A new mechanism to shape the plant epigenome in response to light

A collaborative study, recently published in eLife by the Centro Nacional de Biotecnología (CNB, Madrid) and the Institut de Biologie de l'Ecole normale supérieure (IBENS, Paris), unveils a mechanism that controls the abundance of specific epigenetic marks in response to an environmental signal, in this case light conditions, to promote an adequate developmental pattern in plants. The components of this mechanism are conserved in other eukaryotic organisms, including humans, in which they influence cell proliferation and differentiation. Conclusions of this study are thus relevant to characterize essential processes in other species.

Epigenetic marks (EM) correspond to chemical modifications on the genetic material such as DNA and associated histone proteins. Among different functions, EM allow different cells of the organism to express specific sets of genes in response to changing environmental and developmental signals. In this way, EM act as key regulators of cell proliferation and differentiation. However, the mechanisms that control accumulation of EM throughout an eukaryotic genome in response to external and internal stimuli are poorly known.

In this study, the CNB and IBENS teams uncover that DE-ETIOLATED 1 (DET1), an evolutionarily conserved component of the ubiquitination machinery in multicellular organisms, modulates the accumulation of specific EM on the chromatin of model plant Arabidopsis. More precisely, DET1 determines the genome-wide abundance of Histone H2B monoubiquitination (H2Bub), which is regulated over many Arabidopsis genes upon light exposure to trigger their expression. For this, DET1 controls the stability of a newly characterized H2Bub deubiquitination module (DUBm), whose stability, and consequently cellular abundance, are subject to dramatic variations in response to light signaling. DUBm accumulates in the presence of light but much less in dark-grown plants (for example, upon seed germination underground), when DUBm is degraded in a DET1-dependent manner. Consequently, under dark conditions, H2Bub dynamics remain stalled, possibly limiting the expression of light-responsive genes.

Based on these findings, a model is proposed in which DET1 antagonizes DUBm activity through its proteolytic degradation depending on light/dark conditions. This allows integration of light signals for plants to acquire adequate patterns of H2Bub and correct transcriptional activity. Collectively, this collaborative work unveils a novel mechanism to control the accumulation on an EM over the genome in response to environmental changes. Noteworthy, the components of this pathway; DET1, DUBm, H2Bub, are conserved in other eukaryotic organisms, including humans where these factors are involved in diverse cancer types. Future studies will show whether there are functional relationships between these factors in humans, and will allow identifying the processes they regulate and the external and internal signal governing them.

This study is part of a collaboration between the group of Dr. Vicente Rubio (CNB-CSIC) and that of Drs. Fredy Barneche and Chris Bowler (Institut de biologie de l'Ecole normale supérieure, IBENS, Paris).

Amr Nassrallah, Martin Rougée, Clara Bourbousse, Stephanie Drevensek, Sandra Fonseca, Elisa Iniesto, Ouardia Ait-Mohamed, Anne-Flore Deton-Cabanillas, Gerald Zabulon, Ikhlak Ahmed, David Stroebel, Vanessa Masson, Berangere Lombard, Dominique Eeckhout, Kris Gevaert, Damarys Loew, Auguste Genovesio, Cecile Breyton, Geert de Jaeger, Chris Bowler, Vicente Rubio, Fredy Barneche. DET1-mediated degradation of a SAGA-like deubiquitination module controls H2Bub homeostasis. Elife. 2018 Sep 7;7. pii: e37892. doi: 10.7554/eLife.37892.