Control of Transposon Activity by a Histone H3K4 Demethylase in Rice

Transposon elements (TEs) confer major driving force for genome evolution both in plants and animals. However, the unlimited transpositions of TEs are harmful to the host genome. Thus far, how TEs are controlled by the host genome is still largely unknown.

In this work, Xiaofeng Cao and her colleagues demonstrate that JMJ703, a Jumonji (JMJ) domain containing protein, functions as H3K4me3 demethylase in rice. Two LINE type retrotransposons, Karma and its N-terminal truncation LINE1 were identified as direct targets of JMJ703. In jmj703, the abnormally enriched H3K4me3 at Karma were found to be anti-correlated with DNA methylation. These epigenetic modifications disorder further reactivated the ectopic retrotranspositions of Karma and LINE1 in jmj703.

In addition, they also demonstrated that Tos17, an H3K9me2 targeted LTR subgroup retrotransposon, is unaffected. This prompted them to address such an issue why Karma and Tos17 are controlled by distinct histone modifications. They found that Karma and LINE1 are in heterochromatic regions with depleted H3K4me3, respectively. Whereas Tos17 is in euchromatic region enriched in normal H3K4me3.

Together, their findings implicate that appropriate epigenetic modifications are discriminatively employed by rice genome to specifically control the TEs on the basis of their local chromosomal niche.

These findings provide evidence for the essential role of H3K4 demethylase JMJ703 in proper retrotransposons controlling in rice. It is worth noting that active LINE elements in human genome are the widespread diseases-causing effects. The karyotype similarity between human and rice chromosomes might be a hint for the control of TEs with the same mechanism in human. This work uncovers a linkage between removal an active epigenetic mark and retrotransposon silencing, which would shed light on the tumorigenesis in human.

This work was published online on January 14, 2013 in the Proceedings of the National Academy of Sciences of the United States of America (www.pnas.org/cgi/doi/10.1073/pnas.1217020110). Xiekui Cui, a PhD student of Xiaofeng Cao, is the co-first author of this paper. This work was supported by National Basic Research Program of China and National Natural Science Foundation of China.