Heterosis is a fundamental biological phenomenon characterized by the superior performance of a hybrid over its parents in many traits, but the underlying molecular basis remains elusive. To investigate whether DNA methylation plays a role in heterosis, we compared at single-base-pair resolution the DNA methylomes of Arabidopsis thaliana Landsberg erecta and C24 parental lines and their reciprocal F1 hybrids that exhibited heterosis. Both hybrids displayed increased DNA methylation across their entire genomes, especially in transposable elements. Interestingly, increased methylation of the hybrid genomes predominantly occurred in regions that were differentially methylated in the two parents and covered by small RNAs, implying that the RNAdirected DNA methylation (RdDM) pathway may direct DNA methylation in hybrids. In addition, we found that 77 genes sensitive to methylome remodeling were transcriptionally repressed in both reciprocal hybrids, including genes involved in flavonoid biosynthesis and two circadian oscillator genes CIRCADIAN CLOCK ASSOCIATED1 and LATE ELONGATED HYPOCOTYL. Moreover, growth vigor of F1 hybrids was compromised by treatment with an agent that demethylates DNA and by abolishing production of functional small RNAs due to mutations in Arabidopsis RNA methyltransferase HUA ENHANCER1. Together, our data suggest that genome-wide remodeling of DNA methylation directed by the RdDM pathway may play a role in heterosis.

The ability to switch from skotomorphogenesis to photomorphogenesis is essential for seedling development and plant survival. Recent studies revealed that COP1 and phytochrome-interacting factors

Summary The changing environments strongly affect plants growth and development. Phytohormones, endogenous plant-made small molecules such as ethylene, regulate a wide range of processes throughout the lifetime of plants[1, 2]. The ability of plants to integrate external signals with endogenous regulatory pathways is vital for their survival [3, 4]. Ethylene was found to suppress hypocotyl elongation in darkness[5], while promote it in light[6, 7]. How ethylene regulates hypocotyl elongation in such an opposite way is largely unknown. In particular, how light modulates and even reverses the function of ethylene has yet to be characterized. Here we show that the bHLH transcription factor Phytochrome-Interacting Factor 3 (PIF3), is directly activated by Ethylene-Insensitive 3 (EIN3), and is indispensible for ethylene-induced hypocotyl elongation in light. Ethylene via EIN3 concomitantly activates two contrasting pathways: the PIF3-dependent growth-promoting pathway and an Ethylene-Response Factor 1 (ERF1)-mediated growth-inhibiting pathway. The PIF3 pathway is saturated in dark but progressively fortified with light de-stabilizing PIF proteins to reduce their redundancy. While the ERF1 pathway is mainly functional in dark but gradually saturated with light dramatically stabilizing ERF1 protein. Our findings provide a mechanistic insight into how light modulates internal hormone-regulated plant growth.