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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

Expression of Ct-piwi1 in late stage adult regenerates. All animals are female and were amputated at the 12th segment. All panels shown are posterior ends of amputated adults. All panels are oriented in a ventral view with anterior to the left. Abbreviations: io, immature oocytes; pgz, posterior growth zone; po, putative oocytes. Dotted lines indicate the cut site in all panels. Dark shapes in A and C are contents within the lumen of the gut. (A) At 10 days post-amputation, expression is in the posterior growth zone of the regenerating tissue. (B) 14 days post-amputation showing expression in putative oocytes, the posterior growth zone and loosely organized cells within the coelomic cavity (arrows). (C) Expression in 18 days post-amputation is in immature oocytes in regenerating ovaries, putative oocytes, cells within the coelomic cavity (arrows), and the posterior growth zone. Scale bar, 50 μm for all panels.
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Figure 10: Expression of Ct-piwi1 in late stage adult regenerates. All animals are female and were amputated at the 12th segment. All panels shown are posterior ends of amputated adults. All panels are oriented in a ventral view with anterior to the left. Abbreviations: io, immature oocytes; pgz, posterior growth zone; po, putative oocytes. Dotted lines indicate the cut site in all panels. Dark shapes in A and C are contents within the lumen of the gut. (A) At 10 days post-amputation, expression is in the posterior growth zone of the regenerating tissue. (B) 14 days post-amputation showing expression in putative oocytes, the posterior growth zone and loosely organized cells within the coelomic cavity (arrows). (C) Expression in 18 days post-amputation is in immature oocytes in regenerating ovaries, putative oocytes, cells within the coelomic cavity (arrows), and the posterior growth zone. Scale bar, 50 μm for all panels.

Mentions: At later stages of regeneration, Ct-piwi1 expression becomes more restricted. In 10 through 18 days post-amputation, there is a morphologically distinct pygidium and posterior growth zone. During these stages, Ct-piwi1 is consistently expressed in the posterior growth zone of the regenerating tissue (Figure 10A-C), and at 10 days post-amputation, it is the most prominent expression domain. At 14 days post-amputation, segments become apparent externally and additional expression domains appear, including in a loosely organized group of cells anterior to the posterior growth zone in the ventro-lateral region of the coelomic cavity (Figure 10B, arrows). In addition, in the anterior segments of the regenerating animals, there is expression associated with the ventral face of the gut in the mesoderm; this domain corresponds to the position where the ovaries will form. We interpret these piwi-expressing cells to be oogonia. Approximately 20 segments have regenerated by 18 days post-amputation. At this stage, ovaries have begun to form in the anterior segments of the regenerate, and they contain piwi-expressing immature oocytes (Figure 10C). In the middle segments of the regenerate, Ct-piwi1 is expressed in a pattern very similar to that observed in anterior regenerating segments of 10-day post-amputation adults, in putative oogonia. Expression is also evident in loosely organized cells anterior to the posterior growth zone in the coelomic cavity (Figure 10C, arrows). Similar amputations were also performed on adult males, and there were no detectable differences in Ct-piwi1 expression between males and females within the regenerating tissue from zero to ten days post-amputation (not shown). Moreover, between 14 and 18 days post-amputation, both males and females exhibit similar expression in the posterior growth zone and in a population of loosely organized cells anterior of the posterior growth zone. In summary, there are two distinct phases of Ct-piwi1 expression during regeneration: an early phase in a broad domain during blastemal growth, and a later phase of more restricted expression in the posterior growth zone, regenerating ovaries (of females and hermaphrodites), and in a localized population of loosely organized cells in the coelomic cavity.


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)

Expression of Ct-piwi1 in late stage adult regenerates. All animals are female and were amputated at the 12th segment. All panels shown are posterior ends of amputated adults. All panels are oriented in a ventral view with anterior to the left. Abbreviations: io, immature oocytes; pgz, posterior growth zone; po, putative oocytes. Dotted lines indicate the cut site in all panels. Dark shapes in A and C are contents within the lumen of the gut. (A) At 10 days post-amputation, expression is in the posterior growth zone of the regenerating tissue. (B) 14 days post-amputation showing expression in putative oocytes, the posterior growth zone and loosely organized cells within the coelomic cavity (arrows). (C) Expression in 18 days post-amputation is in immature oocytes in regenerating ovaries, putative oocytes, cells within the coelomic cavity (arrows), 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 10: Expression of Ct-piwi1 in late stage adult regenerates. All animals are female and were amputated at the 12th segment. All panels shown are posterior ends of amputated adults. All panels are oriented in a ventral view with anterior to the left. Abbreviations: io, immature oocytes; pgz, posterior growth zone; po, putative oocytes. Dotted lines indicate the cut site in all panels. Dark shapes in A and C are contents within the lumen of the gut. (A) At 10 days post-amputation, expression is in the posterior growth zone of the regenerating tissue. (B) 14 days post-amputation showing expression in putative oocytes, the posterior growth zone and loosely organized cells within the coelomic cavity (arrows). (C) Expression in 18 days post-amputation is in immature oocytes in regenerating ovaries, putative oocytes, cells within the coelomic cavity (arrows), and the posterior growth zone. Scale bar, 50 μm for all panels.
Mentions: At later stages of regeneration, Ct-piwi1 expression becomes more restricted. In 10 through 18 days post-amputation, there is a morphologically distinct pygidium and posterior growth zone. During these stages, Ct-piwi1 is consistently expressed in the posterior growth zone of the regenerating tissue (Figure 10A-C), and at 10 days post-amputation, it is the most prominent expression domain. At 14 days post-amputation, segments become apparent externally and additional expression domains appear, including in a loosely organized group of cells anterior to the posterior growth zone in the ventro-lateral region of the coelomic cavity (Figure 10B, arrows). In addition, in the anterior segments of the regenerating animals, there is expression associated with the ventral face of the gut in the mesoderm; this domain corresponds to the position where the ovaries will form. We interpret these piwi-expressing cells to be oogonia. Approximately 20 segments have regenerated by 18 days post-amputation. At this stage, ovaries have begun to form in the anterior segments of the regenerate, and they contain piwi-expressing immature oocytes (Figure 10C). In the middle segments of the regenerate, Ct-piwi1 is expressed in a pattern very similar to that observed in anterior regenerating segments of 10-day post-amputation adults, in putative oogonia. Expression is also evident in loosely organized cells anterior to the posterior growth zone in the coelomic cavity (Figure 10C, arrows). Similar amputations were also performed on adult males, and there were no detectable differences in Ct-piwi1 expression between males and females within the regenerating tissue from zero to ten days post-amputation (not shown). Moreover, between 14 and 18 days post-amputation, both males and females exhibit similar expression in the posterior growth zone and in a population of loosely organized cells anterior of the posterior growth zone. In summary, there are two distinct phases of Ct-piwi1 expression during regeneration: an early phase in a broad domain during blastemal growth, and a later phase of more restricted expression in the posterior growth zone, regenerating ovaries (of females and hermaphrodites), and in a localized population of loosely organized cells in the coelomic cavity.

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