atg101

UniProt ID: O13978
Organism: Schizosaccharomyces pombe (strain 972 / ATCC 24843)
Review Status: DRAFT
πŸ“ Provide Detailed Feedback

Gene Description

Atg101 is an essential autophagy initiation factor that functions as a structural stabilizer of Atg13 within the Atg1 kinase complex. The protein contains a HORMA domain that adopts an O-Mad2-like open conformation and forms a constitutive heterodimer with Atg13, stabilizing the intrinsically unstable HORMA domain of Atg13. Atg101 is required for autophagosome formation during nitrogen starvation and is essential for macroautophagy. It localizes to the phagophore assembly site (PAS) upon starvation induction. The protein also contains a conserved WF finger motif responsible for recruiting downstream factors to the autophagosome formation site; a WF-finger mutant retains Atg13 binding yet impairs autophagy, indicating a recruitment function separable from Atg13 stabilization. Although Atg101 is a physical subunit of the Atg1 complex, in S. pombe it is dispensable for Atg1 kinase catalytic activation in vitro (Atg1 activation instead depends on Atg11-mediated dimerization and cis-autophosphorylation), so its core role is adaptor/scaffolding rather than direct kinase regulation. Atg101 was originally identified as mug66 (meiotically up-regulated gene 66) but its core function is in autophagy machinery, not direct meiotic regulation. The meiotic and sporulation phenotypes observed in atg101 mutants are secondary consequences of defective autophagy during nitrogen starvation, which is required for mating and sporulation in S. pombe.

