Limits...
Development and organization of the larval nervous system in Phoronopsis harmeri: new insights into phoronid phylogeny.

Temereva EN, Tsitrin EB - Front. Zool. (2014)

Bottom Line: Phoronid larvae demonstrate some "deuterostome-like" features, which are, in fact, have to be ancestral bilaterian characters.Our new results and previous data indicate that phoronids have retained some plesiomorphic features, which were inherited from the last common ancestor of all Bilateria.It follows that phoronids should be extracted from the Trochozoan (=Spiralia) clade and placed at the base of the Lophotrochozoan stem.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Invertebrate Zoology, Biological faculty, Moscow State University, Moscow 119992, Russia. temereva@mail.ru.

ABSTRACT

Background: The organization and development of the nervous system has traditionally been used as an important character for establishing the relationships among large groups of animals. According to this criterion, phoronids were initially regarded as deuterostomian but have more recently been regarded as protostomian. The resolving of this conflict requires detailed information from poorly investigated members of phoronids, such as Phoronopsis harmeri.

Results: The serotonin-like immunoreactive part of the P. harmeri nervous system changes during larval development. These changes mostly concern the nervous system of the hood and correlate with the appearance of the median and two marginal neurite bundles, the frontal organ, and the sensory field. The apical organ has bilateral symmetry. The tentacular neurite bundle passes under the tentacles, contains several types of perikarya, and gives rise to intertentacular bundles, which branch in the tentacle base and penetrate into adjacent tentacles by two lateroabfrontal bundles. There are two groups of dorsolateral perikarya, which exhibit serotonin-like immunoreactivity, contact the tentacular neurite bundle, and are located near the youngest tentacles. Larvae have a minor nerve ring, which originates from the posterior marginal neurite bundle of the hood, passes above the tentacle base, and gives rise to the mediofrontal neurite bundle in each tentacle. Paired laterofrontal neurite bundles of tentacles form a continuous nerve tract that conducts to the postoral ciliated band.

Discussion: The organization of the nervous system differs among the planktotrophic larvae of phoronid species. These differences may correlate with differences in phoronid biology. Data concerning the innervation of tentacles in different phoronid larvae are conflicting and require careful reinvestigation. The overall organization of the nervous system in phoronid larvae has more in common with the deuterostomian than with the protostomian nervous system. Phoronid larvae demonstrate some "deuterostome-like" features, which are, in fact, have to be ancestral bilaterian characters. Our new results and previous data indicate that phoronids have retained some plesiomorphic features, which were inherited from the last common ancestor of all Bilateria. It follows that phoronids should be extracted from the Trochozoan (=Spiralia) clade and placed at the base of the Lophotrochozoan stem.

No MeSH data available.


Related in: MedlinePlus

Details of organization of the apical organ in competent larvae of Phoronopsis harmeri. (A) Semi-thin parasagittal section of the apical organ. The locations of different types of perikarya are shown. The apical side is at the top; the hood edge is to the right; the dorsal side of the larva is to the left. A portion of the median neurite bundle is visible on the right. (B) Ultrastructural organization of a portion of the apical organ. Two types of perikarya and the neuropil (np) are visible. (C) Ultrastructural details of type 1 perikarya (p1), which have long microvilli (open arrowheads) around the cilium, a root apparatus, large and abundant mitochondria (m), and clear (electron light) synaptic vesicles (cv). (D) Ultrastructural details of a type 2 perikaryon (p2), which contains a dense-core (dc), clear (cv) vesicles, and rudiments of a cilium (highlighted by a circle). (E) Type 3 perikarya (p3) contain a nucleus (n) with a large nucleolus (nu), a large Golgi apparatus (G), and dense-core vesicles (dc). (F) The central portion of the neuropil contacts the basal lamina (bl). Neurites contain numerous synaptic vesicles (closed arrowheads) spread along the thickened membrane. The basal membranes of muscle cells (mc) are also thickened. Abbreviations: bc – blastocoel; bl – basal lamina; c1 – preoral coelom; cc – cells of coelomic lining; cv – clear synaptic vesicles; dc – dense-core vesicles; G – Golgi apparatus; hr – horizontal rootlet; m – mitochondria; mc – muscle cells; mn – median neurite bundle; n – nucleus; np – neuropil; nu – nucleolus; p1 – perikarya of 1 type; p2 – perikarya of 2 type; p3 – perikarya of 3 type; vr – vertical rootlet.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
getmorefigures.php?uid=PMC3924620&req=5

