Function of the male-gamete-specific fusion protein HAP2 in a seven-sexed ciliate

Eric S. Cole, Donna Cassidy-Hanley, Jennifer Fricke Pinello, Hong Zeng, Marion Hsueh, Daniel Kolbin, Courtney Ozzello, Thomas Giddings, Mark Winey, Theodore G. Clark

Research output: Contribution to journalArticle

28 Citations (Scopus)

Abstract

HAP2, a male-gamete-specific protein conserved across vast evolutionary distances, has garnered considerable attention as a potential membrane fusogen required for fertilization in taxa ranging from protozoa and green algae to flowering plants and invertebrate animals [1-6]. However, its presence in Tetrahymena thermophila, a ciliated protozoan with seven sexes or mating types that bypasses the production of male gametes, raises interesting questions regarding the evolutionary origins of gamete-specific functions in sexually dimorphic species. Here we show that HAP2 is expressed in all seven mating types of T. thermophila and that fertility is only blocked when the gene is deleted from both cells of a mating pair. HAP2 deletion strains of complementary mating types can recognize one another and form pairs; however, pair stability is compromised and membrane pore formation at the nuclear exchange junction is blocked. The absence of pore formation is consistent with previous studies suggesting a role for HAP2 in gamete fusion in other systems. We propose a model in which each of the several hundred membrane pores established at the conjugation junction of mating Tetrahymena represents the equivalent of a male/female interface, and that pore formation is driven on both sides of the junction by the presence of HAP2. Such a model supports the idea that many of the disparate functions of sperm and egg were shared by the "isogametes" of early eukaryotes and became partitioned to either male or female sex cells later in evolution.

Original languageEnglish (US)
Pages (from-to)2168-2173
Number of pages6
JournalCurrent Biology
Volume24
Issue number18
DOIs
StatePublished - Sep 22 2014
Externally publishedYes

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Germ Cells
Ciliophora
germ cells
Fusion reactions
Tetrahymena thermophila
Membranes
Protozoa
Proteins
proteins
Algae
Tetrahymena
Chlorophyta
Animals
Invertebrates
Genes
Eukaryota
Fertilization
Membrane Potentials
Ovum
Fertility

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Cole, E. S., Cassidy-Hanley, D., Fricke Pinello, J., Zeng, H., Hsueh, M., Kolbin, D., ... Clark, T. G. (2014). Function of the male-gamete-specific fusion protein HAP2 in a seven-sexed ciliate. Current Biology, 24(18), 2168-2173. https://doi.org/10.1016/j.cub.2014.07.064

Function of the male-gamete-specific fusion protein HAP2 in a seven-sexed ciliate. / Cole, Eric S.; Cassidy-Hanley, Donna; Fricke Pinello, Jennifer; Zeng, Hong; Hsueh, Marion; Kolbin, Daniel; Ozzello, Courtney; Giddings, Thomas; Winey, Mark; Clark, Theodore G.

In: Current Biology, Vol. 24, No. 18, 22.09.2014, p. 2168-2173.

Research output: Contribution to journalArticle

Cole, ES, Cassidy-Hanley, D, Fricke Pinello, J, Zeng, H, Hsueh, M, Kolbin, D, Ozzello, C, Giddings, T, Winey, M & Clark, TG 2014, 'Function of the male-gamete-specific fusion protein HAP2 in a seven-sexed ciliate', Current Biology, vol. 24, no. 18, pp. 2168-2173. https://doi.org/10.1016/j.cub.2014.07.064
Cole ES, Cassidy-Hanley D, Fricke Pinello J, Zeng H, Hsueh M, Kolbin D et al. Function of the male-gamete-specific fusion protein HAP2 in a seven-sexed ciliate. Current Biology. 2014 Sep 22;24(18):2168-2173. https://doi.org/10.1016/j.cub.2014.07.064
Cole, Eric S. ; Cassidy-Hanley, Donna ; Fricke Pinello, Jennifer ; Zeng, Hong ; Hsueh, Marion ; Kolbin, Daniel ; Ozzello, Courtney ; Giddings, Thomas ; Winey, Mark ; Clark, Theodore G. / Function of the male-gamete-specific fusion protein HAP2 in a seven-sexed ciliate. In: Current Biology. 2014 ; Vol. 24, No. 18. pp. 2168-2173.
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