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Mesodermal gene expression during the embryonic and larval development of the articulate brachiopod Terebratalia transversa.

Passamaneck YJ, Hejnol A, Martindale MQ - Evodevo (2015)

Bottom Line: Orthologs of 17 developmental regulatory genes with roles in the development of the mesoderm in other bilaterian animals were found to be expressed in the developing mesoderm of T. transversa.Five genes, Tt.twist, Tt.GATA456, Tt.dachshund, Tt.mPrx, and Tt.NK1, were found to have expression throughout the archenteron wall at the radial gastrula stage, shortly after the initiation of gastrulation.Localized expression domains during gastrulation and larval development evidence early regionalization of the mesoderm and provide a basis for hypotheses regarding the molecular regulation underlying the complex system of musculature observed in the larva.

View Article: PubMed Central - PubMed

Affiliation: Kewalo Marine Laboratory, PBRC, University of Hawaii, 41 Ahui Street, Honolulu, HI 96813 USA ; The Whitney Laboratory for Marine Bioscience, University of Florida, St. Augustine, FL 32080 USA.

ABSTRACT

Background: Brachiopods undergo radial cleavage, which is distinct from the stereotyped development of closely related spiralian taxa. The mesoderm has been inferred to derive from the archenteron walls following gastrulation, and the primary mesoderm derivative in the larva is a complex musculature. To investigate the specification and differentiation of the mesoderm in the articulate brachiopod Terebratalia transversa, we have identified orthologs of genes involved in mesoderm development in other taxa and investigated their spatial and temporal expression during the embryonic and larval development of T. transversa.

Results: Orthologs of 17 developmental regulatory genes with roles in the development of the mesoderm in other bilaterian animals were found to be expressed in the developing mesoderm of T. transversa. Five genes, Tt.twist, Tt.GATA456, Tt.dachshund, Tt.mPrx, and Tt.NK1, were found to have expression throughout the archenteron wall at the radial gastrula stage, shortly after the initiation of gastrulation. Three additional genes, Tt.Pax1/9, Tt.MyoD, and Tt.Six1/2, showed expression at this stage in only a portion of the archenteron wall. Tt.eya, Tt.FoxC, Tt.FoxF, Tt.Mox, Tt.paraxis, Tt.Limpet, and Tt.Mef2 all showed initial mesodermal expression during later gastrula or early larval stages. At the late larval stage, Tt.dachshund, Tt.Limpet, and Tt.Mef2 showed expression in nearly all mesoderm cells, while all other genes were localized to specific regions of the mesoderm. Tt.FoxD and Tt.noggin both showed expression in the ventral mesoderm at the larval stages, with gastrula expression patterns in the archenteron roof and blastopore lip, respectively.

Conclusions: Expression analyses support conserved roles for developmental regulators in the specification and differentiation of the mesoderm during the development of T. transversa. Expression of multiple mesodermal factors in the archenteron wall during gastrulation supports previous morphological observations that this region gives rise to larval mesoderm. Localized expression domains during gastrulation and larval development evidence early regionalization of the mesoderm and provide a basis for hypotheses regarding the molecular regulation underlying the complex system of musculature observed in the larva.

No MeSH data available.


