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Developmental Biology - Histones
How Plants Forget
New research uncovers how a specific epigenetic mark is reset in sperm - allowing for change...
Although they do it differently than humans, plants also have memories.
For example, many plants can sense and remember prolonged cold in the Winter to ensure they flower at the right time during the Spring. This so-called "epigenetic memory" occurs by modifying specialized proteins called histones, which package DNA to fit within the nucleus. Histones also index what DNA exists within a plant or animal cell.
One such modified histone, called H3K27me3, appears to mark genes to be turned off.
When deciding when to grow flowers, cold conditions cause H3K27me3 to accumulate in "flower" genes and suppress their activity.
Previous work from the Berger lab has shown how H3K27me3 is faithfully transmitted from cell to cell.
When Spring or warmer climate begins, histones are released from flowering genes which can now respond unencumbered ("unsuppressed") and unfurl modified leaves we know as petals.
Thus flowering occurs in a warm temperature and in a season indicating winter is over.
But, just as importantly, once they've flowered and made seeds, these seeds need to forget this 'memory' of cold temperature. They need to be able to flower again once a new winter is over. As H3K27me3 is faithfully copied from cell to cell, how do plants forget this memory when making new seeds?
To answer this question, an international team lead by Dr. Michael Borg, a postdoc in the lab of Dr. Frédéric Berger at the Gregor Mendel Institute, Austrian Academy of Sciences, analysed histones in pollen. He hypothesized the process of "forgetting" is most likely embedded in sperm. Sperm carry changes in DNA "data" more frequently than any other cell in the body.
However, researchers were surprised to find H3K27me3 completely disappears in sperm!
They found that sperm accumulate a special histone that is unable to carry H3K27me3. This ensures this cold temperature modification is erased from hundreds of plant genes. Not just those that prevent flowering — but also those genes that control large and important functions in seeds.
"This actually makes a lot of sense from an ecological perspective. Pollen can spread over long distances, by wind or bees for example. Much of their "memory" is carried in H3K27me3 and must adapt to new environments. So seeds should "forget" their dad's environment and remember their mother's, as they are most likely spread and grow next to mom."
Jörg Becker PhD, Principal Investigator, Instituto Gulbenkian de Ciência, led by Frédéric Berger PhD, Gregor Mendel Institute of the Gregor Mendel Institute, Austria.
According to Dr. Berger: "Like plants, animals also erase this epigenetic memory in sperm, but they do it by replacing histones with a completely different protein. This is one of the first examples of how a specialized histone can help reprogram and reset a single epigenetic mark while leaving others untouched. There are many more unstudied histone variants in both plants and animals. We expect that aspects of this resetting mechanism which we discovered, will be found in other organisms and developmental contexts."
The research paper can be read in Nature Cell Biology.
Abstract
Epigenetic marks are reprogrammed in the gametes to reset genomic potential in the next generation. In mammals, paternal chromatin is extensively reprogrammed through the global erasure of DNA methylation and the exchange of histones with protamines1,2. Precisely how the paternal epigenome is reprogrammed in flowering plants has remained unclear since DNA is not demethylated and histones are retained in sperm3,4. Here, we describe a multi-layered mechanism by which H3K27me3 is globally lost from histone-based sperm chromatin in Arabidopsis. This mechanism involves the silencing of H3K27me3 writers, activity of H3K27me3 erasers and deposition of a sperm-specific histone, H3.10 (ref. 5), which we show is immune to lysine 27 methylation. The loss of H3K27me3 facilitates the transcription of genes essential for spermatogenesis and pre-configures sperm with a chromatin state that forecasts gene expression in the next generation. Thus, plants have evolved a specific mechanism to simultaneously differentiate male gametes and reprogram the paternal epigenome.
Authors
Michael Borg, Yannick Jacob, Daichi Susaki, Chantal LeBlanc, Daniel Buendía, Elin Axelsson, Tomokazu Kawashima, Philipp Voigt, Leonor Boavida, Jörg Becker, Tetsuya Higashiyama, Robert Martienssen and Frédéric Berger.
Acknowledgements
About the GMI The Gregor Mendel Institute of Molecular Plant Biology (GMI) was founded by the Austrian Academy of Sciences in 2000 to promote research excellence in plant molecular biology. It is the only international center dedicated to basic plant research in Austria and one of very few throughout the world. Nine research groups study many aspects of plant molecular genetics, including epigenetics, cell biology, plant-pathogen interactions, developmental biology, and population genetics. The GMI is part of the Vienna BioCenter, one of Europe's foremost life science research locations.
The authors thank P. Andersen and J. M. Watson for critical reading of the manuscript, Z. Lorkovic and S. Akimcheva for guidance and technical support, T. Suzuki for sequencing the egg cell transcriptome, and Life Science Editors for editing services. We also thank the Vienna BioCenter Core Facilities for Next Generation Sequencing, Plant Science, HistoPathology, the IMP/IMBA BioOptics Facility and the MENDEL High-Performance Computing team. This work was supported through core funding from the Gregor Mendel Institute, and external grants from the FWF (P 26887 and I 4258) and ERA-CAPS (EVO-REPRO I 2163). M.B. was supported through an FWF Lise Meitner fellowship (M 1818). Y.J., C.L. and R.M. were supported by the Howard Hughes Medical Institute and NIH funding (R01 GM067014). D.S. and T.H. were supported by the Japan Society for the Promotion of Science (18J01963 to D.S. and 16H06464, 16H06465 and 16K21727 to T.H.). P.V. was supported by the Wellcome Trust (104175/Z/14/Z; Sir Henry Dale Fellowship), ERC EU Horizon 2020 research and innovation programme (ERC-STG grant agreement 639253) and core funding from the Wellcome Trust (203149).
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