Dataset Information

Evolution and expression plasticity of opsin genes in a fig pollinator, Ceratosolen solmsi.

ABSTRACT: Figs and fig pollinators have co-evolved species-specific systems of mutualism. So far, it was unknown how visual opsin genes of pollinators have evolved in the light conditions inside their host figs. We cloned intact full-length mRNA sequences of four opsin genes from a species of fig pollinator, Ceratosolen solmsi, and tested for selective pressure and expressional plasticity of these genes. Molecular evolutionary analysis indicated that the four opsin genes evolved under different selective constraints. Subsets of codons in the two long wavelength sensitive opsin (LW1, LW2) genes were positively selected in ancestral fig pollinators. The ultraviolet sensitive opsin (UV) gene was under strong purifying selection, whereas a relaxation of selective constrains occurred on several amino acids in the blue opsin. RT-qPCR analysis suggested that female and male fig pollinators had different expression patterns possibly due to their distinct lifestyles and different responses to light within the syconia. Co-evolutionary history with figs might have influenced the evolution and expression plasticity of opsin genes in fig pollinators.

SUBMITTER: Wang B

PROVIDER: S-EPMC3547053 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Evolution and expression plasticity of opsin genes in a fig pollinator, Ceratosolen solmsi.

Wang Bo B Xiao Jin-Hua JH Bian Sheng-Nan SN Niu Li-Ming LM Murphy Robert W RW Huang Da-Wei DW

PloS one 20130116 1

Figs and fig pollinators have co-evolved species-specific systems of mutualism. So far, it was unknown how visual opsin genes of pollinators have evolved in the light conditions inside their host figs. We cloned intact full-length mRNA sequences of four opsin genes from a species of fig pollinator, Ceratosolen solmsi, and tested for selective pressure and expressional plasticity of these genes. Molecular evolutionary analysis indicated that the four opsin genes evolved under different selective ...[more]

PMID: 23342036

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Project description:BackgroundThe evolution of opsin genes is of great interest because it can provide insight into the evolution of light detection and vision. An interesting group in which to study opsins is Cnidaria because it is a basal phylum sister to Bilateria with much visual diversity within the phylum. Hydra vulgaris (H. vulgaris) is a cnidarian with a plethora of genomic resources to characterize the opsin gene family. This eyeless cnidarian has a behavioral reaction to light, but it remains unknown which of its many opsins functions in light detection. Here, we used phylogenetics and RNA-seq to investigate the molecular evolution of opsin genes and their expression in H. vulgaris. We explored where opsin genes are located relative to each other in an improved genome assembly and where they belong in a cnidarian opsin phylogenetic tree. In addition, we used RNA-seq data from different tissues of the H. vulgaris adult body and different time points during regeneration and budding stages to gain insight into their potential functions.ResultsWe identified 45 opsin genes in H. vulgaris, many of which were located near each other suggesting evolution by tandem duplications. Our phylogenetic tree of cnidarian opsin genes supported previous claims that they are evolving by lineage-specific duplications. We identified two H. vulgaris genes (HvOpA1 and HvOpB1) that fall outside of the two commonly determined Hydra groups; these genes possibly have a function in nematocytes and mucous gland cells respectively. We also found opsin genes that have similar expression patterns to phototransduction genes in H. vulgaris. We propose a H. vulgaris phototransduction cascade that has components of both ciliary and rhabdomeric cascades.ConclusionsThis extensive study provides an in-depth look at the molecular evolution and expression of H. vulgaris opsin genes. The expression data that we have quantified can be used as a springboard for additional studies looking into the specific function of opsin genes in this species. Our phylogeny and expression data are valuable to investigations of opsin gene evolution and cnidarian biology.

Project description:BACKGROUND:Calcium-activated photoproteins are luciferase variants found in photocyte cells of bioluminescent jellyfish (Phylum Cnidaria) and comb jellies (Phylum Ctenophora). The complete genomic sequence from the ctenophore Mnemiopsis leidyi, a representative of the earliest branch of animals that emit light, provided an opportunity to examine the genome of an organism that uses this class of luciferase for bioluminescence and to look for genes involved in light reception. To determine when photoprotein genes first arose, we examined the genomic sequence from other early-branching taxa. We combined our genomic survey with gene trees, developmental expression patterns, and functional protein assays of photoproteins and opsins to provide a comprehensive view of light production and light reception in Mnemiopsis. RESULTS:The Mnemiopsis genome has 10 full-length photoprotein genes situated within two genomic clusters with high sequence conservation that are maintained due to strong purifying selection and concerted evolution. Photoprotein-like genes were also identified in the genomes of the non-luminescent sponge Amphimedon queenslandica and the non-luminescent cnidarian Nematostella vectensis, and phylogenomic analysis demonstrated that photoprotein genes arose at the base of all animals. Photoprotein gene expression in Mnemiopsis embryos begins during gastrulation in migrating precursors to photocytes and persists throughout development in the canals where photocytes reside. We identified three putative opsin genes in the Mnemiopsis genome and show that they do not group with well-known bilaterian opsin subfamilies. Interestingly, photoprotein transcripts are co-expressed with two of the putative opsins in developing photocytes. Opsin expression is also seen in the apical sensory organ. We present evidence that one opsin functions as a photopigment in vitro, absorbing light at wavelengths that overlap with peak photoprotein light emission, raising the hypothesis that light production and light reception may be functionally connected in ctenophore photocytes. We also present genomic evidence of a complete ciliary phototransduction cascade in Mnemiopsis. CONCLUSIONS:This study elucidates the genomic organization, evolutionary history, and developmental expression of photoprotein and opsin genes in the ctenophore Mnemiopsis leidyi, introduces a novel dual role for ctenophore photocytes in both bioluminescence and phototransduction, and raises the possibility that light production and light reception are linked in this early-branching non-bilaterian animal.

Dataset Information

Evolution and expression plasticity of opsin genes in a fig pollinator, Ceratosolen solmsi.

Publications

Evolution and expression plasticity of opsin genes in a fig pollinator, Ceratosolen solmsi.

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