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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

Diagrams of T. transversa development and distribution of musculature in the competent larva. All images are oriented with anterior to the left. Panels (A-D) and (I) are lateral views. Panels (E, F) and (J) are blastoporal/ventral views. Panels (G, H) are ventral views. (A-H) Diagrammatic views of T. transversa gastrula and larval stages. The mesoderm is shaded red, the endoderm is shaded yellow, and the ectoderm is shaded gray. (A, E) The location of the blastopore in the radial gastrula stage is denoted by an asterisk. (D) Lateral view of the late larval stage. One set of dorsal chaetae (black arrowhead) is shown emerging from the mesodermal chaetal sac in the mantle lobe. (H) Ventral view of the late larval stage. Lateral chaetae (black arrows) are shown emerging from the mesodermal chaetal sacs in the mantle lobe. Dorsal chaetae are behind the plane of the cross section (black arrowheads). (I-K) Expression of Tt.tropomyosin during T. transversa development. (I, J)Tt.tropomyosin is expressed in the anterior and lateral portions of the archenteron wall during late gastrula and early larval stages. (K)Tt.tropomyosin is expressed in the mesoderm of the mantle lobe, including the chaetal sacs (black arrowheads) and the lateral regions of the pedicle lobe (black arrows) during the late larval stage. Scale bars are 50 μm in length. (L, M) Phalloidin staining of filamentous actin in the musculature of the competent larval stage. Images are projections of confocal z-series through half of the larva. (L) Lateral view showing complex musculature in the apical, mantle, and pedicle lobes. The prominent pedicle muscles can be observed the ventral region of the larva (white arrowhead). (M) Ventral view of larval musculature. Bundles of muscles are present in the lateral chaetal sacs of the mantle lobe (open arrowheads). Relatively little staining is detected medially in the pedicle lobe (white arrow) between the paired pedicle muscles (white arrowheads).
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Fig1: Diagrams of T. transversa development and distribution of musculature in the competent larva. All images are oriented with anterior to the left. Panels (A-D) and (I) are lateral views. Panels (E, F) and (J) are blastoporal/ventral views. Panels (G, H) are ventral views. (A-H) Diagrammatic views of T. transversa gastrula and larval stages. The mesoderm is shaded red, the endoderm is shaded yellow, and the ectoderm is shaded gray. (A, E) The location of the blastopore in the radial gastrula stage is denoted by an asterisk. (D) Lateral view of the late larval stage. One set of dorsal chaetae (black arrowhead) is shown emerging from the mesodermal chaetal sac in the mantle lobe. (H) Ventral view of the late larval stage. Lateral chaetae (black arrows) are shown emerging from the mesodermal chaetal sacs in the mantle lobe. Dorsal chaetae are behind the plane of the cross section (black arrowheads). (I-K) Expression of Tt.tropomyosin during T. transversa development. (I, J)Tt.tropomyosin is expressed in the anterior and lateral portions of the archenteron wall during late gastrula and early larval stages. (K)Tt.tropomyosin is expressed in the mesoderm of the mantle lobe, including the chaetal sacs (black arrowheads) and the lateral regions of the pedicle lobe (black arrows) during the late larval stage. Scale bars are 50 μm in length. (L, M) Phalloidin staining of filamentous actin in the musculature of the competent larval stage. Images are projections of confocal z-series through half of the larva. (L) Lateral view showing complex musculature in the apical, mantle, and pedicle lobes. The prominent pedicle muscles can be observed the ventral region of the larva (white arrowhead). (M) Ventral view of larval musculature. Bundles of muscles are present in the lateral chaetal sacs of the mantle lobe (open arrowheads). Relatively little staining is detected medially in the pedicle lobe (white arrow) between the paired pedicle muscles (white arrowheads).

