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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.


Adult expression patterns of Ct-piwi1. All panels are a ventral view with anterior to the left. Abbreviations: gd, genital duct; io, immature oocytes; mo, mature oocytes. Dotted lines in A and B indicate the segment boundaries of the fifth and sixth segments. Black solid lines in A and B indicate the boundary between the thorax and abdomen. (A) Ct-piwi1 expression in the PGCs in the fifth and sixth segments of a male (arrow) and bilaterally symmetrical genital ducts spanning the boundary of the seventh and eighth segment. (B) Adult hermaphrodite with expression in the PGCs in the fifth and sixth segments (arrow). Oocyte expression is visible in the ovaries in the 10th segment. (C) Expression is not detected within abdominal segments of adult males. (D) Enlarged view of female showing expression in immature oocytes of abdominal segments. (E) Close-up view of Ct-piwi1-expressing PGCs (arrows) from panel A. (F) Adult female with Ct-piwi1 expression in immature oocytes located in the medial region of the ovary. Note the lack of expression in the large mature oocytes. (G) Close-up view of expression in immature oocytes within a single abdominal segment. Scale bar, 50 μm for all panels.
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Figure 8: Adult expression patterns of Ct-piwi1. All panels are a ventral view with anterior to the left. Abbreviations: gd, genital duct; io, immature oocytes; mo, mature oocytes. Dotted lines in A and B indicate the segment boundaries of the fifth and sixth segments. Black solid lines in A and B indicate the boundary between the thorax and abdomen. (A) Ct-piwi1 expression in the PGCs in the fifth and sixth segments of a male (arrow) and bilaterally symmetrical genital ducts spanning the boundary of the seventh and eighth segment. (B) Adult hermaphrodite with expression in the PGCs in the fifth and sixth segments (arrow). Oocyte expression is visible in the ovaries in the 10th segment. (C) Expression is not detected within abdominal segments of adult males. (D) Enlarged view of female showing expression in immature oocytes of abdominal segments. (E) Close-up view of Ct-piwi1-expressing PGCs (arrows) from panel A. (F) Adult female with Ct-piwi1 expression in immature oocytes located in the medial region of the ovary. Note the lack of expression in the large mature oocytes. (G) Close-up view of expression in immature oocytes within a single abdominal segment. Scale bar, 50 μm for all panels.

Mentions: Expression of Ct-piwi1 was also examined in reproductive adult worms eight weeks post-metamorphosis. The overall expression pattern in adults is similar to that of two-week post-metamorphic juvenile worms. Within the thoracic region (segments 1 to 9) of males and females, Ct-piwi1 expression persists in the putative PGCs localized to segment 5. This structure has continued to enlarge and at this stage contains over 75 Ct-piwi1-expressing cells, typically extending into segment 6 (Figure 8A, B, E, arrows).


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)

Adult expression patterns of Ct-piwi1. All panels are a ventral view with anterior to the left. Abbreviations: gd, genital duct; io, immature oocytes; mo, mature oocytes. Dotted lines in A and B indicate the segment boundaries of the fifth and sixth segments. Black solid lines in A and B indicate the boundary between the thorax and abdomen. (A) Ct-piwi1 expression in the PGCs in the fifth and sixth segments of a male (arrow) and bilaterally symmetrical genital ducts spanning the boundary of the seventh and eighth segment. (B) Adult hermaphrodite with expression in the PGCs in the fifth and sixth segments (arrow). Oocyte expression is visible in the ovaries in the 10th segment. (C) Expression is not detected within abdominal segments of adult males. (D) Enlarged view of female showing expression in immature oocytes of abdominal segments. (E) Close-up view of Ct-piwi1-expressing PGCs (arrows) from panel A. (F) Adult female with Ct-piwi1 expression in immature oocytes located in the medial region of the ovary. Note the lack of expression in the large mature oocytes. (G) Close-up view of expression in immature oocytes within a single abdominal segment. 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 8: Adult expression patterns of Ct-piwi1. All panels are a ventral view with anterior to the left. Abbreviations: gd, genital duct; io, immature oocytes; mo, mature oocytes. Dotted lines in A and B indicate the segment boundaries of the fifth and sixth segments. Black solid lines in A and B indicate the boundary between the thorax and abdomen. (A) Ct-piwi1 expression in the PGCs in the fifth and sixth segments of a male (arrow) and bilaterally symmetrical genital ducts spanning the boundary of the seventh and eighth segment. (B) Adult hermaphrodite with expression in the PGCs in the fifth and sixth segments (arrow). Oocyte expression is visible in the ovaries in the 10th segment. (C) Expression is not detected within abdominal segments of adult males. (D) Enlarged view of female showing expression in immature oocytes of abdominal segments. (E) Close-up view of Ct-piwi1-expressing PGCs (arrows) from panel A. (F) Adult female with Ct-piwi1 expression in immature oocytes located in the medial region of the ovary. Note the lack of expression in the large mature oocytes. (G) Close-up view of expression in immature oocytes within a single abdominal segment. Scale bar, 50 μm for all panels.
Mentions: Expression of Ct-piwi1 was also examined in reproductive adult worms eight weeks post-metamorphosis. The overall expression pattern in adults is similar to that of two-week post-metamorphic juvenile worms. Within the thoracic region (segments 1 to 9) of males and females, Ct-piwi1 expression persists in the putative PGCs localized to segment 5. This structure has continued to enlarge and at this stage contains over 75 Ct-piwi1-expressing cells, typically extending into segment 6 (Figure 8A, B, E, arrows).

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.