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protein coding gene - mmi1 (SPCC736.12c) - nucleur exosome adaptor Mmi1

Gene summary

Standard name
mmi1
Systematic ID
SPCC736.12c
Product
nucleur exosome adaptor Mmi1
Organism
Schizosaccharomyces pombe (fission yeast)
UniProt ID
O74958
ORFeome ID
44/44H11
Characterisation status
biological role published
Feature type
mRNA gene
Genomic location
chromosome III: 337088..340112 reverse strand

Annotation

Comment

PBO:0091907 - a disordered region N-terminal to the YTH domain stabilizes RNA binding, and becomes more ordered upon binding

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GO biological process

GO:0110064 - lncRNA catabolic process

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GO:0061157 - mRNA destabilization

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GO:0180036 - nuclear lncRNA surveillance

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GO:0033621 - nuclear mRNA surveillance of meiosis-specific transcripts

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GO:0071031 - nuclear mRNA surveillance of mRNA 3'-end processing

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GO:0071030 - nuclear mRNA surveillance of spliceosomal pre-mRNA splicing

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GO:0071039 - nuclear polyadenylation-dependent CUT catabolic process

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GO:0071027 - nuclear RNA surveillance

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GO:1902801 - regulation of siRNA-independent facultative heterochromatin formation

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GO:0043628 - regulatory ncRNA 3'-end processing

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GO:0031047 - regulatory ncRNA-mediated gene silencing

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GO:1902794 - siRNA-independent facultative heterochromatin formation

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GO cellular component

GO:0000785 - chromatin

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GO:0005737 - cytoplasm

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GO:1990342 - heterochromatin island

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GO:0033620 - Mei2 nuclear dot complex

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GO:1990251 - nuclear exosome focus

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GO:0005634 - nucleus

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GO molecular function

GO:1905762 - CCR4-NOT complex binding

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GO:0106222 - lncRNA binding

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GO:0003729 - mRNA binding

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GO:1990247 - N6-methyladenosine-containing RNA reader activity

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GO:0036002 - pre-mRNA binding

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GO:0097157 - pre-mRNA intronic binding

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GO:0005515 - protein binding

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GO:0140517 - protein-RNA adaptor activity

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GO:0003723 - RNA binding

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Modification

MOD:00046 - O-phospho-L-serine

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MOD:00047 - O-phospho-L-threonine

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MOD:00048 - O4'-phospho-L-tyrosine

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MOD:00696 - phosphorylated residue

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MOD:01148 - ubiquitinylated lysine

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Multi-locus phenotype

FYPO:0004481 - abolished cell population growth at high temperature

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Genotypes:

FYPO:0000082 - decreased cell population growth at high temperature

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Genotypes:

FYPO:0000080 - decreased cell population growth at low temperature

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Genotypes:

FYPO:0000577 - increased gene silencing

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Genotypes:

FYPO:0002173 - increased level of meiotic gene mRNA during vegetative growth

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Genotypes:

FYPO:0001908 - increased pre-mRNA level

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Genotypes:

FYPO:0001327 - increased protein level during vegetative growth

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Genotypes:

FYPO:0001890 - increased RNA level

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Genotypes:

FYPO:0000825 - increased RNA level during vegetative growth

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Genotypes:

FYPO:0002061 - inviable vegetative cell population

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Genotypes:

FYPO:0007281 - normal level of meiotic gene mRNA during vegetative growth

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Genotypes:

FYPO:0003059 - normal RNA localization to chromatin

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Genotypes:

FYPO:0001234 - slow vegetative cell population growth

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Genotypes:

FYPO:0002060 - viable vegetative cell population

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Genotypes:

Qualitative gene expression

PomGeneEx:0000019 - protein level decreased

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PomGeneEx:0000011 - RNA level increased

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Quantitative gene expression

PBO:0006310 - protein level

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PBO:0011963 - RNA level

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Single locus phenotype

FYPO:0000625 - abnormal premeiotic DNA replication

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Genotypes:

FYPO:0008155 - abnormal regulatory lncRNA 3'-end processing

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Genotypes:

FYPO:0004851 - abnormal RNA metabolic process

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Genotypes:

FYPO:0004811 - abnormal termination of RNA polymerase II transcription

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Genotypes:

FYPO:0005861 - abolished CCR4-NOT complex binding

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Genotypes:

FYPO:0007530 - abolished histone H3-K9 dimethylation at heterochromatin island at meiotic gene during vegetative growth

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Genotypes:

FYPO:0005862 - abolished MTREC complex binding

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Genotypes:

FYPO:0007215 - abolished protein localization to chromatin at lncRNA gene

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Genotypes:

FYPO:0007214 - abolished protein localization to heterochromatin island

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Genotypes:

FYPO:0000705 - abolished protein-protein interaction

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Genotypes:

FYPO:0002133 - abolished protein-RNA interaction

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Genotypes:

FYPO:0001045 - decreased acid phosphatase activity

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Genotypes:

FYPO:0000082 - decreased cell population growth at high temperature

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Genotypes:

FYPO:0000080 - decreased cell population growth at low temperature

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Genotypes:

FYPO:0000303 - decreased conjugation frequency

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Genotypes:

FYPO:0006269 - decreased histone H3-K9 dimethylation at protein coding gene during vegetative growth

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Genotypes:

FYPO:0003230 - decreased histone H3-K9 methylation at heterochromatin island during vegetative growth

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Genotypes:

FYPO:0000708 - decreased mating efficiency

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Genotypes:

FYPO:0000835 - decreased protein level

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Genotypes:

FYPO:0006612 - decreased protein localization to chromatin at transcription termination site

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Genotypes:

FYPO:0007280 - decreased protein localization to nuclear exosome focus

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Genotypes:

FYPO:0002134 - decreased protein-RNA interaction

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Genotypes:

FYPO:0000826 - decreased RNA level

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Genotypes:

FYPO:0000584 - decreased sporulation frequency

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Genotypes:

FYPO:0003053 - increased homologous chromosome pairing at cis-acting homologous chromosome pairing region

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Genotypes:

FYPO:0002960 - increased level of DSR-containing meiotic gene mRNA during vegetative growth

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Genotypes:

FYPO:0002173 - increased level of meiotic gene mRNA during vegetative growth

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Genotypes:

FYPO:0000836 - increased protein level

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Genotypes:

FYPO:0001327 - increased protein level during vegetative growth

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Genotypes:

FYPO:0001890 - increased RNA level

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Genotypes:

FYPO:0000825 - increased RNA level during vegetative growth

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Genotypes:

FYPO:0000316 - inviable after spore germination

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Genotypes:

FYPO:0002148 - inviable after spore germination, multiple cell divisions, abnormal morphology

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Genotypes:

FYPO:0002061 - inviable vegetative cell population

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Genotypes:

FYPO:0005863 - loss of punctate nuclear protein localization

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Genotypes:

FYPO:0006996 - normal antisense RNA level

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Genotypes:

FYPO:0002336 - normal chromatin silencing at silent mating-type cassette

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Genotypes:

FYPO:0000833 - normal protein level during vegetative growth

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Genotypes:

FYPO:0000838 - normal protein localization to nucleus during vegetative growth

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Genotypes:

FYPO:0000703 - normal protein-protein interaction

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Genotypes:

FYPO:0002357 - normal protein-RNA interaction

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Genotypes:

FYPO:0004910 - normal punctate nuclear protein localization

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Genotypes:

FYPO:0001317 - normal RNA level during vegetative growth

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Genotypes:

FYPO:0002085 - normal vegetative cell growth

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Genotypes:

FYPO:0001357 - normal vegetative cell population growth

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Genotypes:

FYPO:0000783 - protein mislocalized to cytoplasm during vegetative growth

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Genotypes:

FYPO:0006862 - RNA mislocalized to cytoplasm during vegetative growth

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Genotypes:

FYPO:0006821 - slow vegetative cell growth

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Genotypes:

Taxonomic conservation

PBO:0011065 - conserved in eukaryotes

PBO:0011071 - conserved in eukaryotes only

PBO:0011064 - conserved in fungi

PBO:0011069 - conserved in metazoa

PBO:0011070 - conserved in vertebrates

PBO:0006222 - predominantly single copy (one to one)

