Ectopic expression of a <i>Chlamydomonas</i> mt+-specific homeodomain protein in mt− gametes initiates zygote development without gamete fusion

Zhao, Hui; Lu, Min; Singh, Ritu; Snell, William J.

doi:10.1101/gad.919501

Cited by 64 publications

(44 citation statements)

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“…Regarding the genetic mechanism underlying the full program of zygote development, GSP1 originating from plus gametes and GSM1 originating from minus gametes both contribute to zygote development, including the resorption of flagella, fusion of nuclei and chloroplasts, destruction of minus gamete G-chloroplast DNA, and secretion of a resistant cell wall (Wilson et al 1999). Earlier studies showed that the ectopic expression of GSP1 in minus gametes or of GSM1 in plus gametes can switch the zygotic differentiation programme on, and the resulting zygotes could undergo a normal meiosis (Zhao et al 2001, Lee et al 2008. Further research has uncovered the functional homology between GSP1/GSM1 and KNOX/BELL, which regulate stem-cell specification in land plants (Lee et al 2008).…”

Section: A Molecular Perspective On Fertility Genetic Controlmentioning

confidence: 99%

Seaweed reproductive biology: environmental and genetic controls

et al. 2017

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Knowledge of life cycle progression and reproduction of seaweeds transcends pure academic interest. Successful and sustainable seaweed exploitation and domestication will indeed require excellent control of the factors controlling growth and reproduction. The relative dominance of the ploidy-phases and their respective morphologies, however, display tremendous diversity. Consequently, the ecological and endogenous factors controlling life cycles are likely to be equally varied. A vast number of research papers addressing theoretical, ecological and physiological aspects of reproduction have been published over the years. Here, we review the current knowledge on reproductive strategies, trade-offs of reproductive effort in natural populations, and the environmental and endogenous factors controlling reproduction. Given that the majority of ecophysiological studies predate the "-omics" era, we examine the extent to which this knowledge of reproduction has been, or can be, applied to further our knowledge of life cycle control in seaweeds.

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Section: A Molecular Perspective On Fertility Genetic Controlmentioning

confidence: 99%

Seaweed reproductive biology: environmental and genetic controls

et al. 2017

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“…One model for the degradation we observed is that degradation of HAP2 in the zygote is brought about by an activity synthesized only by plus gametes and degradation of FUS1 is brought about by an activity synthesized only by minus gametes. A related model is suggested by a novel regulatory mechanism for regulating transcription of zygote-specific genes in Chlamydomonas uncovered by work from our laboratory (Zhao et al, 2001) and the Goodenough laboratory (Lee et al, 2008). Each gamete brings a mating type-specific homeodomain protein to the zygote cytoplasm and only the heterodimer formed from the interaction between the two can activate the zygote developmental pathway.…”

Section: The Rapid Degradation Of Fus1 and Hap2 Is Specific To Zygotesmentioning

confidence: 99%

Membrane fusion triggers rapid degradation of two gamete-specific, fusion-essential proteins in a membrane block to polygamy inChlamydomonas

Liu

Misamore

Snell³

2010

Development

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SUMMARYThe plasma membranes of gametes are specialized for fusion, yet, once fusion occurs, in many organisms 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. During fertilization in the green alga 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 tested whether Chlamydomonas gamete fusion triggers alterations in FUS1 and HAP2 and renders the plasma membranes of the cells incapable of subsequent fusion. We find that, even though the fusogenic sites support multi-cell adhesions, triploid zygotes are rare, indicating a fusion-triggered block to the membrane fusion reaction. 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.