Existing Annotations Review

GO Term Evidence Action Reason
GO:0019901 protein kinase binding
IBA
GO_REF:0000033
MARK AS OVER ANNOTATED
Summary: Atg101 interacts with Atg13, which is part of the Atg1 kinase complex. The Atg1 kinase complex includes the serine/threonine kinase Atg1, and Atg101 is a component of this complex (PMID:26030876, PMID:28976798). However, Atg101 does not directly bind Atg1 kinase; instead it binds the HORMA domain of Atg13. Falcon deep research further shows that in S. pombe Atg101 specifically does NOT bind Atg17 but does bind Atg13's HORMA domain (with Atg1 C-terminal-domain contacts), and that Atg1 kinase autophosphorylation is unchanged in atg101-delta cells (PMID:32909946), so Atg101 is not a direct regulator of the kinase. The actual molecular function is best described as a molecular adaptor that incorporates and stabilizes Atg13 within the complex, not as binding the Atg1 kinase itself.
Reason: The phylogenetically inferred 'protein kinase binding' term implies a direct interaction with a kinase. In S. pombe the experimentally supported binding partner is Atg13 (via HORMA domains), not the Atg1 kinase; Atg101 does not bind Atg17 and is dispensable for Atg1 kinase activation (PMID:32909946). The interaction is therefore better captured by molecular adaptor activity / membership in the Atg1 complex rather than 'protein kinase binding'.
Supporting Evidence:
PMID:28976798
Atg101 interacts with the HORMA domain of Atg13 and this enhances the stability of both proteins.
file:SCHPO/atg101/atg101-deep-research-falcon.md
showed that Atg101 does **not** bind Atg17, but **does** bind Atg13’s HORMA domain and can interact with the Atg1 C‑terminal domain (Atg1CTD), indicating incorporation into the complex via Atg13 and additional contacts.
PMID:32909946
Atg1 from atg13Ξ”, atg17Ξ”, or atg101Ξ” mutant exhibited autophosphorylation activities similar to that of Atg1 from wild type, under both nutrient-rich and nitrogen-starved conditions
file:SCHPO/atg101/atg101-deep-research-perplexity.md
Atg101 maintains selective protein-protein interactions with particular subunits while excluding others. Biochemical analysis demonstrates that Atg101 directly interacts with Atg13 but does not bind to other core subunits such as Atg1, Atg17, or the mammalian FIP200 ortholog Atg11.
GO:1990316 Atg1/ULK1 kinase complex
IBA
GO_REF:0000033
ACCEPT
Summary: Atg101 is a core component of the Atg1 kinase complex in S. pombe. This has been demonstrated by multiple independent studies showing that Atg101 directly interacts with Atg13 and is part of the complex containing Atg1, Atg13, Atg17, and Atg101 (PMID:26030876, PMID:28976798).
Reason: The IBA annotation is strongly supported by direct experimental evidence in S. pombe. Crystal structure of the Atg101-Atg13 complex and biochemical co-purification studies confirm Atg101 as a core subunit of the Atg1 complex.
Supporting Evidence:
PMID:26030876
Here, we report the crystal structure of the fission yeast Atg101-Atg13 complex.
file:SCHPO/atg101/atg101-deep-research-falcon.md
Differential scanning fluorimetry melting temperatures (Tm): **Atg13HORMA ~43Β°C**, **Atg101 ~48Β°C**, and **Atg13HORMA–Atg101 complex ~63Β°C**.
file:SCHPO/atg101/atg101-deep-research-perplexity.md
The defining molecular function of Atg101 involves its direct, constitutive interaction with Atg13 through their respective HORMA domains. The Atg101-Atg13 heterodimer forms the structural basis for autophagy initiation complex assembly across higher eukaryotes.
GO:0000045 autophagosome assembly
IBA
GO_REF:0000033
ACCEPT
Summary: Atg101 is essential for autophagosome assembly in S. pombe. Deletion of atg101 completely blocks CFP-Atg8 processing, indicating that autophagosome formation cannot occur without Atg101 (PMID:23950735). The protein stabilizes Atg13 and is required for proper assembly of the Atg1 complex at the phagophore assembly site.
Reason: The IBA annotation is fully consistent with direct experimental evidence showing atg101 deletion blocks autophagosome formation. This is a core function of the protein.
Supporting Evidence:
PMID:23950735
In addition, we found that atg6, atg11, atg17, and atg101 are also required for CFP-Atg8 processing, thus providing for the first time evidence that they are required for autophagy.
file:SCHPO/atg101/atg101-deep-research-falcon.md
A **WF-finger triple mutant (W110A, P111A, F112A)** retained Atg13 binding but **impaired autophagy**, indicating Atg101 has functional roles beyond stabilizing/binding Atg13.
GO:0000407 phagophore assembly site
IBA
GO_REF:0000033
ACCEPT
Summary: Atg101 localizes to the phagophore assembly site (PAS) during nitrogen starvation in S. pombe. YFP-tagged Atg101 colocalizes with CFP-Atg8 at cytoplasmic puncta induced by starvation (PMID:23950735). The localization depends on proper Atg13 function.
Reason: The IBA annotation is directly supported by experimental localization studies in S. pombe showing Atg101 colocalization with Atg8 at PAS.
Supporting Evidence:
PMID:23950735
Co-expressing other autophagy proteins tagged with YFP in the CFP-Atg8 strain showed that 14 Atg proteins and Ctl1 colocalized with Atg8 on the punctate structure (Figure 3A).