Figure 6: Details of organization of the apical organ in competent larvae of Phoronopsis harmeri. (A) Semi-thin parasagittal section of the apical organ. The locations of different types of perikarya are shown. The apical side is at the top; the hood edge is to the right; the dorsal side of the larva is to the left. A portion of the median neurite bundle is visible on the right. (B) Ultrastructural organization of a portion of the apical organ. Two types of perikarya and the neuropil (np) are visible. (C) Ultrastructural details of type 1 perikarya (p1), which have long microvilli (open arrowheads) around the cilium, a root apparatus, large and abundant mitochondria (m), and clear (electron light) synaptic vesicles (cv). (D) Ultrastructural details of a type 2 perikaryon (p2), which contains a dense-core (dc), clear (cv) vesicles, and rudiments of a cilium (highlighted by a circle). (E) Type 3 perikarya (p3) contain a nucleus (n) with a large nucleolus (nu), a large Golgi apparatus (G), and dense-core vesicles (dc). (F) The central portion of the neuropil contacts the basal lamina (bl). Neurites contain numerous synaptic vesicles (closed arrowheads) spread along the thickened membrane. The basal membranes of muscle cells (mc) are also thickened. Abbreviations: bc – blastocoel; bl – basal lamina; c1 – preoral coelom; cc – cells of coelomic lining; cv – clear synaptic vesicles; dc – dense-core vesicles; G – Golgi apparatus; hr – horizontal rootlet; m – mitochondria; mc – muscle cells; mn – median neurite bundle; n – nucleus; np – neuropil; nu – nucleolus; p1 – perikarya of 1 type; p2 – perikarya of 2 type; p3 – perikarya of 3 type; vr – vertical rootlet.

Mentions: The apical organ of competent P. harmeri larvae has a complex histological structure and consists of several types of perikarya (Figure 6A and B). The first type of perikarya is represented by sensory cells. Numerous sensory cells contact the epidermis surface and bear long microvilli, which surround the cilium (Figure 6C). One short horizontal and two long vertical striated rootlets pass from the basal body of the cilium. The apical cytoplasm is filled with mitochondria and vesicles. The large nucleus, which has electron-lucent karyoplasm and bears one or two nucleoli, occupies the central portion of the cell (Figure 6C). Clear synaptic vesicles, 60-70 nm in diameter, are located near the nucleus. The perikarya of the second type do not contact the surface of the epidermis, form two lateral groups under the neuropil, and contact the basal lamina (Figure 6A, B and D). The large nucleus in the second type of perikarya is about 5 μm in diameter and contains a distinct and large nucleolus, which is quite visible even in semi-thin sections. The cytoplasm contains the rudiments of a cilium including a basal body, an accessory centriole, and a short striated rootlet associated with the Golgi apparatus (Figure 6D). Large (90 ± 3 nm) dense-core vesicles and small (40 ± 2 nm) clear (electron light) synaptic vesicles occur in the second type of perikarya. Perikarya of the third type occupy the most dorsal position and form two groups, each of with is located at the beginning of the tentacular nerve ring branches (Figure 6A). This seems very similar to the location of the FMRFamide-like immunoreactive perikarya (Figure 5C). Perikarya of the third type do not contact the surface of epidermis but have the rudiments of a cilium, which is associated with large Golgi apparatuses (Figure 6E). The large nucleus is devoid of peripheral chromatin and contains a large nucleolus. The cytoplasm is grainy and contains many small mitochondria and vesicles, some of which are dense-core synaptic vesicles. The neuropil of the apical organ contacts the basal lamina in areas where the second type of perikarya is absent. Here, neurites contain numerous synaptic vesicles that are spread along the thickened membrane, which contacts the basal lamina. Muscle cells contact the basal lamina on the opposite side and have thickened membranes.


