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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 during embryonic and larval development. Except for cleavage stages (A-D), all animals are ventral views with anterior to the left. N is a lateral view with ventral down and anterior to the left. Stages shown are indicated in the lower-right of each panel. At the top is a developmental staging chart for C. teleta. Abbreviations: br, brain; end, endoderm; fg, foregut; hg, hindgut; mb, mesodermal bands; pgz; posterior growth zone; vnc, ventral nerve cord. (A) Expression in the cytoplasm of uncleaved zygote (arrow). (B) Expression is in both cells of a 2-cell stage embryo (arrows). (C) Animal view of a four-cell stage embryo showing expression in every cell (arrows). (D) Expression throughout the embryo (arrows). (E) Endodermal expression in a stage 3 larva. (F) Expression in the brain, foregut, and mesodermal bands. (G) Ct-piwi1 is expressed in two cell clusters on the ventral side of the trunk (black arrows), and in the brain, foregut, and mesodermal bands. (H) Expression in the brain, foregut, mesodermal bands, posterior growth zone and in two asymmetrically positioned ventro-lateral cell clusters (arrows). The left cluster is more anterior. (I) Two asymmetrically positioned ventro-lateral cell clusters with the right cluster more anterior. (J) Two bilaterally symmetric ventro-lateral cell clusters. (K) The two Ct-piwi-expressing cell clusters are located close to the midline (arrows). Expression persists in the foregut and posterior growth zone. (L) The two Ct-piwi1-expressing cell clusters are in close proximity near the ventral midline (arrows). Expression persists in the foregut and posterior growth zone. (M) By stage 9, expression is limited to a single cluster at the ventral midline (arrow) and posterior growth zone. (N) Lateral view showing expression in a single cluster in between the gut and ventral nerve cord at the foregut/hindgut boundary. Scale bar, 50 μm for all panels.
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Figure 3: Ct-piwi1 expression patterns during embryonic and larval development. Except for cleavage stages (A-D), all animals are ventral views with anterior to the left. N is a lateral view with ventral down and anterior to the left. Stages shown are indicated in the lower-right of each panel. At the top is a developmental staging chart for C. teleta. Abbreviations: br, brain; end, endoderm; fg, foregut; hg, hindgut; mb, mesodermal bands; pgz; posterior growth zone; vnc, ventral nerve cord. (A) Expression in the cytoplasm of uncleaved zygote (arrow). (B) Expression is in both cells of a 2-cell stage embryo (arrows). (C) Animal view of a four-cell stage embryo showing expression in every cell (arrows). (D) Expression throughout the embryo (arrows). (E) Endodermal expression in a stage 3 larva. (F) Expression in the brain, foregut, and mesodermal bands. (G) Ct-piwi1 is expressed in two cell clusters on the ventral side of the trunk (black arrows), and in the brain, foregut, and mesodermal bands. (H) Expression in the brain, foregut, mesodermal bands, posterior growth zone and in two asymmetrically positioned ventro-lateral cell clusters (arrows). The left cluster is more anterior. (I) Two asymmetrically positioned ventro-lateral cell clusters with the right cluster more anterior. (J) Two bilaterally symmetric ventro-lateral cell clusters. (K) The two Ct-piwi-expressing cell clusters are located close to the midline (arrows). Expression persists in the foregut and posterior growth zone. (L) The two Ct-piwi1-expressing cell clusters are in close proximity near the ventral midline (arrows). Expression persists in the foregut and posterior growth zone. (M) By stage 9, expression is limited to a single cluster at the ventral midline (arrow) and posterior growth zone. (N) Lateral view showing expression in a single cluster in between the gut and ventral nerve cord at the foregut/hindgut boundary. Scale bar, 50 μm for all panels.

