In any living organism, all cells have the same DNA, but each cell's identity is defined by the combination of genes that are turned on or off, any given moment in time. In animals, this cellular memory is erased between generations, so that the new egg has no memory and, as such, has the potential to become any type of cell. In flowering plants, on the contrary, cellular memory passes from generation to generation, with potentially harmful implications for the development of new plants. In the latest issue of the journal Cell*, scientists from Instituto Gulbenkian de Ciência (IGC), in Portugal, and Cold Spring Harbor Laboratory (CSHL), in the USA, describe a novel mechanism whereby potentially mutagenic sequences of mobile DNA are silenced in the pollen grain and in seeds, thus avoiding damage to new plants.
One of the main mechanisms that contributes to cellular memory is the addition of a chemical group - the methyl group - to DNA sequences (a process called methylation). DNA methylation turns a gene off. These changes in gene expression that are heritable, but not directly written in the DNA sequence, are called epigenetics. Using the plant model Arabidopsis thaliana, Jörg Becker, José Feijó and their team, at the IGC, and Robert Martienssen and colleagues, at CSHL, analysed the genome of pollen grains and their precursor cells, the microspores, and pinpointed the sequences of DNA that were methylated. Pollen grains contain two sperm cells (the sexual cells) and an accompanying vegetative nucleus, whose DNA is not passed on to the next generation. Thanks to the technique developed by the IGC team, the researchers were able to separate the two sperm cells and the vegetative nucleus of the pollen grain and look at their methylation status separately.
Joseph Calarco (in the Martienssen lab) and Filipe Borges (in the Becker lab) observed that DNA methylation is largely maintained in the microspores and pollen grains. But there are differences between the different cell types. In the pollen grain, some DNA sequences are methylated in sperm cells but not in the vegetative nucleus, and vice versa. Amongst these non-methylated genes are mobile sequences of DNA, called transposable elements, which could become active and lead to mutagenic effects.
The research team discovered that the situation is rescued by small sequences of RNA (called siRNAs) that restore methylation of transposable elements in the embryo. Indeed, they have found siRNA in sperm cells that silence the transposable elements even before fertilisation, in at least some cases. Transposable elements are very common in all known genomes. In the human genome, for example, they make up 45% of the total genome. They are involved in the evolution of genomes, since when integrated back into the genome they can affect the function and organisation of other genes. However, transposable elements are mutagens, and, therefore, their activation needs to be under tight control, as it may be harmful to the cell and the organism. If such harmful mutations occur in sexual cells, they will be transmitted to the progeny and spread in the population.
Says Jörg Becker, 'We have unveiled a mechanism in the sexual cells that can prevent the activation of potentially harmful transposable elements, while at the same time, upon fusion of sperm cell and egg cell, allowing the formation of a cell with full capacity to become any cell type, that will give rise to a new generation. On the other hand, if female siRNAs in the egg cell do not match incoming transposable elements from the male, they might escape silencing in the developing embryo, with potentially harmful implications for the new plant that is generated. Such an uncontrolled activation of transposable elements might at least in part explain existing hybridization barriers, in which crosses between species result in seed abortion or infertility. Breaking such barriers would increase plant breeder's chances to improve crop species by making use of the phenomenon of hybrid vigor, in which the offspring shows qualities superior to its parents, well exemplified in widely used corn and rice hybrids.'
It was known that flowering plants are an exception to the rule of resetting cellular memory, since modifications may be inherited for hundreds of generations. But the extent to which this happened in the plant sexual cells and how the epigenetic reprogramming of the genome might contribute remained unclear until now. The mechanism now described may also become a strong argument to explain why sexual reproduction evolved and became so prevalent in most higher organisms.
This study was supported by the National Institutes of Health (NIH) in the USA, and Fundação para a Ciência e a Tecnologia (FCT), in Portugal. *Joseph P. Calarco, Filipe Borges, Mark T.A. Donoghue, Frédéric Van Ex, Pauline E. Julien, Telma Lopes, Rui Gardner, Frédéric Berger, José A. Feijó, Jörg D. Becker, Robert A. Martienssen. (2012) Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell.
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