic mechanisms (e.g. changes in chromatin structure and small RNAs) can regulate gene expression at both the transcriptional and post-transcriptional level. Thus, epigenetic modifications could be a key mechanism in the modulation of gene expression after the environmental signal perception. This hypothesis received support by accumulating evidence that epigenetic modifications may contribute to the regulation of phenotypically plastic traits (e.g. Tatra et al., 2000; Bossdorf et al., 2010; Kooke et al., 2015). One of the best-studied examples is the timing of flowering, in which epigenetic factors evidently play an essential role (He, 2009; Jeong et al., 2015). Proper flowering time is crucial to ensure reproductive success, especially in annual species. Therefore, it is finely regulated by integrating various endogenous and environmental signals to ensure that flowering initiates under the most favorable conditions. In A. thaliana, among other environmental signals, flowering time is regulated by cold exposure through the vernalization pathway. In this pathway, prolonged exposure to low temperatures triggers flowering by silencing the flowering repressor FLOWERING LOCUS C (FLC) through epigenetic modifications (Bastow et al., 2004; Sung and Amasino, 2004; Sung et al., 2006; Finnegan and Dennis, 2007; Greb et al., 2007; Schmitz et al., 2008). This repression is mitotically stable and allows rapid flowering in spring. It functions as a memory of prior cold exposure. However, FLC expression is re-activated during embryogenesis so that the next generation requires vernalization again to accelerate flowering (Sheldon et al., 2008). Therefore, vernalization-mediated FLC repression is mitotically stable but meiotically unstable, and this way reliably times one of the most critical transitions for an annual plant. Clearly, the vernalization response (accelerated flowering) is not immediately triggered by the stimulus (low temperatures); on the contrary, the plant starts flowering when the original stimulus (low temperatures) is removed. This is possible thanks to the epigenetic basis of vernalization, which allows preserving the low-temperature stimulus occurring in winter until the following spring, promoting in this way the floral transition (Lang, 1965).

In conclusion, despite the genetic and epigenetic basis of some phenotypic responses are relatively well characterized (e.g. flowering time), the molecular mechanisms regulating the majority of phenotypic responses remain poorly understood. More studies are thus needed to unravel the role of epigenetic mechanisms in phenotypic plasticity, improving our understanding of the role of epigenetic mechanisms in evolution and adaptation.