Development and organization of the larval nervous system in Phoronopsis harmeri: new insights into phoronid phylogeny.

Temereva EN, Tsitrin EB - Front. Zool. (2014)

Details of organization of the apical organ in competent larvae of Phoronopsis harmeri. (A) Semi-thin parasagittal section of the apical organ. The locations of different types of perikarya are shown. The apical side is at the top; the hood edge is to the right; the dorsal side of the larva is to the left. A portion of the median neurite bundle is visible on the right. (B) Ultrastructural organization of a portion of the apical organ. Two types of perikarya and the neuropil (np) are visible. (C) Ultrastructural details of type 1 perikarya (p1), which have long microvilli (open arrowheads) around the cilium, a root apparatus, large and abundant mitochondria (m), and clear (electron light) synaptic vesicles (cv). (D) Ultrastructural details of a type 2 perikaryon (p2), which contains a dense-core (dc), clear (cv) vesicles, and rudiments of a cilium (highlighted by a circle). (E) Type 3 perikarya (p3) contain a nucleus (n) with a large nucleolus (nu), a large Golgi apparatus (G), and dense-core vesicles (dc). (F) The central portion of the neuropil contacts the basal lamina (bl). Neurites contain numerous synaptic vesicles (closed arrowheads) spread along the thickened membrane. The basal membranes of muscle cells (mc) are also thickened. Abbreviations: bc – blastocoel; bl – basal lamina; c1 – preoral coelom; cc – cells of coelomic lining; cv – clear synaptic vesicles; dc – dense-core vesicles; G – Golgi apparatus; hr – horizontal rootlet; m – mitochondria; mc – muscle cells; mn – median neurite bundle; n – nucleus; np – neuropil; nu – nucleolus; p1 – perikarya of 1 type; p2 – perikarya of 2 type; p3 – perikarya of 3 type; vr – vertical rootlet.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC3924620&req=5

Figure 6: Details of organization of the apical organ in competent larvae of Phoronopsis harmeri. (A) Semi-thin parasagittal section of the apical organ. The locations of different types of perikarya are shown. The apical side is at the top; the hood edge is to the right; the dorsal side of the larva is to the left. A portion of the median neurite bundle is visible on the right. (B) Ultrastructural organization of a portion of the apical organ. Two types of perikarya and the neuropil (np) are visible. (C) Ultrastructural details of type 1 perikarya (p1), which have long microvilli (open arrowheads) around the cilium, a root apparatus, large and abundant mitochondria (m), and clear (electron light) synaptic vesicles (cv). (D) Ultrastructural details of a type 2 perikaryon (p2), which contains a dense-core (dc), clear (cv) vesicles, and rudiments of a cilium (highlighted by a circle). (E) Type 3 perikarya (p3) contain a nucleus (n) with a large nucleolus (nu), a large Golgi apparatus (G), and dense-core vesicles (dc). (F) The central portion of the neuropil contacts the basal lamina (bl). Neurites contain numerous synaptic vesicles (closed arrowheads) spread along the thickened membrane. The basal membranes of muscle cells (mc) are also thickened. Abbreviations: bc – blastocoel; bl – basal lamina; c1 – preoral coelom; cc – cells of coelomic lining; cv – clear synaptic vesicles; dc – dense-core vesicles; G – Golgi apparatus; hr – horizontal rootlet; m – mitochondria; mc – muscle cells; mn – median neurite bundle; n – nucleus; np – neuropil; nu – nucleolus; p1 – perikarya of 1 type; p2 – perikarya of 2 type; p3 – perikarya of 3 type; vr – vertical rootlet.
Mentions: The apical organ of competent P. harmeri larvae has a complex histological structure and consists of several types of perikarya (Figure 6A and B). The first type of perikarya is represented by sensory cells. Numerous sensory cells contact the epidermis surface and bear long microvilli, which surround the cilium (Figure 6C). One short horizontal and two long vertical striated rootlets pass from the basal body of the cilium. The apical cytoplasm is filled with mitochondria and vesicles. The large nucleus, which has electron-lucent karyoplasm and bears one or two nucleoli, occupies the central portion of the cell (Figure 6C). Clear synaptic vesicles, 60-70 nm in diameter, are located near the nucleus. The perikarya of the second type do not contact the surface of the epidermis, form two lateral groups under the neuropil, and contact the basal lamina (Figure 6A, B and D). The large nucleus in the second type of perikarya is about 5 μm in diameter and contains a distinct and large nucleolus, which is quite visible even in semi-thin sections. The cytoplasm contains the rudiments of a cilium including a basal body, an accessory centriole, and a short striated rootlet associated with the Golgi apparatus (Figure 6D). Large (90 ± 3 nm) dense-core vesicles and small (40 ± 2 nm) clear (electron light) synaptic vesicles occur in the second type of perikarya. Perikarya of the third type occupy the most dorsal position and form two groups, each of with is located at the beginning of the tentacular nerve ring branches (Figure 6A). This seems very similar to the location of the FMRFamide-like immunoreactive perikarya (Figure 5C). Perikarya of the third type do not contact the surface of epidermis but have the rudiments of a cilium, which is associated with large Golgi apparatuses (Figure 6E). The large nucleus is devoid of peripheral chromatin and contains a large nucleolus. The cytoplasm is grainy and contains many small mitochondria and vesicles, some of which are dense-core synaptic vesicles. The neuropil of the apical organ contacts the basal lamina in areas where the second type of perikarya is absent. Here, neurites contain numerous synaptic vesicles that are spread along the thickened membrane, which contacts the basal lamina. Muscle cells contact the basal lamina on the opposite side and have thickened membranes.

