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Somatic and germline expression of piwi during development and regeneration in the marine polychaete annelid Capitella teleta.

Giani VC, Yamaguchi E, Boyle MJ, Seaver EC - Evodevo (2011)

Bottom Line: Ct-piwi1 is expressed in regenerating tissue, and once segments differentiate, it becomes most prominent in the posterior growth zone and immature oocytes in regenerating ovaries of regenerating segments.In C. teleta, piwi genes may have retained an ancestral role as genetic regulators of both somatic and germline stem cells.It is likely that piwi genes, and associated stem cell co-regulators, became restricted to the germline in some taxa during the course of evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: Kewalo Marine Laboratory, PBRC/University of Hawaii, 41 Ahui St,, Honolulu, HI 96813, USA. seaver@hawaii.edu.

ABSTRACT

Background: Stem cells have a critical role during adult growth and regeneration. Germline stem cells are specialized stem cells that produce gametes during sexual reproduction. Capitella teleta (formerly Capitella sp. I) is a polychaete annelid that reproduces sexually, exhibits adult growth and regeneration, and thus, is a good model to study the relationship between somatic and germline stem cells.

Results: We characterize expression of the two C. teleta orthologs of piwi, genes with roles in germline development in diverse organisms. Ct-piwi1 and Ct-piwi2 are expressed throughout the life cycle in a dynamic pattern that includes both somatic and germline cells, and show nearly identical expression patterns at all stages examined. Both genes are broadly expressed during embryonic and larval development, gradually becoming restricted to putative primordial germ cells (PGCs) and the posterior growth zone. In juveniles, Ct-piwi1 is expressed in the presumptive gonads, and in reproductive adults, it is detected in gonads and the posterior growth zone. In addition, Ct-piwi1 is expressed in a population of putative PGCs that persist in sexually mature adults, likely in a stem cell niche. Ct-piwi1 is expressed in regenerating tissue, and once segments differentiate, it becomes most prominent in the posterior growth zone and immature oocytes in regenerating ovaries of regenerating segments.

Conclusions: In C. teleta, piwi genes may have retained an ancestral role as genetic regulators of both somatic and germline stem cells. It is likely that piwi genes, and associated stem cell co-regulators, became restricted to the germline in some taxa during the course of evolution.

No MeSH data available.


Related in: MedlinePlus

Pattern of Ct-piwi1 expression and EdU incorporation in a stage 7 larva. Larva were exposed to EdU for one hour. All images are from the same animal and same focal plane. All panels are a ventral view with anterior to the left. Abbreviations: fg, foregut; pgz, posterior growth zone. (A) DIC image of a stage 7 larva showing Ct-piwi1 expression in the foregut, posterior growth zone, and two asymmetrically positioned ventro-lateral cell clusters (black arrows). (B) Fluorescently tagged EdU labeling (green) shows regions of dividing cells in the foregut, and posterior growth zone. Note the absence of dividing cells in the Ct-piwi1-expressing asymmetrically positioned ventro-lateral cell clusters (white arrows). (C) A close-up view of the Ct-piwi1 positive asymmetrically positioned ventro-lateral cell clusters (white arrows) from panel (B). (D) Combined DIC and fluorescent images in the region of the posterior growth zone showing co-localization of Ct-piwi1 expression with EdU incorporation. Scale bar, 50 μm for all panels.
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Figure 4: Pattern of Ct-piwi1 expression and EdU incorporation in a stage 7 larva. Larva were exposed to EdU for one hour. All images are from the same animal and same focal plane. All panels are a ventral view with anterior to the left. Abbreviations: fg, foregut; pgz, posterior growth zone. (A) DIC image of a stage 7 larva showing Ct-piwi1 expression in the foregut, posterior growth zone, and two asymmetrically positioned ventro-lateral cell clusters (black arrows). (B) Fluorescently tagged EdU labeling (green) shows regions of dividing cells in the foregut, and posterior growth zone. Note the absence of dividing cells in the Ct-piwi1-expressing asymmetrically positioned ventro-lateral cell clusters (white arrows). (C) A close-up view of the Ct-piwi1 positive asymmetrically positioned ventro-lateral cell clusters (white arrows) from panel (B). (D) Combined DIC and fluorescent images in the region of the posterior growth zone showing co-localization of Ct-piwi1 expression with EdU incorporation. Scale bar, 50 μm for all panels.

Mentions: The position of Ct-piwi1 expression domains was characterized in relation to patterns of cell division in larvae as visualized by EdU incorporation. A comprehensive study of cell division patterns during larval development of C. teleta has been previously reported [27]. Ct-piwi1 expression corresponds with regions of dividing cells in C. teleta larvae, including in the foregut and posterior growth zone in stage 7 larvae (Figure 4A, B, D). However, there are also EdU positive cells that lack Ct-piwi1 expression, and there are Ct-piwi1 positive cells that do not appear to be EdU positive (Figure 4A, B, C, arrows). For example, the putative PGCs are not EdU positive, consistent with our observations that the number of cells does not appear to increase during larval stages. Therefore, there is only partial overlap of these two patterns.


