Title: A Noncanonical Hippo Pathway Regulates Spindle Disassembly and Cytokinesis During Meiosis in Saccharomyces cerevisiae
Abstract
Meiosis in the budding yeast Saccharomyces cerevisiae is used to create haploid yeast spores from a diploid mother cell. During meiosis II, cytokinesis occurs by closure of the prospore membrane, a membrane that initiates at the spindle pole body and grows to surround each of the haploid meiotic products. Timely prospore membrane closure requires SPS1, which encodes an STE20 family GCKIII kinase. To identify genes that may activate SPS1, we utilized a histone phosphorylation defect of sps1 mutants to screen for genes with a similar phenotype and found that cdc15 shared this phenotype. CDC15 encodes a Hippo-like kinase that is part of the mitotic exit network. We find that Sps1 complexes with Cdc15, that Sps1 phosphorylation requires Cdc15, and that CDC15 is also required for timely prospore membrane closure. We also find that SPS1, like CDC15, is required for meiosis II spindle disassembly and sustained anaphase II release of Cdc14 in meiosis. However, the NDR-kinase complex encoded by DBF2/DBF20MOB1 which functions downstream of CDC15 in mitotic cells, does not appear to play a role in spindle disassembly, timely prospore membrane closure, or sustained anaphase II Cdc14 release. Taken together, our results suggest that the mitotic exit network is rewired for exit from meiosis II, such that SPS1 replaces the NDR-kinase complex downstream of CDC15.
Seitz, Brian C.; Mucelli, Xheni; Majano, Maira; Wallis, Zoey; Dodge, Ashley C.; Carmona, Catherine; Durant, Matthew; Maynard, Sharra; Huang, Linda S.(
, Molecular Biology of the Cell)
Bloom, Kerry
(Ed.)
AMA1 and SPS1 control distinct aspects of meiosis II spindle disassembly, with AMA1 affecting the loss of Ase1 and Cin8 during meiosis II spindle disassembly, while SPS1 affects Bim1. The Anaphase Promoting Complex and meiotic/mitotic exit pathways seem to regulate similar targets in meiosis as mitosis, despite utilizing meiosis-specific regulators in those pathways.
Durant, Matthew; Roesner, Joseph M.; Mucelli, Xheni; Slubowski, Christian J.; Klee, Erin; Seitz, Brian C.; Wallis, Zoey; Huang, Linda S.(
, Journal of Fungi)
During sporulation in the budding yeast Saccharomyces cerevisiae, proper development of the prospore membrane is necessary for the formation of viable spores. The prospore membrane will eventually become the plasma membrane of the newly formed haploid spore and also serves as the template for the deposition of the spore wall. The prospore membrane is generated de novo during meiosis II and the growing edge of the prospore membrane is associated with the Leading Edge Protein (LEP) complex. We find that the Smk1 MAP kinase, along with its activator Ssp2, transiently localizes with the LEP during late meiosis II. SSP2 is required for the leading edge localization of Smk1; this localization is independent of the activation state of Smk1. Like other LEP components, the localization of Smk1 at the leading edge also depends on Ady3. Although prospore membrane development begins normally in smk1 and ssp2 mutants, late prospore membrane formation is disrupted, with the formation of ectopic membrane compartments. Thus, MAP kinase signaling plays an important role in the formation of the prospore membrane.
Faithful chromosome segregation is required for both mitotic and meiotic cell divisions and is regulated by multiple mechanisms including the anaphase‐promoting complex/cyclosome (APC/C), which is the largest known E3 ubiquitin‐ligase complex and has been implicated in regulating chromosome segregation in both mitosis and meiosis in animals. However, the role of theAPC/C during plant meiosis remains largely unknown. Here, we show that ArabidopsisAPC8is required for male meiosis.
We used a combination of genetic analyses, cytology and immunolocalisation to define the function of AtAPC8 in male meiosis.
Meiocytes fromapc8‐1plants exhibit several meiotic defects including improper alignment of bivalents at metaphase I, unequal chromosome segregation during anaphaseII, and subsequent formation of polyads. Immunolocalisation using an antitubulin antibody showed thatAPC8 is required for normal spindle morphology. We also observed mitotic defects inapc8‐1,including abnormal sister chromatid segregation and microtubule morphology.
Our results demonstrate that ArabidopsisAPC/C is required for meiotic chromosome segregation and thatAPC/C‐mediated regulation of meiotic chromosome segregation is a conserved mechanism among eukaryotes.
Weiss, Jodi D.; McVey, Shelby L.; Stinebaugh, Sarah E.; Sullivan, Caroline F.; Dawe, R. Kelly; Nannas, Natalie J.(
, International Journal of Molecular Sciences)
The success of an organism is contingent upon its ability to faithfully pass on its genetic material. In the meiosis of many species, the process of chromosome segregation requires that bipolar spindles be formed without the aid of dedicated microtubule organizing centers, such as centrosomes. Here, we describe detailed analyses of acentrosomal spindle assembly and disassembly in time-lapse images, from live meiotic cells of Zea mays. Microtubules organized on the nuclear envelope with a perinuclear ring structure until nuclear envelope breakdown, at which point microtubules began bundling into a bipolar form. However, the process and timing of spindle assembly was highly variable, with frequent assembly errors in both meiosis I and II. Approximately 61% of cells formed incorrect spindle morphologies, with the most prevalent being tripolar spindles. The erroneous spindles were actively rearranged to bipolar through a coalescence of poles before proceeding to anaphase. Spindle disassembly occurred as a two-state process with a slow depolymerization, followed by a quick collapse. The results demonstrate that maize meiosis I and II spindle assembly is remarkably fluid in the early assembly stages, but otherwise proceeds through a predictable series of events.
