IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0029817.html
   My bibliography  Save this article

The Origin of GPCRs: Identification of Mammalian like Rhodopsin, Adhesion, Glutamate and Frizzled GPCRs in Fungi

Author

Listed:
  • Arunkumar Krishnan
  • Markus Sällman Almén
  • Robert Fredriksson
  • Helgi B Schiöth

Abstract

G protein-coupled receptors (GPCRs) in humans are classified into the five main families named Glutamate, Rhodopsin, Adhesion, Frizzled and Secretin according to the GRAFS classification. Previous results show that these mammalian GRAFS families are well represented in the Metazoan lineages, but they have not been shown to be present in Fungi. Here, we systematically mined 79 fungal genomes and provide the first evidence that four of the five main mammalian families of GPCRs, namely Rhodopsin, Adhesion, Glutamate and Frizzled, are present in Fungi and found 142 novel sequences between them. Significantly, we provide strong evidence that the Rhodopsin family emerged from the cAMP receptor family in an event close to the split of Opisthokonts and not in Placozoa, as earlier assumed. The Rhodopsin family then expanded greatly in Metazoans while the cAMP receptor family is found in 3 invertebrate species and lost in the vertebrates. We estimate that the Adhesion and Frizzled families evolved before the split of Unikonts from a common ancestor of all major eukaryotic lineages. Also, the study highlights that the fungal Adhesion receptors do not have N-terminal domains whereas the fungal Glutamate receptors have a broad repertoire of mammalian-like N-terminal domains. Further, mining of the close unicellular relatives of the Metazoan lineage, Salpingoeca rosetta and Capsaspora owczarzaki, obtained a rich group of both the Adhesion and Glutamate families, which in particular provided insight to the early emergence of the N-terminal domains of the Adhesion family. We identified 619 Fungi specific GPCRs across 79 genomes and revealed that Blastocladiomycota and Chytridiomycota phylum have Metazoan-like GPCRs rather than the GPCRs specific for Fungi. Overall, this study provides the first evidence of the presence of four of the five main GRAFS families in Fungi and clarifies the early evolutionary history of the GPCR superfamily.

Suggested Citation

  • Arunkumar Krishnan & Markus Sällman Almén & Robert Fredriksson & Helgi B Schiöth, 2012. "The Origin of GPCRs: Identification of Mammalian like Rhodopsin, Adhesion, Glutamate and Frizzled GPCRs in Fungi," PLOS ONE, Public Library of Science, vol. 7(1), pages 1-15, January.
    • Handle: RePEc:plo:pone00:0029817
    DOI: 10.1371/journal.pone.0029817
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0029817
    Download Restriction: no
    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0029817&type=printable
    Download Restriction: no
    File URL: https://libkey.io/10.1371/journal.pone.0029817?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Daniel M. Rosenbaum & Søren G. F. Rasmussen & Brian K. Kobilka, 2009. "The structure and function of G-protein-coupled receptors," Nature, Nature, vol. 459(7245), pages 356-363, May.
    2. Mansi Srivastava & Emina Begovic & Jarrod Chapman & Nicholas H. Putnam & Uffe Hellsten & Takeshi Kawashima & Alan Kuo & Therese Mitros & Asaf Salamov & Meredith L. Carpenter & Ana Y. Signorovitch & Ma, 2008. "The Trichoplax genome and the nature of placozoans," Nature, Nature, vol. 454(7207), pages 955-960, August.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Christine Guzman & Kurato Mohri & Ryotaro Nakamura & Minato Miyake & Yuko Tsuchiya & Kentaro Tomii & Hiroshi Watanabe, 2024. "Neuronal and non-neuronal functions of the synaptic cell adhesion molecule neurexin in Nematostella vectensis," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Kaihua Zhang & Hao Wu & Nicholas Hoppe & Aashish Manglik & Yifan Cheng, 2022. "Fusion protein strategies for cryo-EM study of G protein-coupled receptors," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    3. Miguel Fribourg & Diomedes E Logothetis & Javier González-Maeso & Stuart C Sealfon & Belén Galocha-Iragüen & Fernando Las-Heras Andrés & Vladimir Brezina, 2017. "Elucidation of molecular kinetic schemes from macroscopic traces using system identification," PLOS Computational Biology, Public Library of Science, vol. 13(2), pages 1-34, February.
    4. Mark J. Wall & Emily Hill & Robert Huckstepp & Kerry Barkan & Giuseppe Deganutti & Michele Leuenberger & Barbara Preti & Ian Winfield & Sabrina Carvalho & Anna Suchankova & Haifeng Wei & Dewi Safitri , 2022. "Selective activation of Gαob by an adenosine A1 receptor agonist elicits analgesia without cardiorespiratory depression," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    5. Eyal Rozenfeld & Merav Tauber & Yair Ben-Chaim & Moshe Parnas, 2021. "GPCR voltage dependence controls neuronal plasticity and behavior," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    6. Bob Zimmermann & Juan D. Montenegro & Sofia M. C. Robb & Whitney J. Fropf & Lukas Weilguny & Shuonan He & Shiyuan Chen & Jessica Lovegrove-Walsh & Eric M. Hill & Cheng-Yi Chen & Katerina Ragkousi & Da, 2023. "Topological structures and syntenic conservation in sea anemone genomes," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    7. Wenli Zhao & Wenru Zhang & Mu Wang & Minmin Lu & Shutian Chen & Tingting Tang & Gisela Schnapp & Holger Wagner & Albert Brennauer & Cuiying Yi & Xiaojing Chu & Shuo Han & Beili Wu & Qiang Zhao, 2022. "Ligand recognition and activation of neuromedin U receptor 2," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    8. Sathvik Anantakrishnan & Athi N. Naganathan, 2023. "Thermodynamic architecture and conformational plasticity of GPCRs," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    9. Anna Strunecka & Otakar Strunecky, 2019. "Chronic Fluoride Exposure and the Risk of Autism Spectrum Disorder," IJERPH, MDPI, vol. 16(18), pages 1-21, September.
    10. Marie Mi Bonde & Jonas Tind Hansen & Samra Joke Sanni & Stig Haunsø & Steen Gammeltoft & Christina Lyngsø & Jakob Lerche Hansen, 2010. "Biased Signaling of the Angiotensin II Type 1 Receptor Can Be Mediated through Distinct Mechanisms," PLOS ONE, Public Library of Science, vol. 5(11), pages 1-15, November.
    11. Manel Zeghal & Geneviève Laroche & Julia Douglas Freitas & Rebecca Wang & Patrick M. Giguère, 2023. "Profiling of basal and ligand-dependent GPCR activities by means of a polyvalent cell-based high-throughput platform," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    12. Pingfen Zhu & Weiqiang Liu & Xiaoxiao Zhang & Meng Li & Gaoming Liu & Yang Yu & Zihao Li & Xuanjing Li & Juan Du & Xiao Wang & Cyril C. Grueter & Ming Li & Xuming Zhou, 2023. "Correlated evolution of social organization and lifespan in mammals," Nature Communications, Nature, vol. 14(1), pages 1-18, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pone00:0029817. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.