Protein features

IDNameInterPro nameDB name
PF04146YTHYTH_domainPFAM
cd21134YTHYTH_domainCDD
PS50882YTHYTH_domainPROSITE_PROFILES
G3DSA:3.10.590.10ph1033 like domainsGENE3D
PTHR12357YTH YT521-B HOMOLOGY DOMAIN-CONTAININGYTH_protPANTHER
mobidb-lite-Disorderdisorder_predictionMOBIDB-Disorder
mobidb-lite-Low-complexitydisorder_predictionMOBIDB-Low-complexity
mobidb-lite-Polardisorder_predictionMOBIDB-Polar
mobidb-lite-Polyampholytedisorder_predictionMOBIDB-Polyampholyte

Orthologs

References / Literature

PMID:26804377 - The architecture of the Schizosaccharomyces pombe CCR4-NOT complex.
Ukleja M et al. Nat Commun 2016 Jan 25;7:10433
PMID:16823445 - Selective elimination of messenger RNA prevents an incidence of untimely meiosis.
Harigaya Y et al. Nature 2006 Jul 06;442(7098):45-50
PMID:20512112 - Importance of polyadenylation in the selective elimination of meiotic mRNAs in growing S. pombe cells.
Yamanaka S et al. EMBO J 2010 Jul 07;29(13):2173-81
PMID:33536434 - A scaffold lncRNA shapes the mitosis to meiosis switch.
Andric V et al. Nat Commun 2021 Feb 03;12(1):770
PMID:37970674 - SUMOylation regulates Lem2 function in centromere clustering and silencing.
Strachan J et al. J Cell Sci 2023 Dec 01;136(23)
PMID:26167880 - SR protein kinases promote splicing of nonconsensus introns.
Lipp JJ et al. Nat Struct Mol Biol 2015 Aug;22(8):611-7
PMID:39705284 - Proteomic and phosphoproteomic analyses reveal that TORC1 is reactivated by pheromone signaling during sexual reproduction in fission yeast.
Bérard M et al. PLoS Biol 2024 Dec 20;22(12):e3002963
PMID:24763107 - Absolute proteome and phosphoproteome dynamics during the cell cycle of Schizosaccharomyces pombe (Fission Yeast).
Carpy A et al. Mol Cell Proteomics 2014 Aug;13(8):1925-36
PMID:28218250 - Chromatin remodeller Fun30 Fft3 induces nucleosome disassembly to facilitate RNA polymerase II elongation.
Lee J et al. Nat Commun 2017 Feb 20;8:14527
PMID:24920274 - Meiotic long non-coding meiRNA accumulates as a dot at its genetic locus facilitated by Mmi1 and plays as a decoy to lure Mmi1.
Shichino Y et al. Open Biol 2014 Jun;4(6):140022
PMID:31269446 - CPF Recruitment to Non-canonical Transcription Termination Sites Triggers Heterochromatin Assembly and Gene Silencing.
Vo TV et al. Cell Rep 2019 Jul 02;28(1):267-281.e5
PMID:22046364 - The fission yeast RNA binding protein Mmi1 regulates meiotic genes by controlling intron specific splicing and polyadenylation coupled RNA turnover.
Chen HM et al. PLoS One 2011;6(10):e26804
PMID:19547744 - Evolution of phosphoregulation: comparison of phosphorylation patterns across yeast species.
Beltrao P et al. PLoS Biol 2009 Jun 16;7(6):e1000134
PMID:18257517 - Phosphoproteome analysis of fission yeast.
Wilson-Grady JT et al. J Proteome Res 2008 Mar;7(3):1088-97
PMID:30726745 - Fission Yeast NDR/LATS Kinase Orb6 Regulates Exocytosis via Phosphorylation of the Exocyst Complex.
Tay YD et al. Cell Rep 2019 Feb 05;26(6):1654-1667.e7
PMID:31883795 - Positioning Heterochromatin at the Nuclear Periphery Suppresses Histone Turnover to Promote Epigenetic Inheritance.
Holla S et al. Cell 2020 Jan 09;180(1):150-164.e15
PMID:39476757 - Characterization of Ksg1 protein kinase-dependent phosphoproteome in the fission yeast S. pombe.
Cipak L et al. Biochem Biophys Res Commun 2024 Oct 25;736:150895
