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Transcriptomic analysis of sea star development through metamorphosis to the highly derived pentameral body plan with a focus on neural transcription factors.

ABSTRACT: The Echinodermata is characterized by a secondarily evolved pentameral body plan. While the evolutionary origin of this body plan has been the subject of debate, the molecular mechanisms underlying its development are poorly understood. We assembled a de novo developmental transcriptome from the embryo through metamorphosis in the sea star Parvulastra exigua. We use the asteroid model as it represents the basal-type echinoderm body architecture. Global variation in gene expression distinguished the gastrula profile and showed that metamorphic and juvenile stages were more similar to each other than to the pre-metamorphic stages, pointing to the marked changes that occur during metamorphosis. Differential expression and gene ontology (GO) analyses revealed dynamic changes in gene expression throughout development and the transition to pentamery. Many GO terms enriched during late metamorphosis were related to neurogenesis and signalling. Neural transcription factor genes exhibited clusters with distinct expression patterns. A suite of these genes was up-regulated during metamorphosis (e.g. Pax6, Eya, Hey, NeuroD, FoxD, Mbx, and Otp). In situ hybridization showed expression of neural genes in the CNS and sensory structures. Our results provide a foundation to understand the metamorphic transition in echinoderms and the genes involved in development and evolution of pentamery.

SUBMITTER: Byrne M

PROVIDER: S-EPMC7315356 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Transcriptomic analysis of sea star development through metamorphosis to the highly derived pentameral body plan with a focus on neural transcription factors.

Byrne Maria M Koop Demian D Strbenac Dario D Cisternas Paula P Balogh Regina R Yang Jean Yee Hwa JYH Davidson Phillip L PL Wray Gregory G

DNA research : an international journal for rapid publication of reports on genes and genomes 20200201 1

The Echinodermata is characterized by a secondarily evolved pentameral body plan. While the evolutionary origin of this body plan has been the subject of debate, the molecular mechanisms underlying its development are poorly understood. We assembled a de novo developmental transcriptome from the embryo through metamorphosis in the sea star Parvulastra exigua. We use the asteroid model as it represents the basal-type echinoderm body architecture. Global variation in gene expression distinguished ...[more]

PMID: 32339242

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Project description:Echinoderms display a vast array of pigmentation and patterning in larval and adult life stages. This coloration is thought to be important for immune defense and camouflage. However, neither the cellular nor molecular mechanism that regulates this complex coloration in the adult is known. Here we knocked out three different genes thought to be involved in the pigmentation pathway(s) of larvae and grew the embryos to adulthood. The genes tested were polyketide synthase (PKS), Flavin-dependent monooxygenase family 3 (FMO3) and glial cells missing (GCM). We found that disabling of the PKS gene at fertilization resulted in albinism throughout all life stages and throughout all cells and tissues of this animal, including the immune cells of the coelomocytes. We also learned that FMO3 is an essential modifier of the polyketide. FMO3 activity is essential for larval pigmentation, but in juveniles and adults, loss of FMO3 activity resulted in the animal becoming pastel purple. Linking the LC-MS analysis of this modified pigment to a naturally purple animal suggested a conserved echinochrome profile yielding a pastel purple. We interpret this result as FMO3 modifies the parent polyketide to contribute to the normal brown/green color of the animal, and that in its absence, other biochemical modifications are revealed, perhaps by other members of the large FMO family in this animal. The FMO modularity revealed here may be important in the evolutionary changes between species and for different immune challenges. We also learned that glial cells missing (GCM), a key transcription factor of the endomesoderm gene regulatory network of embryos in the sea urchin, is required for pigmentation throughout the life stages of this sea urchin, but surprisingly, is not essential for larval development, metamorphosis, or maintenance of adulthood. Mosaic knockout of either PKS or GCM revealed spatial lineage commitment in the transition from bilaterality of the larva to a pentaradial body plan of the adult. The cellular lineages identified by pigment presence or absence (wild-type or knock-out lineages, respectively) followed a strict oral/aboral profile. No circumferential segments were seen and instead we observed 10-fold symmetry in the segments of pigment expression. This suggests that the adult lineage commitments in the five outgrowths of the hydropore in the larva are early, complete, fixed, and each bilaterally symmetric. Overall, these results suggest that pigmentation of this animal is genetically determined and dependent on a population of pigment stem cells that are set-aside in a sub-region of each outgrowth of the pentaradial adult rudiment prior to metamorphosis. This study reveals the complex chemistry of pigment applicable to many organisms, and further, provides an insight into the key transitions from bilateral to pentaradial body plans unique to echinoderms.

Dataset Information

Transcriptomic analysis of sea star development through metamorphosis to the highly derived pentameral body plan with a focus on neural transcription factors.

Publications

Transcriptomic analysis of sea star development through metamorphosis to the highly derived pentameral body plan with a focus on neural transcription factors.

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