Bottom Line: Phoronid larvae demonstrate some "deuterostome-like" features, which are, in fact, have to be ancestral bilaterian characters.Our new results and previous data indicate that phoronids have retained some plesiomorphic features, which were inherited from the last common ancestor of all Bilateria.It follows that phoronids should be extracted from the Trochozoan (=Spiralia) clade and placed at the base of the Lophotrochozoan stem.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Invertebrate Zoology, Biological faculty, Moscow State University, Moscow 119992, Russia. temereva@mail.ru.

ABSTRACT

Background: The organization and development of the nervous system has traditionally been used as an important character for establishing the relationships among large groups of animals. According to this criterion, phoronids were initially regarded as deuterostomian but have more recently been regarded as protostomian. The resolving of this conflict requires detailed information from poorly investigated members of phoronids, such as Phoronopsis harmeri.

Results: The serotonin-like immunoreactive part of the P. harmeri nervous system changes during larval development. These changes mostly concern the nervous system of the hood and correlate with the appearance of the median and two marginal neurite bundles, the frontal organ, and the sensory field. The apical organ has bilateral symmetry. The tentacular neurite bundle passes under the tentacles, contains several types of perikarya, and gives rise to intertentacular bundles, which branch in the tentacle base and penetrate into adjacent tentacles by two lateroabfrontal bundles. There are two groups of dorsolateral perikarya, which exhibit serotonin-like immunoreactivity, contact the tentacular neurite bundle, and are located near the youngest tentacles. Larvae have a minor nerve ring, which originates from the posterior marginal neurite bundle of the hood, passes above the tentacle base, and gives rise to the mediofrontal neurite bundle in each tentacle. Paired laterofrontal neurite bundles of tentacles form a continuous nerve tract that conducts to the postoral ciliated band.

Discussion: The organization of the nervous system differs among the planktotrophic larvae of phoronid species. These differences may correlate with differences in phoronid biology. Data concerning the innervation of tentacles in different phoronid larvae are conflicting and require careful reinvestigation. The overall organization of the nervous system in phoronid larvae has more in common with the deuterostomian than with the protostomian nervous system. Phoronid larvae demonstrate some "deuterostome-like" features, which are, in fact, have to be ancestral bilaterian characters. Our new results and previous data indicate that phoronids have retained some plesiomorphic features, which were inherited from the last common ancestor of all Bilateria. It follows that phoronids should be extracted from the Trochozoan (=Spiralia) clade and placed at the base of the Lophotrochozoan stem.

No MeSH data available.


Related in: MedlinePlus