Membrane fusion triggers rapid degradation of two gamete-specific, fusion-essential proteins in a membrane block to polygamy in Chlamydomonas
Yanjie Liu1, Michael J. Misamore2, and William J. Snell1
1) Department of Cell Biology, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390-9039, USA
2) Department of Biology, Texas Christian University, 2800 S. University Drive, Fort Worth, Texas 76129 USA
The plasma membranes of gametes are specialized for fusion, yet once fusion occurs the new zygote becomes incapable of further membrane fusion reactions. The molecular mechanisms that underlie this loss of fusion capacity (block to polygamy) remain unknown. Previously our laboratory has shown that during fertilization in Chlamydomonas, the plus gamete-specific membrane protein FUS1 is required for adhesion between the apically localized sites on the plasma membranes of plus and minus gametes that are specialized for fusion, and the minus-specific membrane protein HAP2 is essential for completion of the membrane fusion reaction. HAP2 (GCS1) family members are also required for fertilization in Arabidopsis and for the membrane fusion reaction in the malaria organism Plasmodium berghei. Here, we report that even though the gamete fusogenic sites support multi-cell adhesions (up to 30% cells in multi-cell adhesions), triploid zygotes are rare (0.2-0.6% of gametes form triploids), indicating a fusion-triggered block to subsequent fusion. We tested whether Chlamydomonas gamete fusion triggers alterations in FUS1 and HAP2 and renders the plasma membranes of the cells incapable of subsequent fusion. Consistent with the extinction of fusogenic capacity, both FUS1 and HAP2 are degraded upon fusion. The rapid, fusion-triggered cleavage of HAP2 in zygotes is distinct from degradation occurring during constitutive turnover in gametes. Thus, gamete fusion triggers specific degradation of fusion-essential proteins and renders the zygote incapable of fusion. Our results provide the first molecular explanation for a membrane block to polygamy in any organism. This work was supported by grants from the NIH (National Research Service Award GM-20329 to M. J. M. and GM-56778 to W. J. S.).
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