GO:0005634 nucleus
IEA
GO_REF:0000044
KEEP AS NON CORE
Summary: High-throughput analysis of protein localization in S. pombe detected Atg101 in the nucleus (PMID:16823372). This is a secondary localization and not related to its primary autophagy function.
Reason: The nuclear localization is supported by high-throughput localization data but is not related to the core autophagy function of Atg101. The protein's primary function is at the PAS/cytoplasm during autophagy.
Supporting Evidence:
PMID:16823372
Next, we determined the localization of 4,431 proteins, corresponding to approximately 90% of the fission yeast proteome, by tagging each ORF with the yellow fluorescent protein.
GO:0005737 cytoplasm
IEA
GO_REF:0000044
ACCEPT
Summary: Atg101 is localized to the cytoplasm, which is consistent with its function in autophagy. Under non-starvation conditions, Atg101 is diffusely distributed in the cytoplasm before translocating to PAS puncta upon starvation.
Reason: The cytoplasmic localization is accurate and consistent with the protein's function in autophagosome assembly.
Supporting Evidence:
file:SCHPO/atg101/atg101-deep-research-perplexity.md
The majority of the PAS-localizing fission yeast Atg proteins do not accumulate on distinct subcellular structures under non-starvation conditions.
GO:0006914 autophagy
IEA
GO_REF:0000120
ACCEPT
Summary: Atg101 is essential for autophagy in S. pombe. The IEA annotation is based on InterPro domain mapping and is correct. However, the more specific term GO:0016236 (macroautophagy) is more appropriate as the primary process annotation.
Reason: The annotation is correct but somewhat broad. The protein is specifically required for macroautophagy, which is a subtype of autophagy. Keeping this broader term is acceptable alongside the more specific macroautophagy annotation.
Supporting Evidence:
PMID:23950735
In addition, we found that atg6, atg11, atg17, and atg101 are also required for CFP-Atg8 processing, thus providing for the first time evidence that they are required for autophagy.
GO:0015031 protein transport
IEA
GO_REF:0000043
REMOVE
Summary: This annotation is derived from UniProt keyword mapping. While autophagy does involve transport of cytoplasmic materials to the vacuole, the term 'protein transport' is too general and does not accurately capture Atg101's function. Atg101 is not a transport factor per se; it is a structural component of the autophagy initiation complex.
Reason: This annotation is an over-generalization. Atg101 does not function directly in protein transport. Its role is in stabilizing Atg13 and enabling autophagosome assembly. The transport of proteins to the vacuole is a downstream consequence of autophagy, not the direct function of Atg101.
GO:0030435 sporulation resulting in formation of a cellular spore
IEA
GO_REF:0000043
REMOVE
Summary: This annotation is derived from UniProt keyword 'Sporulation'. The atg101 gene was originally identified as mug66 (meiotically up-regulated gene 66). However, the sporulation defect in atg101 mutants is a secondary consequence of defective autophagy. During nitrogen starvation in S. pombe, mating is triggered and followed by meiosis and sporulation. Autophagy mutants show mating defects because they cannot supply enough nitrogen intracellularly. Atg101 is not a sporulation-specific factor.
Reason: The sporulation phenotype is an indirect consequence of defective autophagy during nitrogen starvation, not a direct function of Atg101. The mating defect of autophagy mutants is attributed to an inability to supply enough nitrogen intracellularly through autophagy. This is a classic case of over-annotation based on phenotype rather than direct molecular function.
Supporting Evidence:
PMID:23950735
The mating defect of autophagy mutants, which is attributed to an inability to supply enough nitrogen intracellularly, was only discovered during a focused study on these mutants [3].
file:SCHPO/atg101/atg101-deep-research-falcon.md
Since autophagy is required for spore formation in both budding and fission yeast, the paper suggests the sporulation defect β€œmay be due to a deficiency in autophagy.”
GO:0034045 phagophore assembly site membrane
IEA
GO_REF:0000044
MODIFY
Summary: Atg101 localizes to the phagophore assembly site during autophagy induction, as a subunit of the Atg1/ULK1 complex that constitutes the site rather than as a resident of a membrane bounding it.
Reason: The supporting evidence places Atg101 in a punctate structure with 14 other Atg proteins - that is the assembly site itself. The Atg1 complex, of which Atg101 is a subunit, is the phase-separating component of the PAS, which is a liquid-like protein condensate and not a membrane-bounded compartment (PMID:32025038). GO:0034045 asserts a bounding membrane the PAS does not have (GO issue #29437), and this IEA derives from the UniProt SL-0221 location, which is the propagation source rather than independent evidence. GO:0000407 states exactly what was observed.
Proposed replacements: phagophore assembly site
Supporting Evidence:
PMID:23950735
Co-expressing other autophagy proteins tagged with YFP in the CFP-Atg8 strain showed that 14 Atg proteins and Ctl1 colocalized with Atg8 on the punctate structure (Figure 3A).
GO:0051321 meiotic cell cycle
IEA
GO_REF:0000043
REMOVE
Summary: This annotation is derived from UniProt keyword 'Meiosis'. The gene was originally named mug66 (meiotically up-regulated gene 66) because its expression is induced during meiosis. However, Atg101 is not a meiotic regulator. It is an autophagy factor. The meiotic/mating phenotype observed in atg101 mutants is a secondary consequence of defective autophagy. During nitrogen starvation in S. pombe, autophagy is required to provide intracellular nitrogen for mating and subsequent meiosis. ATG genes are autophagy machinery components, not meiotic regulators. Autophagy is upregulated during meiosis/sporulation, which led to the original mug66 designation, but this reflects transcriptional regulation rather than direct function in meiosis.
Reason: This is a clear case of over-annotation. The meiotic phenotype is an indirect consequence of the autophagy defect. Atg101 is a core autophagy factor, not a meiotic cell cycle regulator. The mating defect of autophagy mutants is attributed to inability to supply nitrogen intracellularly through autophagy, not to a direct role in meiosis. The SPKW annotation conflates transcriptional upregulation during meiosis with direct participation in the meiotic cell cycle.
Supporting Evidence:
PMID:23950735
The mating defect of autophagy mutants, which is attributed to an inability to supply enough nitrogen intracellularly, was only discovered during a focused study on these mutants [3].
file:SCHPO/atg101/atg101-deep-research-perplexity.md
Atg101 represents a remarkable example of functional divergence and evolutionary adaptation, in which a HORMA domain protein has evolved from a role in mitotic checkpoint control to become an essential component of the autophagy initiation machinery.
GO:0005515 protein binding
IPI
PMID:26030876
Structure of the Atg101-Atg13 complex reveals essential role...
MODIFY
Summary: The protein binding annotation is based on the demonstrated interaction between Atg101 and Atg13. The crystal structure of the Atg101-Atg13 complex was solved at 3.0 Angstrom resolution, showing direct HORMA domain-mediated interaction (PMID:26030876).
Reason: While the protein binding annotation is technically correct, it is uninformative. The specific interaction is with Atg13 via HORMA domain dimerization, which forms an obligate, mutually stabilizing heterodimer (falcon deep research). The most informative MF term capturing Atg101's role of bridging Atg13 into the Atg1 initiation complex is molecular adaptor activity. 'Protein kinase binding' (the earlier suggestion) is not appropriate because Atg101 does not bind the Atg1 kinase directly and is dispensable for its activation (PMID:32909946).
Proposed replacements: molecular adaptor activity
Supporting Evidence:
PMID:26030876
Here, we report the crystal structure of the fission yeast Atg101-Atg13 complex.
file:SCHPO/atg101/atg101-deep-research-falcon.md
Their heterodimerization is obligate and stabilizes both partners, providing a structural module within the initiation complex.
GO:0042594 response to starvation
NAS
PMID:34499173
Visual detection of binary, ternary and quaternary protein i...
ACCEPT
Summary: Atg101 is part of the Atg1 complex which is essential for autophagy during starvation. The protein functions in the cellular response to nitrogen starvation by enabling autophagosome formation.
Reason: The annotation is accurate. Atg101 functions in the autophagy pathway which is the primary cellular response to starvation in S. pombe. Autophagy is upregulated during starvation to recycle intracellular components.
Supporting Evidence:
file:SCHPO/atg101/atg101-deep-research-perplexity.md
Macroautophagy (hereafter autophagy) is a catabolic pathway that transports cytoplasmic materials into a degradative organelle, the vacuole or lysosome. This self-digestion process is upregulated during starvation.
GO:1990316 Atg1/ULK1 kinase complex
EXP
PMID:34499173
Visual detection of binary, ternary and quaternary protein i...
ACCEPT
Summary: Direct experimental evidence from the Pil1 co-tethering assay demonstrates Atg101 is part of the Atg1 complex in S. pombe. The study systematically characterized protein-protein interactions in the Atg1 complex.
Reason: Strong experimental evidence supports Atg101 as a core component of the Atg1/ULK1 kinase complex. This is the same GO term as the IBA annotation but with direct experimental evidence.
Supporting Evidence:
PMID:34499173
Using this assay, we systematically characterized the protein-protein interactions in the Atg1 complex and in the phosphatidylinositol 3-kinase (PtdIns3K) complexes
GO:0000045 autophagosome assembly
IMP
PMID:26030876
Structure of the Atg101-Atg13 complex reveals essential role...
ACCEPT
Summary: The mutant phenotype (IMP) evidence shows that atg101 is required for autophagosome assembly. The study demonstrated that Atg101 is essential for autophagy initiation through its role in stabilizing Atg13 and recruiting downstream factors via the WF finger motif.
