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• W2561345641 abstract "Howard Hughes Medical InstituteMassachusetts Institute of TechnologyCambridge, MA 02139SummaryAcell’sdecisiontoundergomeiosisisregulatedbymultiplesignals. In budding yeast, these signals include mating-typestatus, nutrient starvation, and respiration; the need for res-piration is often manifested as a requirement for a nonfer-mentable carbon source. We have dissected the roles ofrespiration and carbon source in promoting entry into themeiotic program. This analysis revealed that respiration isneeded throughout meiosis but a nonfermentable carbonsource is necessary only prior to the meiotic nuclear divi-sions. Anonfermentablecarbonsource servesseveralrolesduring the early stages of meiosis. It is required for PolIItranscription, DNA replication, and recombination. Finally,although the global downregulation of transcription andlack of DNA replication in nonrespiring cells could be duetoalackofenergy,weshowthattheinabilitytoinducegenesinitiating entry into the meiotic program is not. We proposethataseparaterespiration-sensingpathwaygovernsmeioticentry.ResultsA Nonfermentable Carbon Source is Requiredfor Execution of the Meiotic ProgramWe first examined which steps of meiosis require an exoge-nous carbonsource. Cellswere grown in YPA (see Experimen-tal Procedures, available online) and then transferred intostandard sporulation medium containing potassium acetate(KAc) or carbon-free medium containing potassium chloride(KCl), in which cells can only oxidize internal stores of biomol-ecules but cannot derive energy from the medium. As ex-pected [1], cells sporulated efficiently in KAc but not in KCl(Figure 1A). We next tested whether induction of the earlymeiotic genes allowed sporulation in KCl by utilizing a strainbearing an allele of the protein kinase Ime2, ime2-as, whichcan be reversibly inhibited by the ATP analog 1-NA-PP1 [2].In the presence of the inhibitor, IME1, a transcription factorgoverning entry into meiosis [3], and other early meiotic genesareexpressedbutpremeioticDNAreplicationandsubsequentmeiotic events are not initiated [2] (compare also Figures S1Aand S3A). When the inhibitor was washed out of KAc cultures,cells sporulated efficiently only when released into KAc,whereas tetranucleate formation was decreased by morethan 7-fold in cells released into KCl medium (Figure 1B).These results show that a nonfermentable carbon source isneeded for progression through meiosis after induction ofthe early meiotic genes.To determine whether Ime1 production was affected bythe absence of a carbon source, we compared Ime1 proteinlevels between cells incubated in KAc and KCl. Ime1 accu-mulated to similar levels under both conditions (Figure 1C),indicating that cells did not fail to undergo meiosis in KClbecause of defects in Ime1 expression. Accordingly, pre-meiotic DNA replication occurred in KCl after prolonged(10 hr) incubation (Figure S1B). Ime1 induction was also ob-served when cells were transferred to KAc or KCl mediumafter pregrowth in rich (YPD) medium, in which Ime1 expres-sion is minimal (Figure 1D). Treatment of cells with sodiumazide, an inhibitor of cytochrome C oxidase, preventedIme1 production and sporulation (Figures 1A and 1C). Theseresults indicate that respiration, but not a carbon source, isneeded for Ime1 production. A nonfermentable carbonsource, however, is required at the time of or after Ime2function.The Meiotic Nuclear Divisions Require Respirationbut not a Carbon SourceNext,wedeterminedwhetheranonfermentablecarbonsourcewas needed after the completion of premeiotic DNA replica-tion and recombination. To this end, we utilized a strain bear-ing an estrogen-inducible allele of NDT80 [2], a meiotictranscription factor that induces the middle meiotic genes[4].IntheabsenceofNDT80induction,cellsarrestinprophaseI prior to the first meiotic nuclear division [5, 6]. After arrest atthendt80DblockinKAc,cellsweresimultaneouslytransferredto carbon-free (KCl) medium and NDT80 was induced. Cellsunderwent both meiotic divisions (Figure 1E, KAc and KClbars) and formed spores (data not shown) as efficiently asdid a control sample in which NDT80 was induced in KAc.This finding indicates that meiotic divisions can occur in theabsence of an exogenous energy source. Prophase-arrestedcells were not irreversibly committed to meiosis, given thattransfer to rich (YPD) medium at the time of NDT80 inductioncaused cells to resume vegetative growth and no meioticnuclear divisions occurred (Figure 1F). This ability to ‘‘returnto growth’’ agrees with previous findings that commitment tomeiosis occurs at the time of the first nuclear division [1, 7].Ourresults indicate that prophase I-arrested cells do not com-plete sporulation by default upon relief of arrest and that allrequirements for a nonfermentable carbon source are fulfilledby the end of prophase I.We then monitored meiosis in the presence of sodium azideto test whether prophase-arrested cells released into KClmedium oxidized internal stores of biomolecules to fuel thetwo nuclear divisions. Azide blocked sporulation whenadded to cultures either before or after NDT80 induction (Fig-ures 1A and 1E) but did not significantly affect cell viability(Figure S2A), indicating that the failure to undergo the meioticdivisions in the presence of azide results from mitochondrialinhibition and not cell death. Furthermore, addition of dinitro-phenol, an ionophore that dissipates proton gradients, to KClcultures one hour prior to NDT80 induction mimicked theeffectsofazide(Figure1G).Athirdinhibitor, oligomycin,whichblocks mitochondrial ATP synthase, appeared only partially" @default.
• W2561345641 created "2017-01-06" @default.
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• W2561345641 date "2008-01-01" @default.
• W2561345641 modified "2023-09-27" @default.
• W2561345641 title "Report Control of Meiosis by Respiration" @default.
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