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thale cress

This image shows the differences between a pathogen-infected thale cress leaf (top) from a wild type plant (a normal plant with the transposon insertion COPIA-R7 intact) and two mutants (where the mechanism is compromised). The wild type plant remains healthy. The two mutants (middle and bottom) get sick and exhibit disease symptoms caused by the fungal infection.

Credit: Eulgem Lab, UC Riverside.

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How a transposon improves host immunity

Transposons are flexible DNA elements that multiply and change location within the genome—leading them to being called "jumping genes." But, they are also known as transposable elements and even "selfish DNA." Discovered in the 1940s, for years they were thought to be unimportant and appeared to serve no other biological purpose but their own existence.

Now Tokuji Tsuchiya and Thomas Eulgem, geneticists at the University of California, Riverside, challenge these ideas. They report this week in the Proceedings of the National Academy of Sciences that they have discovered a transposon that benefits its host organism.

Working with the thalia cress plant called Arabidopsis—used as a genetic model in plant biology—the scientists found that the COPIA-R7 transposon enhances the immunity of its host. Transposon COPIA-R7 protects Arabidopsis against a microorganism from a large group of fungus-like parasites.

"We provide a new example for an 'adaptive transposon insertion' event — transposon insertions that have beneficial effects on their respective host organisms — and uncover the mechanistic basis of its beneficial effects for plants," said Thomas Eulgem, associate professor of plant cell biology and senior author of the research paper. "While it has been known for a while that transposon insertions can have positive effects on their respective host organisms and accelerate evolution of their hosts, cases of such insertions have been rarely documented and are poorly understood."

The "epigenetic code" helps define the activity state of genes. The movement of transposons is typically inhibited by DNA signals. While the well known 4-letter DNA code instructs the synthesis of proteins, epigenetic signals act as molecular "flags" or "tags" attached to histones—the proteins DNA wraps around to compress it into the cell nucleus—and one flag, known as H3K9me2, prohibits transposons from being active and jumping around within the host genome.

"An exciting aspect of our work is finding that H3K9me2 signals associated with COPIA-R7 have acquired a completely new meaning in RPP7, promoting the activity of this disease-resistance gene," said Eulgem, a member of UC Riverside's Center for Plant Cell Biology. "By modulating levels of the silencing signal in RPP7, plants can adjust the activity of this disease resistance gene.

"Silencing transposon activity is a complex interplay between different epigenetic signals," Eulgem continued. "Typically H3K9me2 is critical for transposon silencing—however, we found H3K9me2 is not important for silencing COPIA-R7, perhaps because this type of epigenetic signal has acquired a different function within the RPP7 gene."

Arabidopsis plants use H3K9me2-mediated messenger RNA to set RPP7 to precisely defined levels. In principle, scientists interested in crop improvement can now use the UCR discovery to design new types of molecular switches based on H3K9me2-mediated messenger RNA. Using standard methods of molecular biology, transposon sequences naturally associated with an epigenetic signal can be inserted into suitable genes, altering the activity levels of those genes.

"Our results are critical to understanding of how transposons can affect the evolution of their hosts — something not well understood at this time," said Tokuji Tsuchiya, the first author of the research paper and an assistant specialist in Eulgem's lab. "Besides this impact on basic research, the epigenetic mechanism we discovered can possibly be used in biotechnological crop improvement. In principle, the switch mechanism we discovered can be applied to all crop species that can be genetically modified."

Next, Eulgem plans to expand his lab's research to how plants modify H3K9me2 levels at COPIA-R7 to adjust RPP7 activity when they are attacked by a pathogenic microorganism—and to explore if this mechanism applies to otherl genes.

"It would make sense to assume that at other transposons, H3K9me2 levels are also modulated during immune responses and that this epigenetic mark affects the activity of other genes that are important for plant immunity," Eulgem said. "If this is true, we have uncovered a completely new genetic — or epigenetic — mechanism that allows plants to sense that they are under pathogen attack and to initiate appropriate immune responses."

Transposable elements (TEs) can drive evolution by creating genetic and epigenetic variation. Although examples of adaptive TE insertions are accumulating, proof that epigenetic information carried by such “domesticated” TEs has been coopted to control host gene function is still limited. We show that COPIA-R7, a TE inserted into the Arabidopsis thaliana disease resistance gene RPP7 recruited the histone mark H3K9me2 to this locus. H3K9me2 levels at COPIA-R7 affect the choice between two alternative RPP7 polyadenylation sites in the pre-mRNA and, thereby, influence the critical balance between RPP7-coding and non–RPP7-coding transcript isoforms. Function of RPP7 is fully dependent on high levels of H3K9me2 at COPIA-R7. We present a direct in vivo demonstration for cooption of a TE-associated histone mark to the epigenetic control of pre-mRNA processing and establish a unique mechanism for regulation of plant immune surveillance gene expression. Our results functionally link a histone mark to alternative polyadenylation and the balance between distinct transcript isoforms from a single gene.

post translational histone modification EDM2 Hyaloperonospora arabidopsidis PHD finger

The research was funded by three grants to Eulgem from the National Science Foundation.
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Original press release: http://www.eurekalert.org/pub_releases/2013-08/uoc--rdb081513.php