Related in: MedlinePlus

Expression patterns of Tt.Limpet and Tt.Mef2. All images are oriented with anterior to the left. Panels (A-D) and (I-L) are lateral views. Panels (E, F) and (M, N) are blastoporal views. Panels (G, H) and (O, P) are ventral views. For detailed descriptions of expression patterns, see text. (A-H)Tt.Limpet is expressed in the apical ectoderm at the gastrula stages. Mesodermal expression is first observed in the early larva in irregular bands in the developing apical and mantle lobes. In the late larva, strong expression is observed in all but the most posterior region of the mesoderm. (I-P) Weak expression of Tt.Mef2 is observed in the apical ectoderm at the late gastrula stage. In the early larva, a strong continuous band of mesodermal expression flanks the anterior portion of the endoderm and extends laterally into the developing mantle lobe. In the late larva, strong expression is observed flanking the endoderm in the apical lobe and extending into the mantle lobe, including the chaetal sacs. Expression to Tt.Mef2 is also observed in the pedicle lobe mesoderm.
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Fig8: Expression patterns of Tt.Limpet and Tt.Mef2. All images are oriented with anterior to the left. Panels (A-D) and (I-L) are lateral views. Panels (E, F) and (M, N) are blastoporal views. Panels (G, H) and (O, P) are ventral views. For detailed descriptions of expression patterns, see text. (A-H)Tt.Limpet is expressed in the apical ectoderm at the gastrula stages. Mesodermal expression is first observed in the early larva in irregular bands in the developing apical and mantle lobes. In the late larva, strong expression is observed in all but the most posterior region of the mesoderm. (I-P) Weak expression of Tt.Mef2 is observed in the apical ectoderm at the late gastrula stage. In the early larva, a strong continuous band of mesodermal expression flanks the anterior portion of the endoderm and extends laterally into the developing mantle lobe. In the late larva, strong expression is observed flanking the endoderm in the apical lobe and extending into the mantle lobe, including the chaetal sacs. Expression to Tt.Mef2 is also observed in the pedicle lobe mesoderm.

Mentions: Mesodermal expression was observed for all 17 genes listed above, and representative photomicrographs of the radial gastrula, asymmetric gastrula, early larval, and late larval stages are presented (FiguresĀ 2, 3, 4, 5, 6, 7, 8, and 9). Photomicrographs and descriptions of gene expression patterns are organized in order of the earliest developmental stage when mesodermal expression was detected for each gene. Two other genes with conserved mesodermal expression in other bilaterian taxa, NK3/bagpipe and NK4/tinman, were investigated but were not found to have mesodermal expression in the embryonic stages evaluated here (data not shown).Figure 2


Mesodermal gene expression during the embryonic and larval development of the articulate brachiopod Terebratalia transversa.

Passamaneck YJ, Hejnol A, Martindale MQ - Evodevo (2015)

Expression patterns of Tt.Limpet and Tt.Mef2. All images are oriented with anterior to the left. Panels (A-D) and (I-L) are lateral views. Panels (E, F) and (M, N) are blastoporal views. Panels (G, H) and (O, P) are ventral views. For detailed descriptions of expression patterns, see text. (A-H)Tt.Limpet is expressed in the apical ectoderm at the gastrula stages. Mesodermal expression is first observed in the early larva in irregular bands in the developing apical and mantle lobes. In the late larva, strong expression is observed in all but the most posterior region of the mesoderm. (I-P) Weak expression of Tt.Mef2 is observed in the apical ectoderm at the late gastrula stage. In the early larva, a strong continuous band of mesodermal expression flanks the anterior portion of the endoderm and extends laterally into the developing mantle lobe. In the late larva, strong expression is observed flanking the endoderm in the apical lobe and extending into the mantle lobe, including the chaetal sacs. Expression to Tt.Mef2 is also observed in the pedicle lobe mesoderm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4404124&req=5