Mentions: Brachiopods develop through a form of radial cleavage, and endomesoderm is formed through invagination of cells at the vegetal pole during gastrulation [34]. Morphological analyses have shown that during early gastrulation, the embryo remains radially symmetrical (Figure 1A,E) and invaginating tissue forming the archenteron extends towards the animal pole [34]. The archenteron consists of two domains, the presumptive endoderm (located on the ‘roof’) and mesoderm located in a ring at the boundary of the ectoderm and endoderm (Figure 1A,E) [33-35]. As gastrulation proceeds, the gastrula becomes asymmetric as the animal and vegetal poles shift positions relative to one another, establishing the anterior-posterior and dorsal-ventral axes (Figure 1B,F). After the blastopore elongates along the ventral side of the embryo, the dorsal surface of the archenteron expands asymmetrically at the boundary of the roof and walls, extending a curtain of cells down towards the ventral side of the embryo [34]. This process generates the mesoderm as a distinct tissue layer, surrounding the endoderm (Figure 1C,G). As the blastopore closes from posterior to anterior, the endoderm seals dorsally to form a sac open to the environment through the remnant of the blastopore anteriorly on the ventral surface of the embryo and closed in a blind ending posteriorly. In the late larval stage, the mesoderm is present in all three main regions of the larva, termed the apical, mantle, and pedicle lobes (Figure 1D,H). Mesodermal differentiation is first indicated by expression of the actin-binding gene Tt.tropomyosin, which is expressed in the anterior and lateral regions of the archenteron wall in the asymmetric gastrula and early larval stages (Figure 1I,J). In the late larval stage, Tt.tropomyosin is expressed in the mesoderm of the mantle lobe, including the chaetal sacs (black arrowheads in Figure 1K), and in the lateral mesoderm of the pedicle lobe (black arrows in Figure 1K). In the final competent larval form, the predominant mesodermal derivative is a complex system of musculature, which includes prominent longitudinal muscles in the pedicle lobe and two pairs of chaetal sacs in the mantle lobe (Figure 1L,M) [36,37].Figure 1


