Di- and Tri- but Not Monomethylation on Histone H3 Lysine 36 Marks Active Transcription of Genes Involved in Flowering Time Regulation and Other Processes in Arabidopsis thaliana

Abstract

Histone lysines can be mono-, di-, or trimethylated, providing an ample magnitude of epigenetic information for transcription regulation. In fungi, SET2 is the sole methyltransferase responsible for mono-, di-, and trimethylation of H3K36. Here we show that in Arabidopsis thaliana, the degree of H3K36 methylation is regulated by distinct methyltransferases. The SET2 homologs SDG8 and SDG26 each can methylate oligonucleosomes in vitro, and both proteins are localized in the nucleus. While the previously reported loss-offunction sdg8 mutants have an early-flowering phenotype, the loss-of-function sdg26 mutants show a lateflowering phenotype. Consistently, several MADS-box flowering repressors are down-regulated by sdg8 but up-regulated by sdg26. The sdg8 but not the sdg26 mutant plants show a dramatically reduced level of both diand trimethyl-H3K36 and an increased level of monomethyl-H3K36. SDG8 is thus specifically required for diand trimethylation of H3K36. Our results further establish that H3K36 di-and tri-but not monomethylation correlates with transcription activation. Finally, we show that SDG8 and VIP4, which encodes a component of the PAF1 complex, act independently and synergistically in transcription regulation. Together our results reveal that the deposition of H3K36 methylation is finely regulated, possibly to cope with the complex regulation of growth and development in higher eukaryotes.During the past few years, histone lysine (K) methylation has been viewed to play widespread roles in transcriptional regulation, DNA repair, and epigenetic inheritance (15, 32). It occurs on histone H3K4, H3K9, H3K27, H3K36, and H4K20 in several studied eukaryotes. In general, H3K4 and H3K36 methylation is associated with actively transcribed genes, whereas H3K9, H3K27, and H4K20 methylation is associated with transcriptional repression and silenced chromatin regions. Furthermore, K residues can be mono-, di-or trimethylated, and the degree of methylation on H3K4, H3K9, H3K27, and H4K20 has considerable influence on transcriptional activation or repression (15,43,55,63). In comparison, methylation on H3K36 is less extensively characterized. In fungi, such as Saccharomyces cerevisiae, Schizosaccharomyces pombe, and Neurospora crassa, a sole histone-lysine-methyltransferase (HKMT), SET2, is responsible for mono-, di-, and trimethylation of H3K36 (1, 35, 49). In mammals, both the Sotos syndrome and leukemia-associated protein NSD1 and the Huntington disease protein HYPB can methylate H3K36 in vitro (42,50). In Arabidopsis thaliana, the loss-of-function sdg8 (also named efs) mutants show a dramatically reduced level of H3K36 dimethylation and an early-flowering phenotype (25,65). Because of these phenotype-associated crucial functions, unraveling the mechanism of deposition of H3K36 methylation in mammals and in plants is of particular importance.Proper timing of flowering is pivotal for the reproductive success of plants and thus is controlled by complex genetic networks, which involve histone modifications and chroma...

SET DOMAIN GROUP2 is the major histone H3 lysine 4 trimethyltransferase in Arabidopsis

“…These findings suggest that histone methylation may play broad and important roles in regulating transcription. Consistent with this notion, several Arabidopsis histone methyltransferase (HMTase) mutants have been found to exhibit a myriad of developmental abnormalities (12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26). Furthermore, transcriptome profiling studies have identified numerous genes that are misregulated in HMTase mutants (19,27,28).…”

“…The substrate specificities and mutant transcriptional profiles have been previously described for two other Arabidopsis histone methyltransferases: ATX1/SDG27 (H3K4me) and the ASHH2/ SDG8 (H3K36me) (19,27). If SDG2 is functionally similar to ATX1 or ASHH2, one might expect similar transcriptional changes in these mutants.…”

“…In four of the five classes, the plant SDGs seem to share similar enzymatic activities with their animal and/or fungal homologs. Specifically, class I SDGs are involved in H3K27me2/3, class II in H3K36me2/3, class III in H3K4me2/3, and class V in H3K9me2 (13,19,33,34). Class IV seems to be an exception: the Arabidopsis proteins SDG15 and SDG34 are responsible for H3K27me1 (24), but it is not clear whether the two yeast homologs (SET3 and SET4) possess HMTase activity.…”

Rice jmjC domain-containing gene JMJ706 encodes H3K9 demethylase required for floral organ development

“…Therefore, JMJ706 may play a role in the conversion between H3K36me1 and H3K36me2. It has recently been shown that H3K36me1 has different function than H3K36me2/me3 in transcriptional regulation in plants (28). Although rice JMJ706 is constitutively expressed (Fig.…”

High-resolution mapping of H4K16 and H3K23 acetylation reveals conserved and unique distribution patterns inArabidopsisand rice

“…H4K16ac is positively correlated with active marks (H3K9ac, H3K18ac, H3K4me2/3 and H3K36me2/3 15,[42][43][44] ) and anti-correlated with repressive modifications (H3K27me1 and H3K9me2 15,45 ) and histone variants H3.1 and H2A.W, which are required for heterochromatin condensation ( Fig. 2A).…”