During meiotic prophase I, accurate segregation of homologous chromosomes requires the establishment of chromosomes with a meiosis-specific architecture. The sister chromatid cohesin complex and the enzyme Topoisomerase II (TOP-2) are important components of meiotic chromosome architecture, but the relationship of these proteins in the context of meiotic chromosome segregation is poorly defined. Here, we analyzed the role of TOP-2 in the timely release of the sister chromatid cohesin subunit REC-8 during spermatogenesis and oogenesis of Caenorhabditis elegans. We show that there is a different requirement for TOP-2 in meiosis of spermatogenesis and oogenesis. The loss-of-function mutation top-2(it7) results in premature REC-8 removal in spermatogenesis, but not oogenesis. This correlates with a failure to maintain the HORMA-domain proteins HTP-1 and HTP-2 (HTP-1/2) on chromosome axes at diakinesis and mislocalization of the downstream components that control REC-8 release including Aurora B kinase. In oogenesis, top-2(it7) causes a delay in the localization of Aurora B to oocyte chromosomes but can be rescued through premature activation of the maturation promoting factor via knockdown of the inhibitor kinase WEE-1.3. The delay in Aurora B localization is associated with an increase in the length of diakinesis bivalents and wee-1.3 RNAi mediated rescue of Aurora B localization in top-2(it7) is associated with a decrease in diakinesis bivalent length. Our results imply that the sex-specific effects of TOP-2 on REC-8 release are due to differences in the temporal regulation of meiosis and chromosome structure in late prophase I in spermatogenesis and oogenesis.
Paulissen, Scott M, Hunt, Cindy A, Seitz, Brian C, Slubowski, Christian J, Yu, Yao, Mucelli, Xheni, Truong, Dang, Wallis, Zoey, Nguyen, Hung T, Newman-Toledo, Shayla, Neiman, Aaron M, and Huang, Linda S. A Noncanonical Hippo Pathway Regulates Spindle Disassembly and Cytokinesis During Meiosis in Saccharomyces cerevisiae. Retrieved from https://par.nsf.gov/biblio/10497114. Genetics 216.2 Web. doi:10.1534/genetics.120.303584.
Paulissen, Scott M, Hunt, Cindy A, Seitz, Brian C, Slubowski, Christian J, Yu, Yao, Mucelli, Xheni, Truong, Dang, Wallis, Zoey, Nguyen, Hung T, Newman-Toledo, Shayla, Neiman, Aaron M, & Huang, Linda S. A Noncanonical Hippo Pathway Regulates Spindle Disassembly and Cytokinesis During Meiosis in Saccharomyces cerevisiae. Genetics, 216 (2). Retrieved from https://par.nsf.gov/biblio/10497114. https://doi.org/10.1534/genetics.120.303584
Paulissen, Scott M, Hunt, Cindy A, Seitz, Brian C, Slubowski, Christian J, Yu, Yao, Mucelli, Xheni, Truong, Dang, Wallis, Zoey, Nguyen, Hung T, Newman-Toledo, Shayla, Neiman, Aaron M, and Huang, Linda S.
"A Noncanonical Hippo Pathway Regulates Spindle Disassembly and Cytokinesis During Meiosis in Saccharomyces cerevisiae". Genetics 216 (2). Country unknown/Code not available: Genetics Society of America. https://doi.org/10.1534/genetics.120.303584.https://par.nsf.gov/biblio/10497114.
@article{osti_10497114,
place = {Country unknown/Code not available},
title = {A Noncanonical Hippo Pathway Regulates Spindle Disassembly and Cytokinesis During Meiosis in Saccharomyces cerevisiae},
url = {https://par.nsf.gov/biblio/10497114},
DOI = {10.1534/genetics.120.303584},
abstractNote = {Abstract Meiosis in the budding yeast Saccharomyces cerevisiae is used to create haploid yeast spores from a diploid mother cell. During meiosis II, cytokinesis occurs by closure of the prospore membrane, a membrane that initiates at the spindle pole body and grows to surround each of the haploid meiotic products. Timely prospore membrane closure requires SPS1, which encodes an STE20 family GCKIII kinase. To identify genes that may activate SPS1, we utilized a histone phosphorylation defect of sps1 mutants to screen for genes with a similar phenotype and found that cdc15 shared this phenotype. CDC15 encodes a Hippo-like kinase that is part of the mitotic exit network. We find that Sps1 complexes with Cdc15, that Sps1 phosphorylation requires Cdc15, and that CDC15 is also required for timely prospore membrane closure. We also find that SPS1, like CDC15, is required for meiosis II spindle disassembly and sustained anaphase II release of Cdc14 in meiosis. However, the NDR-kinase complex encoded by DBF2/DBF20MOB1 which functions downstream of CDC15 in mitotic cells, does not appear to play a role in spindle disassembly, timely prospore membrane closure, or sustained anaphase II Cdc14 release. Taken together, our results suggest that the mitotic exit network is rewired for exit from meiosis II, such that SPS1 replaces the NDR-kinase complex downstream of CDC15.},
journal = {Genetics},
volume = {216},
number = {2},
publisher = {Genetics Society of America},
author = {Paulissen, Scott M and Hunt, Cindy A and Seitz, Brian C and Slubowski, Christian J and Yu, Yao and Mucelli, Xheni and Truong, Dang and Wallis, Zoey and Nguyen, Hung T and Newman-Toledo, Shayla and Neiman, Aaron M and Huang, Linda S},
}
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