Fig8: Expression patterns of Tt.Limpet and Tt.Mef2. All images are oriented with anterior to the left. Panels (A-D) and (I-L) are lateral views. Panels (E, F) and (M, N) are blastoporal views. Panels (G, H) and (O, P) are ventral views. For detailed descriptions of expression patterns, see text. (A-H)Tt.Limpet is expressed in the apical ectoderm at the gastrula stages. Mesodermal expression is first observed in the early larva in irregular bands in the developing apical and mantle lobes. In the late larva, strong expression is observed in all but the most posterior region of the mesoderm. (I-P) Weak expression of Tt.Mef2 is observed in the apical ectoderm at the late gastrula stage. In the early larva, a strong continuous band of mesodermal expression flanks the anterior portion of the endoderm and extends laterally into the developing mantle lobe. In the late larva, strong expression is observed flanking the endoderm in the apical lobe and extending into the mantle lobe, including the chaetal sacs. Expression to Tt.Mef2 is also observed in the pedicle lobe mesoderm.
Mentions: Mesodermal expression was observed for all 17 genes listed above, and representative photomicrographs of the radial gastrula, asymmetric gastrula, early larval, and late larval stages are presented (FiguresĀ 2, 3, 4, 5, 6, 7, 8, and 9). Photomicrographs and descriptions of gene expression patterns are organized in order of the earliest developmental stage when mesodermal expression was detected for each gene. Two other genes with conserved mesodermal expression in other bilaterian taxa, NK3/bagpipe and NK4/tinman, were investigated but were not found to have mesodermal expression in the embryonic stages evaluated here (data not shown).Figure 2

Bottom Line: Orthologs of 17 developmental regulatory genes with roles in the development of the mesoderm in other bilaterian animals were found to be expressed in the developing mesoderm of T. transversa.Five genes, Tt.twist, Tt.GATA456, Tt.dachshund, Tt.mPrx, and Tt.NK1, were found to have expression throughout the archenteron wall at the radial gastrula stage, shortly after the initiation of gastrulation.Localized expression domains during gastrulation and larval development evidence early regionalization of the mesoderm and provide a basis for hypotheses regarding the molecular regulation underlying the complex system of musculature observed in the larva.

View Article: PubMed Central - PubMed

Affiliation: Kewalo Marine Laboratory, PBRC, University of Hawaii, 41 Ahui Street, Honolulu, HI 96813 USA ; The Whitney Laboratory for Marine Bioscience, University of Florida, St. Augustine, FL 32080 USA.

ABSTRACT

Background: Brachiopods undergo radial cleavage, which is distinct from the stereotyped development of closely related spiralian taxa. The mesoderm has been inferred to derive from the archenteron walls following gastrulation, and the primary mesoderm derivative in the larva is a complex musculature. To investigate the specification and differentiation of the mesoderm in the articulate brachiopod Terebratalia transversa, we have identified orthologs of genes involved in mesoderm development in other taxa and investigated their spatial and temporal expression during the embryonic and larval development of T. transversa.

Results: Orthologs of 17 developmental regulatory genes with roles in the development of the mesoderm in other bilaterian animals were found to be expressed in the developing mesoderm of T. transversa. Five genes, Tt.twist, Tt.GATA456, Tt.dachshund, Tt.mPrx, and Tt.NK1, were found to have expression throughout the archenteron wall at the radial gastrula stage, shortly after the initiation of gastrulation. Three additional genes, Tt.Pax1/9, Tt.MyoD, and Tt.Six1/2, showed expression at this stage in only a portion of the archenteron wall. Tt.eya, Tt.FoxC, Tt.FoxF, Tt.Mox, Tt.paraxis, Tt.Limpet, and Tt.Mef2 all showed initial mesodermal expression during later gastrula or early larval stages. At the late larval stage, Tt.dachshund, Tt.Limpet, and Tt.Mef2 showed expression in nearly all mesoderm cells, while all other genes were localized to specific regions of the mesoderm. Tt.FoxD and Tt.noggin both showed expression in the ventral mesoderm at the larval stages, with gastrula expression patterns in the archenteron roof and blastopore lip, respectively.

Conclusions: Expression analyses support conserved roles for developmental regulators in the specification and differentiation of the mesoderm during the development of T. transversa. Expression of multiple mesodermal factors in the archenteron wall during gastrulation supports previous morphological observations that this region gives rise to larval mesoderm. Localized expression domains during gastrulation and larval development evidence early regionalization of the mesoderm and provide a basis for hypotheses regarding the molecular regulation underlying the complex system of musculature observed in the larva.

No MeSH data available.


Related in: MedlinePlus