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Section: Introductionmentioning

confidence: 99%

“…Fertilization is a rapid process in this organism, and zygotes occur within minutes after mtϩ and mtϪ gametes are mixed. Zygote formation is accompanied by inactivation and loss of flagellar agglutinins (the Chlamydomonas equivalent to a block to polyspermy) and activation of transcription of new genes as the zygote developmental pathway commences (Goodenough, 1991;Goodenough et al, 1995b;Pan and Snell, 2000b;Zhao et al, 2001).In studies to delineate the cellular and molecular mechanisms of gamete fusion in Chlamydomonas, we developed methods for isolating and characterizing activated plus mating structures, the fertilization tubules (Wilson et al, 1997).We showed that the isolated organelles retained their ability to bind to mating structures on activated mtϪ gametes. An important next step in dissecting the molecular mechanisms for fusion in Chlamydomonas will be to identify proteins on the fertilization tubule responsible for the functions of the organelle.…”

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confidence: 99%

TheChlamydomonasFus1 Protein Is Present on the Mating TypeplusFusion Organelle and Required for a Critical Membrane Adhesion Event during Fusion withminusGametes

Misamore

Gupta

Snell³

2003

MBoC

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The molecular mechanisms of the defining event in fertilization, gamete fusion, remain poorly understood. The FUS1 gene in the unicellular, biflagellated green alga Chlamydomonas is one of the few sex-specific eukaryotic genes shown by genetic analysis to be essential for gamete fusion during fertilization. In Chlamydomonas, adhesion and fusion of the plasma membranes of activated mtϩ and mtϪ gametes is accomplished via specialized fusion organelles called mating structures. Herein, we identify the endogenous Fus1 protein, test the idea that Fus1 is at the site of fusion, and identify the step in fusion that requires Fus1. Our results show that Fus1 is a ϳ95-kDa protein present on the external surface of both unactivated and activated mtϩ gametes. Bioassays indicate that adhesion between mating type plus and mating type minus fusion organelles requires Fus1 and that Fus1 is functional only after gamete activation. Finally, immunofluorescence demonstrates that the Fus1 protein is present as an apical patch on unactivated gametes and redistributes during gamete activation over the entire surface of the microvillous-like activated plus mating structure, the fertilization tubule. Thus, Fus1 is present on mtϩ gametes at the site of cell-cell fusion and essential for an early step in the fusion process. INTRODUCTIONGamete fusion defines the beginning of a new organism in all sexual species. In most organisms, the events that precede fusion have been well characterized at the cellular level (Snell and White, 1996;Wassarman et al., 2001;Primakoff and Myles, 2002). Initial cell-cell interactions between sperm surface proteins and extracellular matrix molecules on the egg trigger activation of the sperm and exposure of previously cryptic regions of the plasma membrane proposed to be involved in gamete fusion. Once the sperm has made its way to the egg plasma membrane, the membranes of the two gametes interact more intimately, finally bringing about gamete fusion. Several sperm and egg molecules implicated in activation of the sperm have been identified, and we know much about the morphological events that accompany gamete fusion (Yanagimachi, 1994). On the other hand, little is known about the molecular mechanisms that underlie the late steps in fertilization, when the plasma membranes of the interacting gametes adhere and fuse (for review, see Primakoff and Myles, 2002). In the absence of any purely eukaryotic systems in which bona fide fusion proteins have been identified, the best models for fusion of the external plasma membrane of cells have come from studies of fusion of viruses with their eukaryotic target cells (White, 1996;Eckert and Kim, 2001). In these systems, a viral transmembrane surface protein interacts with a receptor in the host cell plasma membrane, leading to docking of the virus particle on the cell surface. Subsequent conformational changes in the interacting proteins finally lead to complete fusion (Dimitrov, 2000;Malashkevich et al., 2001;Mayer, 2001).A small number of eukaryotic genes has been sho...

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Ectopic expression of a Chlamydomonas mt+-specific homeodomain protein in mt− gametes initiates zygote development without gamete fusion

Cited by 64 publications

References 48 publications

Seaweed reproductive biology: environmental and genetic controls

Seaweed reproductive biology: environmental and genetic controls

Membrane fusion triggers rapid degradation of two gamete-specific, fusion-essential proteins in a membrane block to polygamy inChlamydomonas

TheChlamydomonasFus1 Protein Is Present on the Mating TypeplusFusion Organelle and Required for a Critical Membrane Adhesion Event during Fusion withminusGametes

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