The Conserved Plant Sterility Gene HAP2 Functions After Attachment of Fusogenic Membranes in Chlamydomonas and Plasmodium Gametes

Overview

Journal Genes Dev

Specialty Molecular Biology

Date 2008 Mar 28

PMID 18367645

Citations 164

Authors

Yanjie Liu

Rita Tewari

Jue Ning

Andrew M Blagborough

Sara Garbom

Jimin Pei

Nick V Grishin

Robert E Steele

Robert E Sinden

William J Snell

Oliver Billker

Affiliations

Soon will be listed here.

Abstract

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.

Citing Articles

Targeting Bottlenecks in Malaria Transmission: Antibody-Epitope Descriptions Guide the Design of Next-Generation Biomedical Interventions.

Yoo R, Jore M, Julien J Immunol Rev. 2025; 330(1):e70001.

PMID: 39907429 PMC: 11796336. DOI: 10.1111/imr.70001.

DUO1 Activated Zinc Finger (AtDAZ) protein role in the generative cell body morphogenesis.

Rauf A, Wang A, Li Y, Lian Z, Wei S, Khan Q Plant Mol Biol. 2025; 115(1):15.

PMID: 39777569 DOI: 10.1007/s11103-024-01542-w.

Plasmodium NEK1 coordinates MTOC organisation and kinetochore attachment during rapid mitosis in male gamete formation.

Zeeshan M, Rashpa R, Ferguson D, Mckeown G, Nugmanova R, Subudhi A PLoS Biol. 2024; 22(9):e3002802.

PMID: 39255311 PMC: 11414920. DOI: 10.1371/journal.pbio.3002802.

The C-terminal region of the Plasmodium berghei gamete surface 184-kDa protein Pb184 contributes to fertilization and male gamete binding to the residual body.

Nakayama K, Haraguchi A, Hakozaki J, Nakamura S, Kusakisako K, Ikadai H Parasit Vectors. 2024; 17(1):304.

PMID: 39003498 PMC: 11246575. DOI: 10.1186/s13071-024-06374-7.

Novel requirements for HAP2/GCS1-mediated gamete fusion in .

Pinello J, Loidl J, Seltzer E, Cassidy-Hanley D, Kolbin D, Abdelatif A iScience. 2024; 27(6):110146.

PMID: 38904066 PMC: 11187246. DOI: 10.1016/j.isci.2024.110146.

References

Ferris P, Waffenschmidt S, Umen J, Lin H, Lee J, Ishida K . Plus and minus sexual agglutinins from Chlamydomonas reinhardtii. Plant Cell. 2005; 17(2):597-615. PMC: 548829. DOI: 10.1105/tpc.104.028035. View

Wilson N, Foglesong M, Snell W . The Chlamydomonas mating type plus fertilization tubule, a prototypic cell fusion organelle: isolation, characterization, and in vitro adhesion to mating type minus gametes. J Cell Biol. 1997; 137(7):1537-53. PMC: 2137821. DOI: 10.1083/jcb.137.7.1537. View

Primakoff P, Myles D . Penetration, adhesion, and fusion in mammalian sperm-egg interaction. Science. 2002; 296(5576):2183-5. DOI: 10.1126/science.1072029. View

Carter R, Chen D . Malaria transmission blocked by immunisation with gametes of the malaria parasite. Nature. 1976; 263(5572):57-60. DOI: 10.1038/263057a0. View

BUCHANAN M, Imam S, Eskue W, Snell W . Activation of the cell wall degrading protease, lysin, during sexual signalling in Chlamydomonas: the enzyme is stored as an inactive, higher relative molecular mass precursor in the periplasm. J Cell Biol. 1989; 108(1):199-207. PMC: 2115355. DOI: 10.1083/jcb.108.1.199. View