PMID:31072933 - Suppressor screening reveals common kleisin-hinge interaction in condensin and cohesin, but different modes of regulation.
Xu X et al. Proc Natl Acad Sci U S A 2019 May 28;116(22):10889-10898
PMID:32012158 - Meiotic gene silencing complex MTREC/NURS recruits the nuclear exosome to YTH-RNA-binding protein Mmi1.
Shichino Y et al. PLoS Genet 2020 Feb;16(2):e1008598
PMID:25428589 - Long non-coding RNA-mediated transcriptional interference of a permease gene confers drug tolerance in fission yeast.
Ard R et al. Nat Commun 2014 Nov 27;5:5576
PMID:31064814 - Proximity-dependent biotinylation mediated by TurboID to identify protein-protein interaction networks in yeast.
Larochelle M et al. J Cell Sci 2019 May 31;132(11)
PMID:21436456 - Clr4/Suv39 and RNA quality control factors cooperate to trigger RNAi and suppress antisense RNA.
Zhang K et al. Science 2011 Mar 25;331(6024):1624-7
PMID:26670050 - Regulation of mRNA Levels by Decay-Promoting Introns that Recruit the Exosome Specificity Factor Mmi1.
Kilchert C et al. Cell Rep 2015 Dec 22;13(11):2504-2515
GO_REF:0000033 - Annotation inferences using phylogenetic trees
PMID:27851962 - Reconstitution of Targeted Deadenylation by the Ccr4-Not Complex and the YTH Domain Protein Mmi1.
Stowell JAW et al. Cell Rep 2016 Nov 15;17(8):1978-1989
PMID:20473289 - Analysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe.
Kim DU et al. Nat Biotechnol 2010 Jun;28(6):617-623
PMID:27984725 - CDK Substrate Phosphorylation and Ordering the Cell Cycle.
Swaffer MP et al. Cell 2016 Dec 15;167(7):1750-1761.e16
PMID:28735863 - Structural insights into the specific recognition of DSR by the YTH domain containing protein Mmi1.
Wu B et al. Biochem Biophys Res Commun 2017 Sep 16;491(2):310-316
PMID:16823372 - ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe.
Matsuyama A et al. Nat Biotechnol 2006 Jul;24(7):841-7
PMID:20622014 - Negative regulation of meiotic gene expression by the nuclear poly(a)-binding protein in fission yeast.
St-André O et al. J Biol Chem 2010 Sep 03;285(36):27859-68
PMID:33574613 - TOR targets an RNA processing network to regulate facultative heterochromatin, developmental gene expression and cell proliferation.
Wei Y et al. Nat Cell Biol 2021 Mar;23(3):243-256
PMID:21511999 - Comparative functional genomics of the fission yeasts.
Rhind N et al. Science 2011 May 20;332(6032):930-6
PMID:26631744 - Conserved factor Dhp1/Rat1/Xrn2 triggers premature transcription termination and nucleates heterochromatin to promote gene silencing.
Chalamcharla VR et al. Proc Natl Acad Sci U S A 2015 Dec 22;112(51):15548-55
PMID:39367033 - Quantitative proteomics and phosphoproteomics profiling of meiotic divisions in the fission yeast Schizosaccharomyces pombe.
Sivakova B et al. Sci Rep 2024 Oct 04;14(1):23105
PMID:30824696 - Systematic analysis reveals the prevalence and principles of bypassable gene essentiality.
Li J et al. Nat Commun 2019 Mar 01;10(1):1002
PMID:22645662 - Hexanucleotide motifs mediate recruitment of the RNA elimination machinery to silent meiotic genes.
Yamashita A et al. Open Biol 2012 Mar;2(3):120014
PMID:27298342 - Identification of S-phase DNA damage-response targets in fission yeast reveals conservation of damage-response networks.
Willis NA et al. Proc Natl Acad Sci U S A 2016 Jun 28;113(26):E3676-85
PMID:24493644 - lncRNA recruits RNAi and the exosome to dynamically regulate pho1 expression in response to phosphate levels in fission yeast.