Reason: Strong experimental evidence from mutational studies confirms the essential role of Atg101 in autophagosome assembly. This is a core function of the protein.
Supporting Evidence:
PMID:26030876
Mutational studies revealed that Atg101 is responsible for recruiting downstream factors to the autophagosome-formation site in mammals via a newly identified WF finger.
file:SCHPO/atg101/atg101-deep-research-falcon.md
A **WF-finger triple mutant (W110A, P111A, F112A)** retained Atg13 binding but **impaired autophagy**, indicating Atg101 has functional roles beyond stabilizing/binding Atg13.
GO:1990316 Atg1/ULK1 kinase complex
IDA
PMID:26030876
Structure of the Atg101-Atg13 complex reveals essential role...
ACCEPT
Summary: Direct assay (IDA) evidence from the crystal structure and biochemical studies demonstrates that Atg101 is a component of the Atg1 kinase complex, directly interacting with Atg13.
Reason: The crystal structure at 3.0 Angstrom resolution of the Atg101-Atg13 complex provides definitive evidence that Atg101 is a component of the Atg1 complex.
Supporting Evidence:
PMID:26030876
Here, we report the crystal structure of the fission yeast Atg101-Atg13 complex.
GO:0005515 protein binding
IPI
PMID:28976798
Conserved and unique features of the fission yeast core Atg1...
MODIFY
Summary: The protein binding annotation is based on co-immunoprecipitation experiments showing Atg101 interaction with Atg13 via HORMA domain interactions.
Reason: Same as above - protein binding is uninformative. The HORMA-mediated interaction with Atg13 is best captured by molecular adaptor activity (Atg101 bridges Atg13 into the Atg1 complex), not by 'protein kinase binding', since Atg101 does not bind the Atg1 kinase directly and is dispensable for Atg1 kinase activation in S. pombe (PMID:32909946).
Proposed replacements: molecular adaptor activity
Supporting Evidence:
PMID:28976798
Atg101 interacts with the HORMA domain of Atg13 and this enhances the stability of both proteins.
file:SCHPO/atg101/atg101-deep-research-falcon.md
Atg1 purified from **atg101Ξ”** cells showed **autophosphorylation activity similar to wild type** under both nutrient-rich and nitrogen-starvation conditions.
GO:0000407 phagophore assembly site
IDA
PMID:23950735
Global analysis of fission yeast mating genes reveals new au...
ACCEPT
Summary: Direct assay (IDA) evidence from fluorescence microscopy shows Atg101 localization at the phagophore assembly site during starvation. YFP-tagged Atg101 colocalizes with CFP-Atg8 at cytoplasmic puncta.
Reason: Direct microscopy evidence confirms Atg101 localization at PAS during autophagy induction.
Supporting Evidence:
PMID:23950735
Co-expressing other autophagy proteins tagged with YFP in the CFP-Atg8 strain showed that 14 Atg proteins and Ctl1 colocalized with Atg8 on the punctate structure (Figure 3A).
GO:0016236 macroautophagy
IMP
PMID:23950735
Global analysis of fission yeast mating genes reveals new au...
ACCEPT
Summary: The mutant phenotype (IMP) evidence from the CFP-Atg8 processing assay shows that atg101 deletion completely blocks macroautophagy. The atg101 deletion mutant fails to process CFP-Atg8, indicating a complete block in autophagosome formation and delivery to vacuoles.
Reason: This is the most specific and accurate biological process annotation for Atg101's core function. The CFP-Atg8 processing assay provides definitive evidence for the requirement of Atg101 in macroautophagy.
Supporting Evidence:
PMID:23950735
In addition, we found that atg6, atg11, atg17, and atg101 are also required for CFP-Atg8 processing, thus providing for the first time evidence that they are required for autophagy.
GO:0005634 nucleus
HDA
PMID:16823372
ORFeome cloning and global analysis of protein localization ...
KEEP AS NON CORE
Summary: High-throughput analysis (HDA) from the global protein localization study detected Atg101 in the nucleus. This represents a secondary localization and is not related to autophagy function.
Reason: The nuclear localization is supported by HDA but represents a non-functional pool or secondary localization. The primary site of Atg101 function is at the PAS in the cytoplasm.
Supporting Evidence:
PMID:16823372
Next, we determined the localization of 4,431 proteins, corresponding to approximately 90% of the fission yeast proteome, by tagging each ORF with the yellow fluorescent protein.
GO:0005829 cytosol
HDA
PMID:16823372
ORFeome cloning and global analysis of protein localization ...
ACCEPT
Summary: High-throughput analysis (HDA) detected Atg101 in the cytosol. Under non-starvation conditions, Atg101 is diffusely distributed in the cytoplasm/cytosol before concentrating at PAS upon starvation.
Reason: The cytosolic localization is consistent with the protein's function and distribution before autophagy induction.
Supporting Evidence:
PMID:16823372
Next, we determined the localization of 4,431 proteins, corresponding to approximately 90% of the fission yeast proteome, by tagging each ORF with the yellow fluorescent protein.

