H2A.Z-Containing Nucleosomes Mediate the Thermosensory Response in Arabidopsis

Abstract

Plants are highly sensitive to temperature and can perceive a difference of as little as 1 degrees C. How temperature is sensed and integrated in development is unknown. In a forward genetic screen in Arabidopsis, we have found that nucleosomes containing the alternative histone H2A.Z are essential to perceiving ambient temperature correctly. Genotypes deficient in incorporating H2A.Z into nucleosomes phenocopy warm grown plants, and show a striking constitutive warm temperature transcriptome. We show that nucleosomes containing H2A.Z display distinct responses to temperature in vivo, independently of transcription. Using purified nucleosomes, we are able to show that H2A.Z confers distinct DNA-unwrapping properties on nucleosomes, indicating a direct mechanism for the perception of temperature through DNA-nucleosome fluctuations. Our results show that H2A.Z-containing nucleosomes provide thermosensory information that is used to coordinate the ambient temperature transcriptome. We observe the same effect in budding yeast, indicating that this is an evolutionarily conserved mechanism.

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“…2A). [46][47][48][49][50] Interestingly, our results showed a significant positive correlation between H4K16ac and H3K23ac (Pearson's correlation coefficient D 0.73, P < 2.2 £ 10 ¡16 ), previously shown to be associated with transcriptional activation. 18 It is to be noted that the published H3K23ac ChIP-seq was performed using 3-week-old leaves, 18 whereas, in our study, H4K16ac was profiled from 2-week-old seedlings.…”

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“…This influences the ability of RNAP II to transcribe this gene, thus eliciting a temperature response. 27 In agreement with this scenario, the arp6 mutant, which is deficient in H2A.Z deposition, displays, among other phenotypes, a constitutive warm temperature response. Sandra Cortijo, from Phil Wigge's group (The Sainsbury Laboratory, Cambridge, UK), presented new insight into the interplay between the H2A.Z occupancy and transcriptional changes in response to temperature variations.…”

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“…H2A.Z nucleosomes have been shown to regulate transcription in a temperature-dependent manner in Arabidopsis as their occupancy in transcriptional start sites of genes reduces with concomitant increases in temperature [11]. However, little is known about the mechanisms controlling temperature-dependent grain development in grasses.…”