Opsin Repertoire and Expression Patterns in Horseshoe Crabs: Evidence from the Genome of Limulus polyphemus (Arthropoda: Chelicerata)

Barbara-Anne Battelle, Joseph F. Ryan, Karen E. Kempler, Spencer R. Saraf, Catherine E. Marten, Wesley C. Warren, Patrick J. Minx, Michael J. Montague, Pamela J. Green, Skye A. Schmidt, Lucinda Fulton, Nipam H. Patel, Meredith E. Protas, Richard K. Wilson, Megan L. Porter

    Research output: Contribution to journalArticlepeer-review

    Abstract

    Horseshoe crabs are xiphosuran chelicerates, the sister groupto arachnids. As such, they are important for understandingthemost recent common ancestor of Euchelicerata and the evolution and diversification of Arthropoda. Limulus polyphemus is the most investigated of the four extant species of horseshoe crabs, and the structure and function of its visual system have long been a major focus of studies critical for understanding the evolution of visual systems in arthropods. Likewise, studies of genes encoding Limulus opsins, the protein component of the visual pigments, are critical for understanding opsin evolution and diversification among chelicerates, where knowledge of opsins is limited, and more broadly among arthropods. In the present study, we sequenced and assembled a high quality nuclear genomic sequence of L. polyphemus and used these data to annotate the full repertoire of Limulus opsins.Weconducted a detailed phylogenetic analysis of Limulus opsins, including using gene structure and synteny information to identify relationships among different opsin classes.We used our phylogeny to identify significant genomic events that shaped opsin evolution and therefore the visual systemof Limulus.We also describe the tissue expression patterns of the 18 opsins identified and show that transcripts encoding a number, including a peropsin, are present throughout the central nervous system. In additionto significantly extending our understanding of photosensitivity in Limulus and providing critical insight into the genomic evolution of horseshoe crab opsins, this work provides a valuable genomic resource for addressing myriad questions related to xiphosuran physiology and arthropod evolution.

    Original languageAmerican English
    Pages (from-to)1571-1589
    Number of pages19
    JournalGenome Biology and Evolution
    Volume8
    Issue number5
    StatePublished - Apr 29 2016

    Funding

    The Limulus genome project was conceived by N.P. and R.K.W. and completed at the McDonnell Genome Institute at Washington University School of Medicine by W.C.W., P.M., M.J.M. and L.F. with critical input from P.J.G., S.A.S., M.E.P. and B.-A.B. The project was supported by the National Human Genome Research Institute [2U54HG00307909 to R.K.W.], and the National Science Foundation [MCB1021636 to P.J.G.]. Analyses of Limulus opsins and their expression was conceived by B.-A.B., J.F.R. and M.L.P. and executed at the University of Florida’s Whitney Laboratory for Marine Bioscience and the University of Hawaii, Manoa by B.-A.B., J.F.R., M.L.R., K.E.K., S.R.S., and C.E.M. The study was supported by the National Science Foundation [IOS 1146175 and DBI 0648969 to B.-A.B.], startup funds from the University of Florida DSP Research Strategic Initiatives #00114464 and University of Florida Office of the Provost Programs to J.F.R., and startup funds from the University of Hawaii, Manoa to M.L.P. S.R.S was a National Science Foundation Research Experience for Undergraduates trainee at the Whitney Laboratory [DBI 0648969]. The article was prepared by B.-A.B., J.F.R., M.L.P. and M.J.M. with critical input from each of the authors. The authors thank Terence Murphey at NCBI for genome annotation.

    FundersFunder number
    McDonnell Genome Institute at Washington University School of Medicine
    University of Florida Office of the Provost Programs
    National Science FoundationMCB1021636, IOS 1146175, DBI 0648969, 1156528
    National Human Genome Research Institute2U54HG00307909
    Directorate for Biological Sciences0648969, 1146175, 1021636
    University of Florida00114464
    University of Hawai'i
    Experimental Social Science Laboratory, University of California Berkeley
    Office of the Provost, University of South Carolina

      ASJC Scopus Subject Areas

      • General Medicine

      Keywords

      • Limulus polyphemus
      • xiphosuran
      • opsin
      • photoreceptors
      • evolution
      • Xiphosuran
      • Evolution
      • Photoreceptors
      • Opsin

      Disciplines

      • Genetics and Genomics
      • Marine Biology

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