Mentions: We characterized expression of the two C. teleta piwi genes during embryonic and larval development by whole mount in situ hybridization. C. teleta development has been previously described and follows an established staging system (Figure 3, top) [27]. In uncleaved zygotes, two-cell and four-cell stage embryos, Ct-piwi1 transcripts can only be detected after an extended color reaction (Figure 3A-C, arrows). In subsequent cleavage stages, Ct-piwi1 is broadly expressed in most if not all cells (Figure 3D, arrows). Gastrulation occurs during stage 3, and at this stage the Ct-piwi1 expression pattern becomes more restricted within the embryo. Near the end of gastrulation and following closure of the blastopore, Ct-piwi1 is transiently expressed in the endoderm (Figure 3E). In early stage larvae (stage 4), Ct-piwi1 is expressed in several discrete domains including the presumptive brain, foregut, and mesodermal bands (Figure 3F). These expression domains persist into stage 5, and in addition, two small ventro-lateral clusters of cells appear in the mid-body segments. These clusters are medial to the mesodermal bands (Figure 3G, arrows), and become more easily detected at later larval stages. At stage 6, brain expression weakens, while expression becomes more apparent in the foregut, trunk mesoderm, and a band of Ct-piwi1-expressing cells immediately anterior to the telotroch that corresponds to the posterior growth zone (Figure 3H). In addition, expression in the two ventro-lateral cell clusters becomes more prominent; each cluster contains two to five cells and is positioned within the mesoderm (Figure 3H, arrows). There is variation in the position of the ventro-lateral cell clusters within segments 4 and 5 in stage 6 larvae, and three distinct patterns are observed: (1) asymmetrically positioned clusters with the left cluster more anterior (n = 14/35) (Figure 3H, arrows), (2) asymmetrically positioned clusters with the right cluster more anterior (n = 11/35) (Figure 3I, arrows), and (3) bilaterally symmetric cell clusters (n = 10/35) (Figure 3J, arrows). By stages 7 and 8, expression is limited to the foregut, posterior growth zone, and ventro-lateral cell clusters (Figure 3K and Figure 3L, arrows). At these stages, the position of the ventro-lateral cell clusters is closer to the ventral midline relative to their position at stage 6. The position of the Ct-piwi1 positive ventro-lateral clusters also varies among stage 8 larvae, with the following observed patterns: (1) bilaterally symmetric clusters at the midline (n = 15/35), (2) bilaterally symmetric clusters lateral to the midline (n = 11/35), (3) asymmetrically positioned clusters lateral to the midline, with one of the clusters more anterior to the other (n = 9/35) (Figure 3L, arrows). By stage 9, only a single cluster at the ventral midline of segment 4 is apparent (Figure 3M, arrows). This cluster is positioned dorsal to the ventral nerve cord and ventral to the gut tube, at the boundary between the foregut and midgut (Figure 3N). From stage 6 to stage 9, the position of these Ct-piwi1-expressing cells changes from paired ventro-lateral clusters (n = 35/35) to a single cluster at the ventral midline (n = 30/32). The observed variation in the position of the ventro-lateral cell clusters of Ct-piwi1-expressing cells and their progression to the ventral midline is consistent with migratory behavior of these cells. There is no obvious increase in the number of cells in these clusters between stage 6 and stage 9. We hypothesize that these cells are PGCs. By stage 9, Ct-piwi1 expression is restricted to the posterior growth zone and a single cluster of putative PGCs at the ventral midline.


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 during embryonic and larval development. Except for cleavage stages (A-D), all animals are ventral views with anterior to the left. N is a lateral view with ventral down and anterior to the left. Stages shown are indicated in the lower-right of each panel. At the top is a developmental staging chart for C. teleta. Abbreviations: br, brain; end, endoderm; fg, foregut; hg, hindgut; mb, mesodermal bands; pgz; posterior growth zone; vnc, ventral nerve cord. (A) Expression in the cytoplasm of uncleaved zygote (arrow). (B) Expression is in both cells of a 2-cell stage embryo (arrows). (C) Animal view of a four-cell stage embryo showing expression in every cell (arrows). (D) Expression throughout the embryo (arrows). (E) Endodermal expression in a stage 3 larva. (F) Expression in the brain, foregut, and mesodermal bands. (G) Ct-piwi1 is expressed in two cell clusters on the ventral side of the trunk (black arrows), and in the brain, foregut, and mesodermal bands. (H) Expression in the brain, foregut, mesodermal bands, posterior growth zone and in two asymmetrically positioned ventro-lateral cell clusters (arrows). The left cluster is more anterior. (I) Two asymmetrically positioned ventro-lateral cell clusters with the right cluster more anterior. (J) Two bilaterally symmetric ventro-lateral cell clusters. (K) The two Ct-piwi-expressing cell clusters are located close to the midline (arrows). Expression persists in the foregut and posterior growth zone. (L) The two Ct-piwi1-expressing cell clusters are in close proximity near the ventral midline (arrows). Expression persists in the foregut and posterior growth zone. (M) By stage 9, expression is limited to a single cluster at the ventral midline (arrow) and posterior growth zone. (N) Lateral view showing expression in a single cluster in between the gut and ventral nerve cord at the foregut/hindgut boundary. Scale bar, 50 μm for all panels.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
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Figure 3: Ct-piwi1 expression patterns during embryonic and larval development. Except for cleavage stages (A-D), all animals are ventral views with anterior to the left. N is a lateral view with ventral down and anterior to the left. Stages shown are indicated in the lower-right of each panel. At the top is a developmental staging chart for C. teleta. Abbreviations: br, brain; end, endoderm; fg, foregut; hg, hindgut; mb, mesodermal bands; pgz; posterior growth zone; vnc, ventral nerve cord. (A) Expression in the cytoplasm of uncleaved zygote (arrow). (B) Expression is in both cells of a 2-cell stage embryo (arrows). (C) Animal view of a four-cell stage embryo showing expression in every cell (arrows). (D) Expression throughout the embryo (arrows). (E) Endodermal expression in a stage 3 larva. (F) Expression in the brain, foregut, and mesodermal bands. (G) Ct-piwi1 is expressed in two cell clusters on the ventral side of the trunk (black arrows), and in the brain, foregut, and mesodermal bands. (H) Expression in the brain, foregut, mesodermal bands, posterior growth zone and in two asymmetrically positioned ventro-lateral cell clusters (arrows). The left cluster is more anterior. (I) Two asymmetrically positioned ventro-lateral cell clusters with the right cluster more anterior. (J) Two bilaterally symmetric ventro-lateral cell clusters. (K) The two Ct-piwi-expressing cell clusters are located close to the midline (arrows). Expression persists in the foregut and posterior growth zone. (L) The two Ct-piwi1-expressing cell clusters are in close proximity near the ventral midline (arrows). Expression persists in the foregut and posterior growth zone. (M) By stage 9, expression is limited to a single cluster at the ventral midline (arrow) and posterior growth zone. (N) Lateral view showing expression in a single cluster in between the gut and ventral nerve cord at the foregut/hindgut boundary. Scale bar, 50 μm for all panels.
