Comparative genomics in Chlamydomonas and Plasmodium identifies an ancient nuclear envelope protein family essential for sexual reproduction in protists, fungi, plants, and vertebrates

Jue Ning, Thomas D. Otto, Claudia Pfander, Frank Schwach, Mathieu Brochet, Ellen Bushell, David Goulding, Mandy Sanders, Paul A. Lefebvre, Jimin Pei, Nick V. Grishin, Gary Vanderlaan, Oliver Billker, William J. Snell

Research output: Contribution to journalArticle

35 Citations (Scopus)

Abstract

Fertilization is a crucial yet poorly characterized event in eukaryotes. Our previous discovery that the broadly conserved protein HAP2 (GCS1) functioned in gametemembrane fusion in the unicellular green alga Chlamydomonas and the malaria pathogen Plasmodium led us to exploit the rare biological phenomenon of isogamy in Chlamydomonas in a comparative transcriptomics strategy to uncover additional conserved sexual reproduction genes. All previously identified Chlamydomonas fertilization-essential genes fell into related clusters based on their expression patterns. Out of several conserved genes in a minus gamete cluster, we focused on Cre06.g280600, an ortholog of the fertilization-related Arabidopsis GEX1. Gene disruption, cell biological, and immunolocalization studies show that CrGEX1 functions in nuclear fusion in Chlamydomonas. Moreover, CrGEX1 and its Plasmodium ortholog, PBANKA_113980, are essential for production of viable meiotic progeny in both organisms and thus for mosquito transmission of malaria. Remarkably, we discovered that the genes are members of a large, previously unrecognized family whose first-characterized member, KAR5, is essential for nuclear fusion during yeast sexual reproduction. Our comparative transcriptomics approach provides a new resource for studying sexual development and demonstrates that exploiting the data can lead to the discovery of novel biology that is conserved across distant taxa.

Original languageEnglish (US)
Pages (from-to)1198-1215
Number of pages18
JournalGenes and Development
Volume27
Issue number10
DOIs
StatePublished - May 15 2013

Fingerprint

Chlamydomonas
Plasmodium
Nuclear Envelope
Nuclear Proteins
Genomics
Reproduction
Vertebrates
Fungi
Nuclear Fusion
Fertilization
Genes
Plasmodium malariae
Biological Phenomena
Sexual Development
Chlorophyta
Essential Genes
Culicidae
Eukaryota
Arabidopsis
Germ Cells

Keywords

  • Chlamydomonas
  • Fertilization
  • KAR5/GEX1/Brambleberry
  • Nuclear envelope fusion
  • Plasmodium
  • RNA sequencing

ASJC Scopus subject areas

  • Genetics
  • Developmental Biology

Cite this

Comparative genomics in Chlamydomonas and Plasmodium identifies an ancient nuclear envelope protein family essential for sexual reproduction in protists, fungi, plants, and vertebrates. / Ning, Jue; Otto, Thomas D.; Pfander, Claudia; Schwach, Frank; Brochet, Mathieu; Bushell, Ellen; Goulding, David; Sanders, Mandy; Lefebvre, Paul A.; Pei, Jimin; Grishin, Nick V.; Vanderlaan, Gary; Billker, Oliver; Snell, William J.

In: Genes and Development, Vol. 27, No. 10, 15.05.2013, p. 1198-1215.

Research output: Contribution to journalArticle

Ning, J, Otto, TD, Pfander, C, Schwach, F, Brochet, M, Bushell, E, Goulding, D, Sanders, M, Lefebvre, PA, Pei, J, Grishin, NV, Vanderlaan, G, Billker, O & Snell, WJ 2013, 'Comparative genomics in Chlamydomonas and Plasmodium identifies an ancient nuclear envelope protein family essential for sexual reproduction in protists, fungi, plants, and vertebrates', Genes and Development, vol. 27, no. 10, pp. 1198-1215. https://doi.org/10.1101/gad.212746.112
Ning, Jue ; Otto, Thomas D. ; Pfander, Claudia ; Schwach, Frank ; Brochet, Mathieu ; Bushell, Ellen ; Goulding, David ; Sanders, Mandy ; Lefebvre, Paul A. ; Pei, Jimin ; Grishin, Nick V. ; Vanderlaan, Gary ; Billker, Oliver ; Snell, William J. / Comparative genomics in Chlamydomonas and Plasmodium identifies an ancient nuclear envelope protein family essential for sexual reproduction in protists, fungi, plants, and vertebrates. In: Genes and Development. 2013 ; Vol. 27, No. 10. pp. 1198-1215.
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