Limits...
Epigenetic patterns maintained in early Caenorhabditis elegans embryos can be established by gene activity in the parental germ cells.

Arico JK, Katz DJ, van der Vlag J, Kelly WG - PLoS Genet. (2011)

Bottom Line: Expression in the adult germ cells also correlates with more robust expression in the somatic lineages of the offspring.These results suggest that differential expression in the parental germ lines may provide a potential mechanism for the establishment of parent-of-origin epigenomic content.This content can be maintained and may heritably affect gene expression in the offspring.

View Article: PubMed Central - PubMed

Affiliation: Biology Department, Rollins Research Center, Emory University, Atlanta, Georgia, United States of America.

ABSTRACT
Epigenetic information, such as parental imprints, can be transmitted with genetic information from parent to offspring through the germ line. Recent reports show that histone modifications can be transmitted through sperm as a component of this information transfer. How the information that is transferred is established in the parent and maintained in the offspring is poorly understood. We previously described a form of imprinted X inactivation in Caenorhabditis elegans where dimethylation on histone 3 at lysine 4 (H3K4me2), a mark of active chromatin, is excluded from the paternal X chromosome (Xp) during spermatogenesis and persists through early cell divisions in the embryo. Based on the observation that the Xp (unlike the maternal X or any autosome) is largely transcriptionally inactive in the paternal germ line, we hypothesized that transcriptional activity in the parent germ line may influence epigenetic information inherited by and maintained in the embryo. We report that chromatin modifications and histone variant patterns assembled in the germ line can be retained in mature gametes. Furthermore, despite extensive chromatin remodeling events at fertilization, the modification patterns arriving with the gametes are largely retained in the early embryo. Using transgenes, we observe that expression in the parental germline correlates with differential chromatin assembly that is replicated and maintained in the early embryo. Expression in the adult germ cells also correlates with more robust expression in the somatic lineages of the offspring. These results suggest that differential expression in the parental germ lines may provide a potential mechanism for the establishment of parent-of-origin epigenomic content. This content can be maintained and may heritably affect gene expression in the offspring.

Show MeSH

Related in: MedlinePlus

Somatic GFP intensity is higher in offspring from germline expressing than in offspring from germline silent parents.Average GFP intensity (arbitrary units) of somatic nuclei in offspring from germline GFP expressing (KW1336) parents vs germline GFP silenced (N2 outcrossed 20+ generations) parents at larval stages (L2 and L3/L4) and adults. Number of animals scored is indicated in parentheses. Error bars show standard deviation. L2 (p<0.0001). L3/L4 (p<0.009). Adult (p<0.0001).
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC3111476&req=5

pgen-1001391-g006: Somatic GFP intensity is higher in offspring from germline expressing than in offspring from germline silent parents.Average GFP intensity (arbitrary units) of somatic nuclei in offspring from germline GFP expressing (KW1336) parents vs germline GFP silenced (N2 outcrossed 20+ generations) parents at larval stages (L2 and L3/L4) and adults. Number of animals scored is indicated in parentheses. Error bars show standard deviation. L2 (p<0.0001). L3/L4 (p<0.009). Adult (p<0.0001).

Mentions: The increased expression frequency in embryos from the germline-expressing parents, which exceeded the inheritance rate of the transgene, indicated that at least part of the GFP detected in these embryos was provided maternally. We therefore compared GFP fluorescence of the two sets of transgenic offspring at larval and adult stages. L2 larvae through adult stage offspring from germline-expressing parents still showed significantly higher levels of GFP expression compared to the germline-silenced offspring both immediately after germline silencing occurs, and after many generations of the transgene being shut down in the germline (data not shown and Figure 6). These results indicate that, at least for this transgene, expression in the adult germ line strongly correlates with enhanced somatic expression in the offspring, even in late stages of development.


Epigenetic patterns maintained in early Caenorhabditis elegans embryos can be established by gene activity in the parental germ cells.

Arico JK, Katz DJ, van der Vlag J, Kelly WG - PLoS Genet. (2011)

Somatic GFP intensity is higher in offspring from germline expressing than in offspring from germline silent parents.Average GFP intensity (arbitrary units) of somatic nuclei in offspring from germline GFP expressing (KW1336) parents vs germline GFP silenced (N2 outcrossed 20+ generations) parents at larval stages (L2 and L3/L4) and adults. Number of animals scored is indicated in parentheses. Error bars show standard deviation. L2 (p<0.0001). L3/L4 (p<0.009). Adult (p<0.0001).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3111476&req=5

pgen-1001391-g006: Somatic GFP intensity is higher in offspring from germline expressing than in offspring from germline silent parents.Average GFP intensity (arbitrary units) of somatic nuclei in offspring from germline GFP expressing (KW1336) parents vs germline GFP silenced (N2 outcrossed 20+ generations) parents at larval stages (L2 and L3/L4) and adults. Number of animals scored is indicated in parentheses. Error bars show standard deviation. L2 (p<0.0001). L3/L4 (p<0.009). Adult (p<0.0001).
Mentions: The increased expression frequency in embryos from the germline-expressing parents, which exceeded the inheritance rate of the transgene, indicated that at least part of the GFP detected in these embryos was provided maternally. We therefore compared GFP fluorescence of the two sets of transgenic offspring at larval and adult stages. L2 larvae through adult stage offspring from germline-expressing parents still showed significantly higher levels of GFP expression compared to the germline-silenced offspring both immediately after germline silencing occurs, and after many generations of the transgene being shut down in the germline (data not shown and Figure 6). These results indicate that, at least for this transgene, expression in the adult germ line strongly correlates with enhanced somatic expression in the offspring, even in late stages of development.

Bottom Line: Expression in the adult germ cells also correlates with more robust expression in the somatic lineages of the offspring.These results suggest that differential expression in the parental germ lines may provide a potential mechanism for the establishment of parent-of-origin epigenomic content.This content can be maintained and may heritably affect gene expression in the offspring.

View Article: PubMed Central - PubMed

Affiliation: Biology Department, Rollins Research Center, Emory University, Atlanta, Georgia, United States of America.

ABSTRACT
Epigenetic information, such as parental imprints, can be transmitted with genetic information from parent to offspring through the germ line. Recent reports show that histone modifications can be transmitted through sperm as a component of this information transfer. How the information that is transferred is established in the parent and maintained in the offspring is poorly understood. We previously described a form of imprinted X inactivation in Caenorhabditis elegans where dimethylation on histone 3 at lysine 4 (H3K4me2), a mark of active chromatin, is excluded from the paternal X chromosome (Xp) during spermatogenesis and persists through early cell divisions in the embryo. Based on the observation that the Xp (unlike the maternal X or any autosome) is largely transcriptionally inactive in the paternal germ line, we hypothesized that transcriptional activity in the parent germ line may influence epigenetic information inherited by and maintained in the embryo. We report that chromatin modifications and histone variant patterns assembled in the germ line can be retained in mature gametes. Furthermore, despite extensive chromatin remodeling events at fertilization, the modification patterns arriving with the gametes are largely retained in the early embryo. Using transgenes, we observe that expression in the parental germline correlates with differential chromatin assembly that is replicated and maintained in the early embryo. Expression in the adult germ cells also correlates with more robust expression in the somatic lineages of the offspring. These results suggest that differential expression in the parental germ lines may provide a potential mechanism for the establishment of parent-of-origin epigenomic content. This content can be maintained and may heritably affect gene expression in the offspring.

Show MeSH
Related in: MedlinePlus