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

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

Diagrams of T. transversa development and distribution of musculature in the competent larva. All images are oriented with anterior to the left. Panels (A-D) and (I) are lateral views. Panels (E, F) and (J) are blastoporal/ventral views. Panels (G, H) are ventral views. (A-H) Diagrammatic views of T. transversa gastrula and larval stages. The mesoderm is shaded red, the endoderm is shaded yellow, and the ectoderm is shaded gray. (A, E) The location of the blastopore in the radial gastrula stage is denoted by an asterisk. (D) Lateral view of the late larval stage. One set of dorsal chaetae (black arrowhead) is shown emerging from the mesodermal chaetal sac in the mantle lobe. (H) Ventral view of the late larval stage. Lateral chaetae (black arrows) are shown emerging from the mesodermal chaetal sacs in the mantle lobe. Dorsal chaetae are behind the plane of the cross section (black arrowheads). (I-K) Expression of Tt.tropomyosin during T. transversa development. (I, J)Tt.tropomyosin is expressed in the anterior and lateral portions of the archenteron wall during late gastrula and early larval stages. (K)Tt.tropomyosin is expressed in the mesoderm of the mantle lobe, including the chaetal sacs (black arrowheads) and the lateral regions of the pedicle lobe (black arrows) during the late larval stage. Scale bars are 50 μm in length. (L, M) Phalloidin staining of filamentous actin in the musculature of the competent larval stage. Images are projections of confocal z-series through half of the larva. (L) Lateral view showing complex musculature in the apical, mantle, and pedicle lobes. The prominent pedicle muscles can be observed the ventral region of the larva (white arrowhead). (M) Ventral view of larval musculature. Bundles of muscles are present in the lateral chaetal sacs of the mantle lobe (open arrowheads). Relatively little staining is detected medially in the pedicle lobe (white arrow) between the paired pedicle muscles (white arrowheads).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Fig1: Diagrams of T. transversa development and distribution of musculature in the competent larva. All images are oriented with anterior to the left. Panels (A-D) and (I) are lateral views. Panels (E, F) and (J) are blastoporal/ventral views. Panels (G, H) are ventral views. (A-H) Diagrammatic views of T. transversa gastrula and larval stages. The mesoderm is shaded red, the endoderm is shaded yellow, and the ectoderm is shaded gray. (A, E) The location of the blastopore in the radial gastrula stage is denoted by an asterisk. (D) Lateral view of the late larval stage. One set of dorsal chaetae (black arrowhead) is shown emerging from the mesodermal chaetal sac in the mantle lobe. (H) Ventral view of the late larval stage. Lateral chaetae (black arrows) are shown emerging from the mesodermal chaetal sacs in the mantle lobe. Dorsal chaetae are behind the plane of the cross section (black arrowheads). (I-K) Expression of Tt.tropomyosin during T. transversa development. (I, J)Tt.tropomyosin is expressed in the anterior and lateral portions of the archenteron wall during late gastrula and early larval stages. (K)Tt.tropomyosin is expressed in the mesoderm of the mantle lobe, including the chaetal sacs (black arrowheads) and the lateral regions of the pedicle lobe (black arrows) during the late larval stage. Scale bars are 50 μm in length. (L, M) Phalloidin staining of filamentous actin in the musculature of the competent larval stage. Images are projections of confocal z-series through half of the larva. (L) Lateral view showing complex musculature in the apical, mantle, and pedicle lobes. The prominent pedicle muscles can be observed the ventral region of the larva (white arrowhead). (M) Ventral view of larval musculature. Bundles of muscles are present in the lateral chaetal sacs of the mantle lobe (open arrowheads). Relatively little staining is detected medially in the pedicle lobe (white arrow) between the paired pedicle muscles (white arrowheads).
Mentions: Brachiopods develop through a form of radial cleavage, and endomesoderm is formed through invagination of cells at the vegetal pole during gastrulation [34]. Morphological analyses have shown that during early gastrulation, the embryo remains radially symmetrical (Figure 1A,E) and invaginating tissue forming the archenteron extends towards the animal pole [34]. The archenteron consists of two domains, the presumptive endoderm (located on the ‘roof’) and mesoderm located in a ring at the boundary of the ectoderm and endoderm (Figure 1A,E) [33-35]. As gastrulation proceeds, the gastrula becomes asymmetric as the animal and vegetal poles shift positions relative to one another, establishing the anterior-posterior and dorsal-ventral axes (Figure 1B,F). After the blastopore elongates along the ventral side of the embryo, the dorsal surface of the archenteron expands asymmetrically at the boundary of the roof and walls, extending a curtain of cells down towards the ventral side of the embryo [34]. This process generates the mesoderm as a distinct tissue layer, surrounding the endoderm (Figure 1C,G). As the blastopore closes from posterior to anterior, the endoderm seals dorsally to form a sac open to the environment through the remnant of the blastopore anteriorly on the ventral surface of the embryo and closed in a blind ending posteriorly. In the late larval stage, the mesoderm is present in all three main regions of the larva, termed the apical, mantle, and pedicle lobes (Figure 1D,H). Mesodermal differentiation is first indicated by expression of the actin-binding gene Tt.tropomyosin, which is expressed in the anterior and lateral regions of the archenteron wall in the asymmetric gastrula and early larval stages (Figure 1I,J). In the late larval stage, Tt.tropomyosin is expressed in the mesoderm of the mantle lobe, including the chaetal sacs (black arrowheads in Figure 1K), and in the lateral mesoderm of the pedicle lobe (black arrows in Figure 1K). In the final competent larval form, the predominant mesodermal derivative is a complex system of musculature, which includes prominent longitudinal muscles in the pedicle lobe and two pairs of chaetal sacs in the mantle lobe (Figure 1L,M) [36,37].Figure 1

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