Shah S et al. Genes Dev 2014 Feb 01;28(3):231-44
PMID:29618061 - Histone deacetylation promotes transcriptional silencing at facultative heterochromatin.
Watts BR et al. Nucleic Acids Res 2018 Jun 20;46(11):5426-5440
PMID:29695507 - A low-complexity region in the YTH domain protein Mmi1 enhances RNA binding.
Stowell JAW et al. J Biol Chem 2018 Jun 15;293(24):9210-9222
PMID:29996109 - Quantitative Phosphoproteomics Reveals the Signaling Dynamics of Cell-Cycle Kinases in the Fission Yeast Schizosaccharomyces pombe.
Swaffer MP et al. Cell Rep 2018 Jul 10;24(2):503-514
PMID:32415063 - Conserved protein Pir2 ARS2 mediates gene repression through cryptic introns in lncRNAs.
Thillainadesan G et al. Nat Commun 2020 May 15;11(1):2412
PMID:38833506 - A systematic screen identifies Saf5 as a link between splicing and transcription in fission yeast.
Borao S et al. PLoS Genet 2024 Jun 04;20(6):e1011316
PMID:30257894 - mmi1 and rep2 mRNAs are novel RNA targets of the Mei2 RNA-binding protein during early meiosis in Schizosaccharomyces pombe .
Mukherjee K et al. Open Biol 2018 Sep 26;8(9)
PMID:21317872 - Red1 promotes the elimination of meiosis-specific mRNAs in vegetatively growing fission yeast.
Sugiyama T et al. EMBO J 2011 Mar 16;30(6):1027-39
PMID:23297348 - Comprehensive proteomics analysis reveals new substrates and regulators of the fission yeast clp1/cdc14 phosphatase.
Chen JS et al. Mol Cell Proteomics 2013 May;12(5):1074-86
PMID:26412298 - A Degenerate Cohort of Yeast Membrane Trafficking DUBs Mediates Cell Polarity and Survival.
Beckley JR et al. Mol Cell Proteomics 2015 Dec;14(12):3132-41
PMID:30651569 - A conserved dimer interface connects ERH and YTH family proteins to promote gene silencing.
Xie G et al. Nat Commun 2019 Jan 16;10(1):251
PMID:24081329 - Poly(A) tail-mediated gene regulation by opposing roles of Nab2 and Pab2 nuclear poly(A)-binding proteins in pre-mRNA decay.
Grenier St-Sauveur V et al. Mol Cell Biol 2013 Dec;33(23):4718-31
PMID:22582262 - Meiosis-specific noncoding RNA mediates robust pairing of homologous chromosomes in meiosis.
Ding DQ et al. Science 2012 May 11;336(6082):732-6
PMID:24210919 - Mtr4-like protein coordinates nuclear RNA processing for heterochromatin assembly and for telomere maintenance.
Lee NN et al. Cell 2013 Nov 21;155(5):1061-74
PMID:32101745 - Dense Transposon Integration Reveals Essential Cleavage and Polyadenylation Factors Promote Heterochromatin Formation.
Lee SY et al. Cell Rep 2020 Feb 25;30(8):2686-2698.e8
PMID:23697806 - A genome-wide resource of cell cycle and cell shape genes of fission yeast.
Hayles J et al. Open Biol 2013 May 22;3(5):130053
PMID:25720772 - Quantitative phosphoproteomics reveals pathways for coordination of cell growth and division by the conserved fission yeast kinase pom1.
Kettenbach AN et al. Mol Cell Proteomics 2015 May;14(5):1275-87
PMID:23980030 - A novel factor Iss10 regulates Mmi1-mediated selective elimination of meiotic transcripts.
Yamashita A et al. Nucleic Acids Res 2013 Nov;41(21):9680-7
PMID:28765164 - Selective termination of lncRNA transcription promotes heterochromatin silencing and cell differentiation.
Touat-Todeschini L et al. EMBO J 2017 Sep 01;36(17):2626-2641
PMID:23101633 - Quantitative analysis of fission yeast transcriptomes and proteomes in proliferating and quiescent cells.
Marguerat S et al. Cell 2012 Oct 26;151(3):671-83
