Daisuke Muramatsu

Pericentric Heterochromatin Generated by HP1 Protein Interaction-defective Histone Methyltransferase Suv39h1

Background: Histone H3 lysine 9 trimethylation (H3K9me3) and heterochromatin protein HP1 accumulations are hallmarks of heterochromatin. Results: Pericentric accumulation of histone methyltransferase, Suv39h, and Suv39h-mediated H3K9me3 occurs without Suv39h-HP1 binding and HP1 accumulation. Conclusion: The functional relationship between Suv39h and HP1 for pericentric heterochromatin formation is clarified. Significance: The Suv39h-mediated heterochromatin formation can be further elucidated from this model. Pericentric regions form epigenetically organized silent heterochromatin structures that accumulate histone H3 lysine 9 trimethylation (H3K9me3) and HP1. At pericentric regions, Suv39h is the major enzyme that generates H3K9me3. Suv39h also interacts directly with HP1, a methylated H3K9-binding protein. However, it is not well characterized how HP1 interaction is important for Suv39h accumulation and Suv39h-mediated H3K9me3 formation at the pericentromere. To address this, we introduced the HP1 binding-defective N-terminally truncated mouse Suv39h1 (ΔN) into Suv39h-deficient embryonic stem cells. Interestingly, pericentric accumulation of ΔN and ΔN-mediated H3K9me3 was observed to recover, but HP1 accumulation was only marginally restored. ΔN also rescued DNA methyltransferase Dnmt3a and -3b accumulation and DNA methylation of the pericentromere. In contrast, other pericentric heterochromatin features, such as ATRX protein association and H4K20me3, were not recovered. Finally, derepressed major satellite repeats were partially silenced by ΔN expression. These findings clearly showed that the Suv39h-HP1 binding is dispensable for pericentric H3K9me3 and DNA methylation, but this interaction and HP1 recruitment/accumulation seem to be crucial for complete formation of heterochromatin.

Impact of nucleic acid and methylated H3K9 binding activities of Suv39h1 on its heterochromatin assembly

SUV39H is the major histone H3 lysine 9 (H3K9)-specific methyltransferase that targets pericentric regions and is crucial for assembling silent heterochromatin. SUV39H recognizes trimethylated H3K9 (H3K9me3) via its chromodomain (CD), and enriched H3K9me3 allows SUV39H to target specific chromosomal regions. However, the detailed targeting mechanisms, especially for naïve chromatin without preexisting H3K9me3, are poorly understood. Here we show that Suv39h1’s CD (Suv39h1-CD) binds nucleic acids, and this binding is important for its function in heterochromatin assembly. Suv39h1-CD had higher binding affinity for RNA than DNA, and its ability to bind nucleic acids was independent of its H3K9me3 recognition. Suv39h1 bound major satellite RNAs in vivo, and knockdown of major satellite RNAs lowered Suv39h1 retention on pericentromere. Suv39h1 mutational studies indicated that both the nucleic acid–binding and H3K9me–binding activities of Suv39h1-CD were crucial for its pericentric heterochromatin assembly. These results suggest that chromatin-bound RNAs contribute to creating SUV39H’s target specificity. DOI: http://dx.doi.org/10.7554/eLife.25317.001

For whom the male waves: four types of claw-waving display and their audiences in the fiddler crab, Uca lactea

Some animals are known to use several different signals which convey different messages. In the fiddler crab, Uca lactea, I found that males performed at least four types of claw-waving display: lateral-circular, lateral-flick, rapid-vertical, and circular waving. The major audiences and the seasonal occurrence patterns of the displays differed among waving types. Lateral-circular waving (combinations of slow lateral extension, quick flexion, and circumduction of the major claw) was mostly performed to female audiences and was observed frequently in the breeding season. Lateral-flick waving (quick lateral abduction to the audience) was frequently performed to neighbor residents but rarely performed to females in the breeding season. Rapid vertical waving (rapid dorso-ventral protraction and retraction) was observed throughout the observation period and was most frequently performed to burrowless males. Circular waving (simple circumduction) was frequently observed prior to the breeding season and had no obvious audience in most cases. The results showed that males performed different types of claw-waving in different contexts. Males may have needed to use several different types of waving in order to transmit different messages. Digital video images relating to this article are available at http://www.momo-p.com/showdetail-e.php?movieid=momo091127ul01a, http://www.momo-p.com/showdetail-e.php?movieid=momo091127ul02a, http://www.momo-p.com/showdetail-e.php?movieid=momo091127ul03a, http://www.momo-p.com/showdetail-e.php?movieid=momo091127ul04a.

To Build or Not to Build - or to Destroy Burrow Hoods in a Population of Uca Lactea

Abstract Males of several fiddler crab species sometimes construct sand structures (referred to as “hoods” in Uca lactea) at the entrance to their burrow, to which they attract females. Like the bowers of bowerbirds, sand structures of fiddler crabs are external ornaments that exist physically apart from the animals. Despite the mating benefit gained by possessing a structure, many males do not construct structures and some males even destroy their own structures. Structure destruction cannot be explained by the time and energy costs associated with structure construction or maintenance. This implies that the possession of a structure alone can be costly. In the present study on U. lactea, I experimentally planted hoods at the burrows of males that did not have hoods, and compared their frequency of hood destruction with that of control males (builders whose hoods were replaced with those of other males). Non-builders destroyed planted hoods more frequently than control males. Females, which do not construct hoods, also destroyed experimentally planted hoods more frequently than control males. Hoods are able to attract females, but the possession of hoods may incur some costs for crabs, probably because hoods also attract males and non-receptive females. Hence, only males that can afford the costs are likely to construct hoods.

Temporary loss of a sexual signal (claw loss) affects the frequency of sand structure construction in the fiddler crab

In iteroparous animals, individual decisions about when and how much to invest in reproduction are related to lifetime reproductive success, and the ability to assess ones own competitive ability in ones current condition is necessary for optimising the reproductive investment. Male fiddler crabs have an enlarged claw which is used for courtship and combat, but they sometimes lose the claw. The clawless males would have disadvantages in courtship and combat until they regenerated the claw. Here it is examined whether males modify their reproductive investment in response to their current condition. Most clawless males did not construct sand structures to attract females; thus, they invested little in current reproduction. Small males were also less likely to construct structures. Clawless and small males may invest little in current reproduction and instead allocate energy to claw regeneration or body growth for future reproduction, or invest in an alternative mating tactic, such as surface mating.

Sand ornaments used to attract females are avoided by rival males in the fiddler crab Uca lactea

Males of several fiddler crab species sometimes construct sand structures at the entrances to their burrows to which they attract females for mating. Sand structures are thought to exploit fiddler crabs’ risk-reducing behaviour by enticing them into the burrows, so males as well as females are expected to be attracted by the structures. Males with structures may thus incur greater costs to repel intruding males than males without structures, and only males that can afford such costs are likely to build structures. Given that the sand structures are constructed only by males that have sufficient ability to fend off intruders, other crabs may regard the structures as an indicator of those males’ potential fighting ability. In the present study, I showed that burrowless males of Uca lactea were averse to burrows with structures when there were no predators nearby, but that burrowless females showed no such tendency. Sand structures in fiddler crabs may have originated as a sensory trap to attract females, but other males may use the structure as an indicator of the resident male’s fighting ability. However, the sand structures did not appear to function as a signal to attract females.