Mentions: We characterized expression of the two C. teleta piwi genes during embryonic and larval development by whole mount in situ hybridization. C. teleta development has been previously described and follows an established staging system (Figure 3, top) [27]. In uncleaved zygotes, two-cell and four-cell stage embryos, Ct-piwi1 transcripts can only be detected after an extended color reaction (Figure 3A-C, arrows). In subsequent cleavage stages, Ct-piwi1 is broadly expressed in most if not all cells (Figure 3D, arrows). Gastrulation occurs during stage 3, and at this stage the Ct-piwi1 expression pattern becomes more restricted within the embryo. Near the end of gastrulation and following closure of the blastopore, Ct-piwi1 is transiently expressed in the endoderm (Figure 3E). In early stage larvae (stage 4), Ct-piwi1 is expressed in several discrete domains including the presumptive brain, foregut, and mesodermal bands (Figure 3F). These expression domains persist into stage 5, and in addition, two small ventro-lateral clusters of cells appear in the mid-body segments. These clusters are medial to the mesodermal bands (Figure 3G, arrows), and become more easily detected at later larval stages. At stage 6, brain expression weakens, while expression becomes more apparent in the foregut, trunk mesoderm, and a band of Ct-piwi1-expressing cells immediately anterior to the telotroch that corresponds to the posterior growth zone (Figure 3H). In addition, expression in the two ventro-lateral cell clusters becomes more prominent; each cluster contains two to five cells and is positioned within the mesoderm (Figure 3H, arrows). There is variation in the position of the ventro-lateral cell clusters within segments 4 and 5 in stage 6 larvae, and three distinct patterns are observed: (1) asymmetrically positioned clusters with the left cluster more anterior (n = 14/35) (Figure 3H, arrows), (2) asymmetrically positioned clusters with the right cluster more anterior (n = 11/35) (Figure 3I, arrows), and (3) bilaterally symmetric cell clusters (n = 10/35) (Figure 3J, arrows). By stages 7 and 8, expression is limited to the foregut, posterior growth zone, and ventro-lateral cell clusters (Figure 3K and Figure 3L, arrows). At these stages, the position of the ventro-lateral cell clusters is closer to the ventral midline relative to their position at stage 6. The position of the Ct-piwi1 positive ventro-lateral clusters also varies among stage 8 larvae, with the following observed patterns: (1) bilaterally symmetric clusters at the midline (n = 15/35), (2) bilaterally symmetric clusters lateral to the midline (n = 11/35), (3) asymmetrically positioned clusters lateral to the midline, with one of the clusters more anterior to the other (n = 9/35) (Figure 3L, arrows). By stage 9, only a single cluster at the ventral midline of segment 4 is apparent (Figure 3M, arrows). This cluster is positioned dorsal to the ventral nerve cord and ventral to the gut tube, at the boundary between the foregut and midgut (Figure 3N). From stage 6 to stage 9, the position of these Ct-piwi1-expressing cells changes from paired ventro-lateral clusters (n = 35/35) to a single cluster at the ventral midline (n = 30/32). The observed variation in the position of the ventro-lateral cell clusters of Ct-piwi1-expressing cells and their progression to the ventral midline is consistent with migratory behavior of these cells. There is no obvious increase in the number of cells in these clusters between stage 6 and stage 9. We hypothesize that these cells are PGCs. By stage 9, Ct-piwi1 expression is restricted to the posterior growth zone and a single cluster of putative PGCs at the ventral midline.

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