PMID:28199302 - Untimely expression of gametogenic genes in vegetative cells causes uniparental disomy.
Folco HD et al. Nature 2017 Mar 02;543(7643):126-130
PMID:40185772 - A bifunctional snoRNA with separable activities in guiding rRNA 2'-O-methylation and scaffolding gametogenesis effectors.
Leroy E et al. Nat Commun 2025 Apr 05;16(1):3250
PMID:24713849 - Post-transcriptional regulation of meiotic genes by a nuclear RNA silencing complex.
Egan ED et al. RNA 2014 Jun;20(6):867-81
PMID:25989903 - The fission yeast MTREC complex targets CUTs and unspliced pre-mRNAs to the nuclear exosome.
Zhou Y et al. Nat Commun 2015 May 20;6:7050
PMID:28841135 - Ubiquitination-dependent control of sexual differentiation in fission yeast.
Simonetti F et al. Elife 2017 Aug 25;6
PMID:30321377 - Proteomic profiling and functional characterization of post-translational modifications of the fission yeast RNA exosome.
Telekawa C et al. Nucleic Acids Res 2018 Nov 30;46(21):11169-11183
PMID:27402898 - Relative contributions of the structural and catalytic roles of Rrp6 in exosomal degradation of individual mRNAs.
Mukherjee K et al. RNA 2016 Sep;22(9):1311-9
PMID:26673708 - A novel RNA-binding mode of the YTH domain reveals the mechanism for recognition of determinant of selective removal by Mmi1.
Wang C et al. Nucleic Acids Res 2016 Jan 29;44(2):969-82
PMID:26771498 - A Proteome-wide Fission Yeast Interactome Reveals Network Evolution Principles from Yeasts to Human.
Vo TV et al. Cell 2016 Jan 14;164(1-2):310-323
PMID:26942678 - Enhancer of Rudimentary Cooperates with Conserved RNA-Processing Factors to Promote Meiotic mRNA Decay and Facultative Heterochromatin Assembly.
Sugiyama T et al. Mol Cell 2016 Mar 03;61(5):747-759
PMID:22144463 - RNA elimination machinery targeting meiotic mRNAs promotes facultative heterochromatin formation.
Zofall M et al. Science 2012 Jan 06;335(6064):96-100
PMID:32546512 - Inactivation of fission yeast Erh1 de-represses pho1 expression: evidence that Erh1 is a negative regulator of prt lncRNA termination.
Schwer B et al. RNA 2020 Oct;26(10):1334-1344
PMID:21712547 - Mitotic substrates of the kinase aurora with roles in chromatin regulation identified through quantitative phosphoproteomics of fission yeast.
Koch A et al. Sci Signal 2011 Jun 28;4(179):rs6
PMID:29424342 - YTH-RNA-binding protein prevents deleterious expression of meiotic proteins by tethering their mRNAs to nuclear foci.
Shichino Y et al. Elife 2018 Feb 09;7
PMID:31974447 - Formation of S. pombe Erh1 homodimer mediates gametogenic gene silencing and meiosis progression.
Hazra D et al. Sci Rep 2020 Jan 23;10(1):1034
PMID:33823663 - A TOR (target of rapamycin) and nutritional phosphoproteome of fission yeast reveals novel targets in networks conserved in humans.
Halova L et al. Open Biol 2021 Apr;11(4):200405
PMID:37615341 - Schizosaccharomyces pombe Rtf2 is important for replication fork barrier activity of RTS1 via splicing of Rtf1 .
Budden AM et al. Elife 2023 Aug 24;12
PMID:25774602 - Rapid epigenetic adaptation to uncontrolled heterochromatin spreading.
Wang J et al. Elife 2015 Mar 16;4
PMID:27165520 - Transcription of lncRNA prt, clustered prt RNA sites for Mmi1 binding, and RNA polymerase II CTD phospho-sites govern the repression of pho1 gene expression under phosphate-replete conditions in fission yeast.
Chatterjee D et al. RNA 2016 Jul;22(7):1011-25