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The conserved plant sterility gene HAP2 functions after attachment of fusogenic membranes in Chlamydomonas and Plasmodium gametes

¹ Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, Texas 75390, USA; ² Division of Cell and Molecular Biology, Imperial College London, London SW7 2AZ, United Kingdom; ³ Institute of Genetics, University of Nottingham, Queen’s Medical Centre, Nottingham NG7 2UH, United Kingdom; ⁴ The Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 SA1, United Kingdom; ⁵ Howard Hughes Medical Institute, University of Texas Southwestern Medical Center at Dallas, Dallas, Texas 75390, USA; ⁶ Department of Biological Chemistry and the Developmental Biology Center, University of California, Irvine, California 92697, USA

The cellular and molecular mechanisms that underlie species-specific membrane fusion between male and female gametes remain largely unknown. Here, by use of gene discovery methods in the green alga Chlamydomonas, gene disruption in the rodent malaria parasite Plasmodium berghei, and distinctive features of fertilization in both organisms, we report discovery of a mechanism that accounts for a conserved protein required for gamete fusion. A screen for fusion mutants in Chlamydomonas identified a homolog of HAP2, an Arabidopsis sterility gene. Moreover, HAP2 disruption in Plasmodium blocked fertilization and thereby mosquito transmission of malaria. HAP2 localizes at the fusion site of Chlamydomonas minus gametes, yet Chlamydomonas minus and Plasmodium hap2 male gametes retain the ability, using other, species-limited proteins, to form tight prefusion membrane attachments with their respective gamete partners. Membrane dye experiments show that HAP2 is essential for membrane merger. Thus, in two distantly related eukaryotes, species-limited proteins govern access to a conserved protein essential for membrane fusion.

[Keywords: Gamete fusion; cell–cell fusion; malaria; HAP2; Chlamydomonas, Plasmodium]]

Received January 28, 2008; revised version accepted February 22, 2008.

⁸ Corresponding authors.

E-MAIL william.snell{at}utsouthwestern.edu; FAX (214) 648-8694.

⁹ E-MAIL ob4{at}sanger.ac.uk; FAX 44-20-7594-5424.

Supplemental material is available at http://www.genesdev.org.

Article published online ahead of print. Article and publication date are online at http://www.genesdev.org/cgi/doi/10.1101/gad.1656508.

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