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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

Ct-piwi1 expression patterns in two-week post-metamorphic juveniles. All panels are ventral views with anterior to the left. Abbreviations: mgp, male gamete precursor; io, immature oocytes; pgz, posterior growth zone; fgp, female germline precursors. 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 thoracic abdominal boundary. (A) In a male juvenile, Ct-piwi1 expression is in the PGCs in the fifth and sixth segments (arrow), and in bilaterally symmetrical male gamete precursors at the boundaries of the seventh and eighth segment and eighth and ninth segment. (B) In a female juvenile, expression is in the PGCs (arrow) and immature oocytes in the ovaries, which begin at the 10th segment (the first abdominal segment). (C) Male juvenile displaying lack of expression in abdominal segments. (D) Female juvenile showing Ct-piwi1 expression in immature oocytes in abdominal segments. (E) Expression in the posterior growth zone of a male juvenile. (F) In a female juvenile, expression is in female germline precursors and the posterior growth zone. Scale bar, 50 μm for all panels.
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Figure 7: Ct-piwi1 expression patterns in two-week post-metamorphic juveniles. All panels are ventral views with anterior to the left. Abbreviations: mgp, male gamete precursor; io, immature oocytes; pgz, posterior growth zone; fgp, female germline precursors. 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 thoracic abdominal boundary. (A) In a male juvenile, Ct-piwi1 expression is in the PGCs in the fifth and sixth segments (arrow), and in bilaterally symmetrical male gamete precursors at the boundaries of the seventh and eighth segment and eighth and ninth segment. (B) In a female juvenile, expression is in the PGCs (arrow) and immature oocytes in the ovaries, which begin at the 10th segment (the first abdominal segment). (C) Male juvenile displaying lack of expression in abdominal segments. (D) Female juvenile showing Ct-piwi1 expression in immature oocytes in abdominal segments. (E) Expression in the posterior growth zone of a male juvenile. (F) In a female juvenile, expression is in female germline precursors and the posterior growth zone. Scale bar, 50 μm for all panels.

Mentions: In two-week post-metamorphic juvenile worms, Ct-piwi1 expression domains are similar to those observed in one week post-metamorphic juvenile worms. The appearance of ovaries within the females is the biggest difference between the two stages. The ovaries appear as paired ventral structures adjacent to the lateral edges of the intestine, and at this stage primarily contain previtellogenic oocytes. The most anterior segment that contains ovaries is the 10th segment (Figure 7B), posterior to the thoracic region, and at this stage the ovaries span many segments. Ct-piwi1 is expressed in immature oocytes within the ovaries of females (Figure 7B, D), and is not detected within mid-body abdominal segments of males (Figure 7C). In males, Ct-piwi1-expressing cells are present in two pairs of ventro-lateral cell clusters positioned at the boundaries between segments 7 and 8 and segments 8 and 9 (Figure 7A). The structure containing the putative PGCs is larger in area and more elongated compared to the structure in one-week post-metamorphic juveniles, and now contains approximately 50 cells, within segments 5 to 6 (Figure 7A, B, arrows). The posterior growth zone of males and females maintains strong Ct-piwi1 expression, which is most prominent in the mesoderm (Figure 7E, F). Anterior to the posterior growth zone in females, there are segmentally repeated, paired ventral cell clusters between the ventral nerve cord and gut that express Ct-piwi1 (Figure 7F). These clusters are positioned along the anterior face of the septa at the segmental boundary. We hypothesize that these cell clusters are female germline precursors that will colonize the future ovaries once these segments mature and ovaries form within them. In approximately one-third to one-half of the two-week juveniles (n = 13/30), we also observed Ct-piwi1 expression in cells scattered in the trunk within the coelomic cavity (not shown). These cells have a large nuclear to cytoplasmic ratio, lack obvious signs of morphological differentiation, and their position is highly variable within the coelomic cavity among individuals. We rarely saw these cells in one-week juveniles and reproductive adults.