Eksi S, Czesny B, van Gemert G, Sauerwein R, Eling W, Williamson K . Malaria transmission-blocking antigen, Pfs230, mediates human red blood cell binding to exflagellating male parasites and oocyst production. Mol Microbiol. 2006; 61(4):991-8. DOI: 10.1111/j.1365-2958.2006.05284.x. View

Faure J, Digonnet C, Dumas C . An in vitro system for adhesion and fusion of maize gametes. Science. 1994; 263(5153):1598-600. DOI: 10.1126/science.263.5153.1598. View

Wang Q, Pan J, Snell W . Intraflagellar transport particles participate directly in cilium-generated signaling in Chlamydomonas. Cell. 2006; 125(3):549-62. DOI: 10.1016/j.cell.2006.02.044. View

Kroft T, Gleason E, LHernault S . The spe-42 gene is required for sperm-egg interactions during C. elegans fertilization and encodes a sperm-specific transmembrane protein. Dev Biol. 2005; 286(1):169-81. DOI: 10.1016/j.ydbio.2005.07.020. View

10.

Sollner T . Intracellular and viral membrane fusion: a uniting mechanism. Curr Opin Cell Biol. 2004; 16(4):429-35. DOI: 10.1016/j.ceb.2004.06.015. View

11.

Doberstein S, Fetter R, Mehta A, Goodman C . Genetic analysis of myoblast fusion: blown fuse is required for progression beyond the prefusion complex. J Cell Biol. 1997; 136(6):1249-61. PMC: 2132517. DOI: 10.1083/jcb.136.6.1249. View

12.

Silflow C, Lavoie M, Tam L, Tousey S, Sanders M, Wu W . The Vfl1 Protein in Chlamydomonas localizes in a rotationally asymmetric pattern at the distal ends of the basal bodies. J Cell Biol. 2001; 153(1):63-74. PMC: 2185524. DOI: 10.1083/jcb.153.1.63. View

13.

Detmers P, Goodenough U, Condeelis J . Elongation of the fertilization tubule in Chlamydomonas: new observations on the core microfilaments and the effect of transient intracellular signals on their structural integrity. J Cell Biol. 1983; 97(2):522-32. PMC: 2112536. DOI: 10.1083/jcb.97.2.522. View

14.

Estrada B, Maeland A, Gisselbrecht S, Bloor J, Brown N, Michelson A . The MARVEL domain protein, Singles Bar, is required for progression past the pre-fusion complex stage of myoblast fusion. Dev Biol. 2007; 307(2):328-39. PMC: 1994691. DOI: 10.1016/j.ydbio.2007.04.045. View

15.

Ellerman D, Cohen D, Da Ros V, Morgenfeld M, Busso D, Cuasnicu P . Sperm protein "DE" mediates gamete fusion through an evolutionarily conserved site of the CRISP family. Dev Biol. 2006; 297(1):228-37. DOI: 10.1016/j.ydbio.2006.05.013. View

16.

Peng X, Sun M, Yang H . A novel in vitro system for gamete fusion in maize. Cell Res. 2005; 15(9):734-8. DOI: 10.1038/sj.cr.7290343. View

17.

Jahn R, Lang T, Sudhof T . Membrane fusion. Cell. 2003; 112(4):519-33. DOI: 10.1016/s0092-8674(03)00112-0. View

18.

Inoue N, Yamaguchi R, Ikawa M, Okabe M . Sperm-egg interaction and gene manipulated animals. Soc Reprod Fertil Suppl. 2007; 65:363-71. View

19.

Kumar N . Target antigens of malaria transmission blocking immunity exist as a stable membrane bound complex. Parasite Immunol. 1987; 9(3):321-35. DOI: 10.1111/j.1365-3024.1987.tb00511.x. View

20.

Matsuda Y, Saito T, Yamaguchi T, Kawase H . Cell wall lytic enzyme released by mating gametes of Chlamydomonas reinhardtii is a metalloprotease and digests the sodium perchlorate-insoluble component of cell wall. J Biol Chem. 1985; 260(10):6373-7. View