Core Functions

Atg101 is essential for macroautophagy in S. pombe. Deletion of atg101 completely blocks CFP-Atg8 processing, indicating that autophagosome formation cannot occur without Atg101 (PMID:23950735). The protein functions as a non-enzymatic molecular adaptor/scaffold that forms an obligate HORMA-domain heterodimer with the N-terminal HORMA domain of Atg13, stabilizing the otherwise unstable Atg13 HORMA domain (differential scanning fluorimetry: Atg13HORMA Tm ~43 C, Atg101 ~48 C, Atg13HORMA-Atg101 complex ~63 C; PMID:26030876, PMID:28976798). This heterodimer incorporates Atg101 into the Atg1 initiation complex via Atg13 (and Atg1 C-terminal domain contacts), while a conserved WF finger surface mediates separable recruitment of downstream factors. Notably, in S. pombe Atg101 is dispensable for Atg1 kinase catalytic activation in vitro (Atg1 from atg101-delta cells autophosphorylates normally); Atg1 activation instead depends on Atg11-mediated dimerization (PMID:32909946). The core molecular role is therefore adaptor/scaffolding within the initiation complex rather than direct kinase regulation.

Supporting Evidence:
  • PMID:23950735
    In addition, we found that atg6, atg11, atg17, and atg101 are also required for CFP-Atg8 processing, thus providing for the first time evidence that they are required for autophagy.
  • PMID:26030876
    Here, we report the crystal structure of the fission yeast Atg101-Atg13 complex.
  • file:SCHPO/atg101/atg101-deep-research-falcon.md
    Their heterodimerization is obligate and stabilizes both partners, providing a structural module within the initiation complex.
  • PMID:32909946
    Atg1 from atg13Ξ”, atg17Ξ”, or atg101Ξ” mutant exhibited autophosphorylation activities similar to that of Atg1 from wild type, under both nutrient-rich and nitrogen-starved conditions

References

Loading supporting content…

Download this section (compressed HTML)

Suggested Questions for Experts

Q: What are the specific downstream factors recruited by the Atg101 WF finger motif in S. pombe?

Q: Does the nuclear localization of Atg101 have any functional significance, or is it incidental?

Q: Are there conditions other than nitrogen starvation that induce Atg101 localization to PAS in S. pombe?

Suggested Experiments

Experiment: Mass spectrometry analysis of Atg101 WF finger mutants to identify interaction partners dependent on this motif

Hypothesis: The WF finger motif recruits specific WIPI-family proteins to PAS for autophagosome membrane expansion

Experiment: Conditional expression/depletion systems to test if Atg101 nuclear localization has any function

Hypothesis: The nuclear pool of Atg101 may be a reserve or may have an uncharacterized nuclear function

Deep Research

Falcon

(atg101-deep-research-falcon.md)

Loading supporting content…

Download this section (compressed HTML)

Perplexity

(atg101-deep-research-perplexity.md)

Loading supporting content…

Download this section (compressed HTML)

πŸ“š Additional Documentation

Bioreason Rl Predictions

(atg101-bioreason-rl-predictions.md)

Loading supporting content…

Download this section (compressed HTML)

Bioreason Rl Review

(atg101-bioreason-rl-review.md)

Loading supporting content…

Download this section (compressed HTML)

πŸ“„ View Raw YAML

Loading supporting content…

Download this section (compressed HTML)