Somatic and germline expression of piwi during development and regeneration in the marine polychaete annelid Capitella teleta.

Giani VC, Yamaguchi E, Boyle MJ, Seaver EC - Evodevo (2011)

Pattern of Ct-piwi1 expression and EdU incorporation in a stage 7 larva. Larva were exposed to EdU for one hour. All images are from the same animal and same focal plane. All panels are a ventral view with anterior to the left. Abbreviations: fg, foregut; pgz, posterior growth zone. (A) DIC image of a stage 7 larva showing Ct-piwi1 expression in the foregut, posterior growth zone, and two asymmetrically positioned ventro-lateral cell clusters (black arrows). (B) Fluorescently tagged EdU labeling (green) shows regions of dividing cells in the foregut, and posterior growth zone. Note the absence of dividing cells in the Ct-piwi1-expressing asymmetrically positioned ventro-lateral cell clusters (white arrows). (C) A close-up view of the Ct-piwi1 positive asymmetrically positioned ventro-lateral cell clusters (white arrows) from panel (B). (D) Combined DIC and fluorescent images in the region of the posterior growth zone showing co-localization of Ct-piwi1 expression with EdU incorporation. Scale bar, 50 μm for all panels.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3113731&req=5

Figure 4: Pattern of Ct-piwi1 expression and EdU incorporation in a stage 7 larva. Larva were exposed to EdU for one hour. All images are from the same animal and same focal plane. All panels are a ventral view with anterior to the left. Abbreviations: fg, foregut; pgz, posterior growth zone. (A) DIC image of a stage 7 larva showing Ct-piwi1 expression in the foregut, posterior growth zone, and two asymmetrically positioned ventro-lateral cell clusters (black arrows). (B) Fluorescently tagged EdU labeling (green) shows regions of dividing cells in the foregut, and posterior growth zone. Note the absence of dividing cells in the Ct-piwi1-expressing asymmetrically positioned ventro-lateral cell clusters (white arrows). (C) A close-up view of the Ct-piwi1 positive asymmetrically positioned ventro-lateral cell clusters (white arrows) from panel (B). (D) Combined DIC and fluorescent images in the region of the posterior growth zone showing co-localization of Ct-piwi1 expression with EdU incorporation. Scale bar, 50 μm for all panels.
Mentions: The position of Ct-piwi1 expression domains was characterized in relation to patterns of cell division in larvae as visualized by EdU incorporation. A comprehensive study of cell division patterns during larval development of C. teleta has been previously reported [27]. Ct-piwi1 expression corresponds with regions of dividing cells in C. teleta larvae, including in the foregut and posterior growth zone in stage 7 larvae (Figure 4A, B, D). However, there are also EdU positive cells that lack Ct-piwi1 expression, and there are Ct-piwi1 positive cells that do not appear to be EdU positive (Figure 4A, B, C, arrows). For example, the putative PGCs are not EdU positive, consistent with our observations that the number of cells does not appear to increase during larval stages. Therefore, there is only partial overlap of these two patterns.

Bottom Line: Ct-piwi1 is expressed in regenerating tissue, and once segments differentiate, it becomes most prominent in the posterior growth zone and immature oocytes in regenerating ovaries of regenerating segments.In C. teleta, piwi genes may have retained an ancestral role as genetic regulators of both somatic and germline stem cells.It is likely that piwi genes, and associated stem cell co-regulators, became restricted to the germline in some taxa during the course of evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: Kewalo Marine Laboratory, PBRC/University of Hawaii, 41 Ahui St,, Honolulu, HI 96813, USA. seaver@hawaii.edu.

ABSTRACT

Background: Stem cells have a critical role during adult growth and regeneration. Germline stem cells are specialized stem cells that produce gametes during sexual reproduction. Capitella teleta (formerly Capitella sp. I) is a polychaete annelid that reproduces sexually, exhibits adult growth and regeneration, and thus, is a good model to study the relationship between somatic and germline stem cells.

Results: We characterize expression of the two C. teleta orthologs of piwi, genes with roles in germline development in diverse organisms. Ct-piwi1 and Ct-piwi2 are expressed throughout the life cycle in a dynamic pattern that includes both somatic and germline cells, and show nearly identical expression patterns at all stages examined. Both genes are broadly expressed during embryonic and larval development, gradually becoming restricted to putative primordial germ cells (PGCs) and the posterior growth zone. In juveniles, Ct-piwi1 is expressed in the presumptive gonads, and in reproductive adults, it is detected in gonads and the posterior growth zone. In addition, Ct-piwi1 is expressed in a population of putative PGCs that persist in sexually mature adults, likely in a stem cell niche. Ct-piwi1 is expressed in regenerating tissue, and once segments differentiate, it becomes most prominent in the posterior growth zone and immature oocytes in regenerating ovaries of regenerating segments.

Conclusions: In C. teleta, piwi genes may have retained an ancestral role as genetic regulators of both somatic and germline stem cells. It is likely that piwi genes, and associated stem cell co-regulators, became restricted to the germline in some taxa during the course of evolution.

No MeSH data available.


Related in: MedlinePlus