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)

Ct-piwi1 expression patterns in two-week post-metamorphic juveniles. All panels are ventral views with anterior to the left. Abbreviations: mgp, male gamete precursor; io, immature oocytes; pgz, posterior growth zone; fgp, female germline precursors. 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 thoracic abdominal boundary. (A) In a male juvenile, Ct-piwi1 expression is in the PGCs in the fifth and sixth segments (arrow), and in bilaterally symmetrical male gamete precursors at the boundaries of the seventh and eighth segment and eighth and ninth segment. (B) In a female juvenile, expression is in the PGCs (arrow) and immature oocytes in the ovaries, which begin at the 10th segment (the first abdominal segment). (C) Male juvenile displaying lack of expression in abdominal segments. (D) Female juvenile showing Ct-piwi1 expression in immature oocytes in abdominal segments. (E) Expression in the posterior growth zone of a male juvenile. (F) In a female juvenile, expression is in female germline precursors and the posterior growth zone. 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 7: Ct-piwi1 expression patterns in two-week post-metamorphic juveniles. All panels are ventral views with anterior to the left. Abbreviations: mgp, male gamete precursor; io, immature oocytes; pgz, posterior growth zone; fgp, female germline precursors. 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 thoracic abdominal boundary. (A) In a male juvenile, Ct-piwi1 expression is in the PGCs in the fifth and sixth segments (arrow), and in bilaterally symmetrical male gamete precursors at the boundaries of the seventh and eighth segment and eighth and ninth segment. (B) In a female juvenile, expression is in the PGCs (arrow) and immature oocytes in the ovaries, which begin at the 10th segment (the first abdominal segment). (C) Male juvenile displaying lack of expression in abdominal segments. (D) Female juvenile showing Ct-piwi1 expression in immature oocytes in abdominal segments. (E) Expression in the posterior growth zone of a male juvenile. (F) In a female juvenile, expression is in female germline precursors and the posterior growth zone. Scale bar, 50 μm for all panels.
Mentions: In two-week post-metamorphic juvenile worms, Ct-piwi1 expression domains are similar to those observed in one week post-metamorphic juvenile worms. The appearance of ovaries within the females is the biggest difference between the two stages. The ovaries appear as paired ventral structures adjacent to the lateral edges of the intestine, and at this stage primarily contain previtellogenic oocytes. The most anterior segment that contains ovaries is the 10th segment (Figure 7B), posterior to the thoracic region, and at this stage the ovaries span many segments. Ct-piwi1 is expressed in immature oocytes within the ovaries of females (Figure 7B, D), and is not detected within mid-body abdominal segments of males (Figure 7C). In males, Ct-piwi1-expressing cells are present in two pairs of ventro-lateral cell clusters positioned at the boundaries between segments 7 and 8 and segments 8 and 9 (Figure 7A). The structure containing the putative PGCs is larger in area and more elongated compared to the structure in one-week post-metamorphic juveniles, and now contains approximately 50 cells, within segments 5 to 6 (Figure 7A, B, arrows). The posterior growth zone of males and females maintains strong Ct-piwi1 expression, which is most prominent in the mesoderm (Figure 7E, F). Anterior to the posterior growth zone in females, there are segmentally repeated, paired ventral cell clusters between the ventral nerve cord and gut that express Ct-piwi1 (Figure 7F). These clusters are positioned along the anterior face of the septa at the segmental boundary. We hypothesize that these cell clusters are female germline precursors that will colonize the future ovaries once these segments mature and ovaries form within them. In approximately one-third to one-half of the two-week juveniles (n = 13/30), we also observed Ct-piwi1 expression in cells scattered in the trunk within the coelomic cavity (not shown). These cells have a large nuclear to cytoplasmic ratio, lack obvious signs of morphological differentiation, and their position is highly variable within the coelomic cavity among individuals. We rarely saw these cells in one-week juveniles and reproductive adults.

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