Dataset Information

Transcriptomic analysis of the highly derived radial body plan of a sea urchin.

ABSTRACT: With their complex life cycle and highly derived body plan, echinoderms are unique among bilaterians. Although early development has been intensively studied, the molecular mechanisms underlying development of the adult echinoderm and its unusual radial body plan are largely unknown. To investigate the evolution of developmental changes in gene expression underlying radial body plan development and metamorphosis, we assembled a reference transcriptome de novo and used RNA-seq to measure gene expression profiles across larval, metamorphic, and postmetamorphic life cycle phases in the sea urchin Heliocidaris erythrogramma. Our results present a high-resolution view of gene expression dynamics during the complex transition from pre- to postmetamorphic development and suggest that distinct sets of regulatory and effector proteins are used during different life history phases. These analyses provide an important foundation for more detailed analyses of the evolution of the radial adult body of echinoderms.

SUBMITTER: Wygoda JA

PROVIDER: S-EPMC4007537 | biostudies-literature | 2014 Apr

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Transcriptomic analysis of the highly derived radial body plan of a sea urchin.

Wygoda Jennifer A JA Yang Yee Y Byrne Maria M Wray Gregory A GA

Genome biology and evolution 20140401 4

With their complex life cycle and highly derived body plan, echinoderms are unique among bilaterians. Although early development has been intensively studied, the molecular mechanisms underlying development of the adult echinoderm and its unusual radial body plan are largely unknown. To investigate the evolution of developmental changes in gene expression underlying radial body plan development and metamorphosis, we assembled a reference transcriptome de novo and used RNA-seq to measure gene exp ...[more]

PMID: 24696402

Similar Datasets

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.

Project description:BackgroundThe sea urchin embryo has been an important model organism in developmental biology for more than a century. This is due to its relatively simple construction, translucent appearance, and the possibility to follow the fate of individual cells as development to the pluteus larva proceeds. Because the larvae contain tiny calcitic skeletal elements, the spicules, they are also important model organisms for biomineralization research. Similar to other biominerals the spicule contains an organic matrix, which is thought to play an important role in its formation. However, only few spicule matrix proteins were identified previously.ResultsUsing mass spectrometry-based methods we have identified 231 proteins in the matrix of the S. purpuratus spicule matrix. Approximately two thirds of the identified proteins are either known or predicted to be extracellular proteins or transmembrane proteins with large ectodomains. The ectodomains may have been solubilized by partial proteolysis and subsequently integrated into the growing spicule. The most abundant protein of the spicule matrix is SM50. SM50-related proteins, SM30-related proteins, MSP130 and related proteins, matrix metalloproteases and carbonic anhydrase are among the most abundant components.ConclusionsThe spicule matrix is a relatively complex mixture of proteins not only containing matrix-specific proteins with a function in matrix assembly or mineralization, but also: 1) proteins possibly important for the formation of the continuous membrane delineating the mineralization space; 2) proteins for secretory processes delivering proteinaceous or non-proteinaceous precursors; 3) or proteins reflecting signaling events at the cell/matrix interface. Comparison of the proteomes of different skeletal matrices allows prediction of proteins of general importance for mineralization in sea urchins, such as SM50, SM30-E, SM29 or MSP130. The comparisons also help point out putative tissue-specific proteins, such as tooth phosphodontin or specific spicule matrix metalloproteases of the MMP18/19 group. Furthermore, the direct sequence analysis of peptides by MS/MS validates many predicted genes and confirms the existence of the corresponding proteins.

Dataset Information

Transcriptomic analysis of the highly derived radial body plan of a sea urchin.

Publications

Transcriptomic analysis of the highly derived radial body plan of a sea urchin.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets