TDO

UniProt ID: A0A7G4RN94
Organism: Doryteuthis pealeii
Review Status: IN PROGRESS
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Gene Description

Tryptophan 2,3-dioxygenase (TDO) is a heme-dependent oxidoreductase that catalyzes the first committed step in ommochrome pigment biosynthesis in D. pealeii, converting L-tryptophan to N-formylkynurenine via oxidative cleavage of the indole ring. TDO is expressed in the retina and chromatophore layer of the skin, the two principal ommochrome-pigmented tissues. Crawford et al. (2020) demonstrated that CRISPR-Cas9 knockout of TDO in D. pealeii embryos efficiently eliminated pigmentation in both eyes and chromatophores with >90% disruption efficiency, while ink sac melanin pigmentation was unaffected. This was the first gene knockout achieved in any cephalopod. TDO inhibition with 680C91 also completely blocked pigmentation, confirming the enzyme is required for ommochrome synthesis. Notably, D. pealeii lacks an IDO (indoleamine 2,3-dioxygenase) ortholog, unlike Euprymna berryi where IDO can compensate for TDO loss. TDO belongs to the PANTHER family PTHR10138 (Tryptophan 2,3-dioxygenase), is predicted to function as a homotetramer (dimer of dimers), and contains a single heme cofactor per subunit. The gene spans 13 exons over 120 kb of genomic DNA.

Existing Annotations Review

GO Term Evidence Action Reason
GO:0004833 L-tryptophan 2,3-dioxygenase activity
IEA
GO_REF:0000120
ACCEPT
Summary: L-tryptophan 2,3-dioxygenase activity (EC 1.13.11.11) is the defining enzymatic function of TDO. This IEA annotation is based on combined automated methods (InterPro, ARBA, PANTHER, UniRule). In D. pealeii, Crawford et al. (2020) demonstrated that CRISPR-Cas9 knockout of TDO eliminated ommochrome pigmentation, and pharmacological inhibition with 680C91 (a TDO-selective inhibitor) blocked pigmentation in both eyes and chromatophores [PMID:32735817]. The UniProt entry confirms TDO catalyzes L-tryptophan + O2 = N-formylkynurenine (Rhea:RHEA:24536). Phylogenetic analysis confirmed this gene as a bona fide TDO (distinct from IDO) [PMID:32735817].
Reason: This is the core enzymatic function of TDO, supported by sequence homology, PANTHER family assignment (PTHR10138), HAMAP rule MF_03020, and functional knockout data in this species showing loss of ommochrome pigmentation.
Supporting Evidence:
PMID:32735817
In invertebrates, Tryptophan, 2,3 Dioxygenase (TDO) catalyzes the first committed step in ommochrome biosynthesis, converting Tryptophan to N-Formylkyneurenine.
PMID:32735817
A phylogenetic comparison of this sequence with diverse TDOs, and indolamine-2,3-dioxygenases (a different enzyme that catalyzes the same reaction), supported its identity as TDO.
GO:0006569 L-tryptophan catabolic process
IEA
GO_REF:0000117
ACCEPT
Summary: L-tryptophan catabolic process is annotated via ARBA machine learning. TDO catalyzes the oxidative cleavage of L-tryptophan as the first step in the kynurenine pathway. Crawford et al. (2020) showed that TDO knockout eliminates ommochrome biosynthesis from tryptophan in D. pealeii [PMID:32735817]. This term is correct but could be more specific. The UniProt record lists both GO:0019441 (L-tryptophan catabolic process to kynurenine) and GO:0019442 (L-tryptophan catabolic process to acetyl-CoA), and GO:0019441 more precisely captures TDO function as it catalyzes the first step to kynurenine specifically.
Reason: L-tryptophan catabolic process correctly describes the biological process TDO participates in. While a more specific term like L-tryptophan catabolic process to kynurenine (GO:0019441) would be ideal, that term is now obsolete in GO. GO:0006569 is the most appropriate active term for this function. Crawford et al. (2020) showed TDO knockout eliminates the tryptophan-to-ommochrome pathway in D. pealeii [PMID:32735817].
Supporting Evidence:
PMID:32735817
TDO catalyzes the first committed step in ommochrome biosynthesis, converting Tryptophan to N-Formylkyneurenine.
GO:0020037 heme binding
IEA
GO_REF:0000120
ACCEPT
Summary: Heme binding is annotated by combined IEA methods (InterPro, ARBA, PANTHER, UniRule). The UniProt record explicitly states: "Binds 1 heme group per subunit" (HAMAP-Rule:MF_03020), and lists heme as a cofactor (ChEBI:30413). TDO is a heme-dependent dioxygenase, and heme is essential for its catalytic mechanism. This is well-established for TDO family members across all species.
Reason: Heme binding is integral to TDO catalytic function. The enzyme requires bound heme to catalyze oxidative cleavage of the tryptophan indole ring. This is confirmed by UniProt cofactor annotation and is a defining feature of the TDO family (HAMAP MF_03020, Pfam PF03301 Trp_dioxygenase).
Supporting Evidence:
PMID:32735817
we determined whether a TDO-selective inhibitor (680C91) impeded pigmentation in developing embryos.
GO:0046872 metal ion binding
IEA
GO_REF:0000002
MARK AS OVER ANNOTATED
Summary: Metal ion binding is annotated via InterPro2GO mapping (IPR037217). This is correct as TDO binds iron through its heme prosthetic group. However, this term is very generic and redundant with the more informative heme binding (GO:0020037) annotation already present, which more precisely captures the nature of the metal cofactor interaction.
Reason: While technically correct (TDO binds iron via heme), GO:0046872 (metal ion binding) is too generic to be informative. The heme binding annotation (GO:0020037) already captures this function at a more appropriate level of specificity. The metal ion binding term does not add useful functional information beyond what heme binding conveys.
GO:0006727 ommochrome biosynthetic process
IDA
PMID:32735817
Highly Efficient Knockout of a Squid Pigmentation Gene
NEW
Summary: NEW annotation. Crawford et al. (2020) demonstrated by CRISPR-Cas9 knockout that TDO is required for ommochrome biosynthesis in D. pealeii. TDO knockout eliminated pigmentation in both chromatophores and eyes, which contain ommochrome pigments. The TDO-selective inhibitor 680C91 also blocked pigmentation. In situ hybridization confirmed TDO expression in chromatophore precursors and eyes. This is the most biologically meaningful annotation for this gene in cephalopods, as ommochrome pigmentation is the primary downstream biological process served by TDO in this organism.
Reason: Ommochrome biosynthesis is the key biological process requiring TDO in cephalopods. CRISPR knockout and pharmacological inhibition both demonstrate TDO is essential for ommochrome production. This annotation is not present in the existing GOA set but is strongly supported by direct experimental evidence in this species.
Supporting Evidence:
PMID:32735817
In cephalopods, the pigments in the eyes and chromatophores are ommochromes, a derivative of tryptophan
PMID:32735817
Knocking out TDO in squid embryos efficiently eliminated pigmentation. By precisely timing CRISPR-Cas9 delivery during early development, the degree of pigmentation could be finely controlled. Genotyping revealed knockout efficiencies routinely greater than 90%.
PMID:32735817
We added 680C91 to developing embryos at stage 20, and it clearly blocked pigmentation in both the eyes and chromatophores, with animals developing normally otherwise.
PMID:29989284
Ommochromes are widely occurring coloured molecules of invertebrates, arising from tryptophan catabolism through the so-called Tryptophan → Ommochrome pathway.
GO:0043473 pigmentation
IMP
PMID:32735817
Highly Efficient Knockout of a Squid Pigmentation Gene
NEW
Summary: NEW annotation. Crawford et al. (2020) showed that TDO knockout by CRISPR-Cas9 resulted in loss of pigmentation in D. pealeii embryos, with chromatophore and eye pigmentation eliminated. Ink sac melanin was unaffected, demonstrating TDO specifically contributes to ommochrome-based pigmentation. Ahuja et al. (2023) further showed in E. berryi that TDO knockout delays pigmentation and TDO+IDO double knockout produces complete albinism [PMID:37343558].
Reason: Pigmentation is the primary phenotype affected by TDO loss of function. The knockout phenotype directly demonstrates involvement in pigmentation. This is a core biological role for TDO in cephalopods, where ommochrome pigments color the chromatophores and retina.
Supporting Evidence:
PMID:32735817
pigmentation is completely absent from the chromatophores and is minimal in the eyes which are light red
PMID:37343558
The knockout of tdo in D. pealeii completely inhibited pigmentation but had little to no effect in E. berryi.

Core Functions

TDO catalyzes the oxidative cleavage of L-tryptophan to N-formylkynurenine, the first committed step in the kynurenine pathway and ommochrome biosynthesis in D. pealeii. CRISPR-Cas9 knockout eliminated ommochrome pigmentation in both eyes and chromatophores with >90% efficiency, and pharmacological inhibition with 680C91 confirmed the enzyme is required. D. pealeii lacks an IDO ortholog, making TDO the sole enzyme for this reaction. TDO is a heme-dependent dioxygenase that binds one heme group per subunit. The downstream kynurenine pathway intermediates 3-hydroxykynurenine and xanthurenic acid serve as precursors for xanthommatin and related ommatin pigments deposited in specialized ommochromasomes within chromatophore and retinal pigment cells (PMID:29989284). The TDO-selective inhibitor 680C91 at 3.15 mM from stage 20-27 phenocopied the CRISPR knockout, confirming enzymatic activity is required upstream of ommochrome deposition. Genotyping of CRISPR-edited embryos showed a mean of 38 +/- 13 distinct indel events per animal, with no dominant allele, yet produced near-complete pigmentation loss, demonstrating the strong genotype-phenotype link. In E. berryi, TDO knockout alone produced only slightly delayed pigmentation due to IDO compensation, but TDO+IDO double knockout yielded complete albinism enabling the first in vivo calcium imaging of neural activity in a cephalopod (PMID:37343558).

Supporting Evidence:
  • PMID:32735817
    Tryptophan, 2,3 Dioxygenase (TDO) catalyzes the first committed step in ommochrome biosynthesis, converting Tryptophan to N-Formylkyneurenine
  • PMID:32735817
    Knocking out TDO in squid embryos efficiently eliminated pigmentation
  • PMID:37343558
    The knockout of tdo in D. pealeii completely inhibited pigmentation but had little to no effect in E. berryi.

References

Gene Ontology annotation through association of InterPro records with GO terms
Electronic Gene Ontology annotations created by ARBA machine learning models
Combined Automated Annotation using Multiple IEA Methods
Highly Efficient Knockout of a Squid Pigmentation Gene
  • TDO was selected as a knockout target because ommochromes pigment cephalopod eyes and chromatophores, and TDO catalyzes the first committed step in their biosynthesis.
  • A single TDO gene was identified in the D. pealeii genome, spanning 13 exons over 120 kb. Phylogenetic analysis confirmed the gene as a bona fide TDO distinct from IDO.
  • In situ hybridization showed TDO expression in chromatophore precursors on arms and mantle, and in eyes; RNAseq confirmed highest expression in retina and chromatophore layer of skin.
  • TDO-selective inhibitor 680C91 completely blocked pigmentation in both eyes and chromatophores, with animals developing normally otherwise.
  • CRISPR-Cas9 knockout with two sgRNAs targeting exons 1 and 2 eliminated pigmentation with >90% disruption efficiency. Ink sac melanin was unaffected, confirming specificity for the ommochrome pathway.
  • This was the first gene knockout achieved in any cephalopod.
Ommochromes in invertebrates: biochemistry and cell biology
  • Ommochromes are widely occurring coloured molecules of invertebrates, arising from tryptophan catabolism through the Tryptophan → Ommochrome pathway. They are mainly known to mediate compound eye vision, as well as reversible and irreversible colour patterning.
    "Ommochromes are widely occurring coloured molecules of invertebrates, arising from tryptophan catabolism through the so-called Tryptophan to Ommochrome pathway."
  • Ommochromasomes are the organelles where ommochromes are synthesised and stored, playing an important role in mediating ommochrome functions. They are part of the lysosome-related organelles (LROs) family, which includes vertebrate melanosomes.
    "Ommochromasomes are the organelles where ommochromes are synthesised and stored. Hence, they play an important role in mediating ommochrome functions."
  • Ommochromes may also be involved in cell homeostasis by detoxifying free tryptophan and buffering oxidative stress, in addition to their roles in pigmentation and vision.
    "Ommochromes might also be involved in cell homeostasis by detoxifying free tryptophan and buffering oxidative stress."
Creation of an albino squid line by CRISPR-Cas9 and its application for in vivo functional imaging of neural activity
  • In E. berryi, TDO knockout alone did not eliminate pigmentation despite >90% disruption efficiency, due to compensation by IDO. D. pealeii genome lacks IDO orthologs, explaining why TDO knockout alone is sufficient in that species.
  • E. berryi homozygous TDO knockout showed slightly delayed pigmentation during development. TDO+IDO double knockout produced complete albinism.
  • TDO expression in E. berryi is approximately 20-fold higher than IDO in stage 24 embryos. TDO is expressed in eyes and chromatophores, similar to D. pealeii.
  • Albino E. berryi enabled the first in vivo calcium imaging of neural activity in a cephalopod using two-photon microscopy.

Suggested Questions for Experts

Q: Does D. pealeii TDO have any role in tryptophan catabolism beyond ommochrome biosynthesis (e.g. kynurenine pathway metabolites for immune or neural signaling)?

Suggested experts: Rosenthal JJC, Albertin CB

Q: What are the consequences of partial TDO loss on chromatophore function and dynamic color change in adult squid?

Suggested experts: Crawford K

Q: Is there any post-translational regulation of TDO activity in cephalopods, as seen with substrate activation in mammalian TDO?

Suggested Experiments

Experiment: Characterize the enzymatic kinetics of recombinant D. pealeii TDO, including heme stoichiometry and substrate specificity, to confirm in vitro activity.

Hypothesis: D. pealeii TDO has similar catalytic properties to mammalian TDO, with strict specificity for L-tryptophan over other indoleamine substrates.

Type: biochemistry

Experiment: Use single-cell RNA-seq to map TDO expression across chromatophore subtypes and developmental stages in D. pealeii embryos.

Hypothesis: TDO expression is restricted to ommochrome-producing cell types (chromatophores and retinal pigment cells) and onset correlates with pigmentation timing.

Type: transcriptomics

Experiment: Measure kynurenine pathway metabolite levels (N-formylkynurenine, kynurenine, 3-hydroxykynurenine, xanthurenic acid) in TDO knockout vs wildtype D. pealeii embryos by LC-MS/MS.

Hypothesis: TDO knockout eliminates kynurenine pathway flux entirely in D. pealeii due to the absence of IDO, unlike in E. berryi where IDO provides compensation.

Type: metabolomics

Experiment: Test whether partial TDO knockout in adult squid affects chromatophore expansion dynamics and camouflage behavior using video analysis.

Hypothesis: Reduced ommochrome content from partial TDO loss impairs chromatophore opacity and dynamic range of color change.

Type: behavioral/physiological

📚 Additional Documentation

Deep Research Falcon

(TDO-deep-research-falcon.md)

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organism: DORPE
gene_id: TDO
gene_symbol: TDO
uniprot_accession: A0A7G4RN94
protein_description: 'RecName: Full=Tryptophan 2,3-dioxygenase {ECO:0000256|HAMAP-Rule:MF_03020};
Short=TDO {ECO:0000256|HAMAP-Rule:MF_03020}; EC=1.13.11.11 {ECO:0000256|HAMAP-Rule:MF_03020};
AltName: Full=Tryptamin 2,3-dioxygenase {ECO:0000256|HAMAP-Rule:MF_03020}; AltName:
Full=Tryptophan oxygenase {ECO:0000256|HAMAP-Rule:MF_03020}; Short=TO {ECO:0000256|HAMAP-Rule:MF_03020};
Short=TRPO {ECO:0000256|HAMAP-Rule:MF_03020}; AltName: Full=Tryptophan pyrrolase
{ECO:0000256|HAMAP-Rule:MF_03020}; AltName: Full=Tryptophanase {ECO:0000256|HAMAP-Rule:MF_03020};'
gene_info: Name=TDO {ECO:0000313|EMBL:QMT62772.1};
organism_full: Doryteuthis pealeii (Longfin inshore squid) (Loligo pealeii).
protein_family: Belongs to the tryptophan 2,3-dioxygenase family.
protein_domains: Trp/Indoleamine_2_3_dOase-like. (IPR037217); Trp_2_3_dOase. (IPR004981);
Trp_dioxygenase (PF03301)
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Question

Gene Research for Functional Annotation

⚠️ CRITICAL: Gene/Protein Identification Context

BEFORE YOU BEGIN RESEARCH: You MUST verify you are researching the CORRECT gene/protein. Gene symbols can be ambiguous, especially for less well-characterized genes from non-model organisms.

Target Gene/Protein Identity (from UniProt):

  • UniProt Accession: A0A7G4RN94
  • Protein Description: RecName: Full=Tryptophan 2,3-dioxygenase {ECO:0000256|HAMAP-Rule:MF_03020}; Short=TDO {ECO:0000256|HAMAP-Rule:MF_03020}; EC=1.13.11.11 {ECO:0000256|HAMAP-Rule:MF_03020}; AltName: Full=Tryptamin 2,3-dioxygenase {ECO:0000256|HAMAP-Rule:MF_03020}; AltName: Full=Tryptophan oxygenase {ECO:0000256|HAMAP-Rule:MF_03020}; Short=TO {ECO:0000256|HAMAP-Rule:MF_03020}; Short=TRPO {ECO:0000256|HAMAP-Rule:MF_03020}; AltName: Full=Tryptophan pyrrolase {ECO:0000256|HAMAP-Rule:MF_03020}; AltName: Full=Tryptophanase {ECO:0000256|HAMAP-Rule:MF_03020};
  • Gene Information: Name=TDO {ECO:0000313|EMBL:QMT62772.1};
  • Organism (full): Doryteuthis pealeii (Longfin inshore squid) (Loligo pealeii).
  • Protein Family: Belongs to the tryptophan 2,3-dioxygenase family.
  • Key Domains: Trp/Indoleamine_2_3_dOase-like. (IPR037217); Trp_2_3_dOase. (IPR004981); Trp_dioxygenase (PF03301)

MANDATORY VERIFICATION STEPS:

  1. Check if the gene symbol "TDO" matches the protein description above
  2. Verify the organism is correct: Doryteuthis pealeii (Longfin inshore squid) (Loligo pealeii).
  3. Check if protein family/domains align with what you find in literature
  4. If you find literature for a DIFFERENT gene with the same or similar symbol, STOP

If Gene Symbol is Ambiguous or You Cannot Find Relevant Literature:

DO NOT PROCEED WITH RESEARCH ON A DIFFERENT GENE. Instead:
- State clearly: "The gene symbol 'TDO' is ambiguous or literature is limited for this specific protein"
- Explain what you found (e.g., "Found extensive literature on a different gene with the same symbol in a different organism")
- Describe the protein based ONLY on the UniProt information provided above
- Suggest that the protein function can be inferred from domain/family information

Research Target:

Please provide a comprehensive research report on the gene TDO (gene ID: TDO, UniProt: A0A7G4RN94) in DORPE.

The research report should be a detailed narrative explaining the function, biological processes, and localization of the gene product. Citations should be given for all claims.

You should prioritize authoritative reviews and primary scientific literature when conducting research. You can supplement
this with annotations you find in gene/protein databases, but these can be outdated or inaccurate.

We are specifically interested in the primary function of the gene - for enzymes, what reaction is catalyzed, and what is the substrate specificity? For transporters, what is the substrate? For structural proteins or adapters, what is the broader structural role? For signaling molecules, what is the role in the pathway.

We are interested in where in or outside the cell the gene product carries out its function.

We are also interested in the signaling or biochemical pathways in which the gene functions. We are less interested in broad pleiotropic effects, except where these elucidate the precise role.

Include evidence where possible. We are interested in both experimental evidence as well as inference from structure, evolution, or bioinformatic analysis. Precise studies should be prioritized over high-throughput, where available.

Output

Question: You are an expert researcher providing comprehensive, well-cited information.

Provide detailed information focusing on:
1. Key concepts and definitions with current understanding
2. Recent developments and latest research (prioritize 2023-2024 sources)
3. Current applications and real-world implementations
4. Expert opinions and analysis from authoritative sources
5. Relevant statistics and data from recent studies

Format as a comprehensive research report with proper citations. Include URLs and publication dates where available.
Always prioritize recent, authoritative sources and provide specific citations for all major claims.

Gene Research for Functional Annotation

⚠️ CRITICAL: Gene/Protein Identification Context

BEFORE YOU BEGIN RESEARCH: You MUST verify you are researching the CORRECT gene/protein. Gene symbols can be ambiguous, especially for less well-characterized genes from non-model organisms.

Target Gene/Protein Identity (from UniProt):

  • UniProt Accession: A0A7G4RN94
  • Protein Description: RecName: Full=Tryptophan 2,3-dioxygenase {ECO:0000256|HAMAP-Rule:MF_03020}; Short=TDO {ECO:0000256|HAMAP-Rule:MF_03020}; EC=1.13.11.11 {ECO:0000256|HAMAP-Rule:MF_03020}; AltName: Full=Tryptamin 2,3-dioxygenase {ECO:0000256|HAMAP-Rule:MF_03020}; AltName: Full=Tryptophan oxygenase {ECO:0000256|HAMAP-Rule:MF_03020}; Short=TO {ECO:0000256|HAMAP-Rule:MF_03020}; Short=TRPO {ECO:0000256|HAMAP-Rule:MF_03020}; AltName: Full=Tryptophan pyrrolase {ECO:0000256|HAMAP-Rule:MF_03020}; AltName: Full=Tryptophanase {ECO:0000256|HAMAP-Rule:MF_03020};
  • Gene Information: Name=TDO {ECO:0000313|EMBL:QMT62772.1};
  • Organism (full): Doryteuthis pealeii (Longfin inshore squid) (Loligo pealeii).
  • Protein Family: Belongs to the tryptophan 2,3-dioxygenase family.
  • Key Domains: Trp/Indoleamine_2_3_dOase-like. (IPR037217); Trp_2_3_dOase. (IPR004981); Trp_dioxygenase (PF03301)

MANDATORY VERIFICATION STEPS:

  1. Check if the gene symbol "TDO" matches the protein description above
  2. Verify the organism is correct: Doryteuthis pealeii (Longfin inshore squid) (Loligo pealeii).
  3. Check if protein family/domains align with what you find in literature
  4. If you find literature for a DIFFERENT gene with the same or similar symbol, STOP

If Gene Symbol is Ambiguous or You Cannot Find Relevant Literature:

DO NOT PROCEED WITH RESEARCH ON A DIFFERENT GENE. Instead:
- State clearly: "The gene symbol 'TDO' is ambiguous or literature is limited for this specific protein"
- Explain what you found (e.g., "Found extensive literature on a different gene with the same symbol in a different organism")
- Describe the protein based ONLY on the UniProt information provided above
- Suggest that the protein function can be inferred from domain/family information

Research Target:

Please provide a comprehensive research report on the gene TDO (gene ID: TDO, UniProt: A0A7G4RN94) in DORPE.

The research report should be a detailed narrative explaining the function, biological processes, and localization of the gene product. Citations should be given for all claims.

You should prioritize authoritative reviews and primary scientific literature when conducting research. You can supplement
this with annotations you find in gene/protein databases, but these can be outdated or inaccurate.

We are specifically interested in the primary function of the gene - for enzymes, what reaction is catalyzed, and what is the substrate specificity? For transporters, what is the substrate? For structural proteins or adapters, what is the broader structural role? For signaling molecules, what is the role in the pathway.

We are interested in where in or outside the cell the gene product carries out its function.

We are also interested in the signaling or biochemical pathways in which the gene functions. We are less interested in broad pleiotropic effects, except where these elucidate the precise role.

Include evidence where possible. We are interested in both experimental evidence as well as inference from structure, evolution, or bioinformatic analysis. Precise studies should be prioritized over high-throughput, where available.

Research Report: Functional Annotation of TDO (UniProt A0A7G4RN94) in Doryteuthis pealeii (Longfin inshore squid)

1. Target verification (critical disambiguation)

The gene symbol TDO is ambiguous across taxa (e.g., vertebrate TDO2), but the Doryteuthis pealeii target relevant to UniProt A0A7G4RN94 is strongly supported as a tryptophan 2,3-dioxygenase family enzyme by: (i) a squid-specific locus identified by BLAST against known TDO/IDO sequences and placed in a phylogeny to distinguish TDO from related dioxygenases (e.g., IDO), (ii) mapping to a single genomic locus reported as 13 exons spanning >120 kb and deposited as GenBank MT648678, and (iii) a causal pigmentation phenotype following inhibition or CRISPR disruption of this locus in D. pealeii embryos/hatchlings. (crawford2020highlyefficientknockout pages 8-10, crawford2020highlyefficientknockout pages 1-3)

2. Key concepts and current biochemical understanding

2.1 Definition and catalytic reaction

Tryptophan 2,3-dioxygenase (TDO; EC 1.13.11.11) is a heme-containing dioxygenase that catalyzes oxidative cleavage of the indole ring of L-tryptophan to yield N-formyl-L-kynurenine (NFK)—the first (often rate-limiting) committed step of the kynurenine pathway (KP). (alves2024thebiologyand pages 2-5)

Although TDO and indoleamine 2,3-dioxygenases (IDO1/IDO2) perform the same overall initial KP chemistry, they are described as differing in structure, substrate specificity, and tissue distribution, which affects biological roles across organisms. (alves2024thebiologyand pages 2-5)

2.2 Substrate specificity (inference relevant to squid)

A 2024 KP-focused review summarizes that (for human TDO as a well-studied reference) TDO shows high physiological specificity for L-tryptophan (with much lower activity on D-tryptophan), supporting the common annotation of TDO enzymes as primarily L-Trp oxygenases. (alves2024thebiologyand pages 5-6)

Given that D. pealeii TDO is experimentally tied to ommochrome pigmentation derived from tryptophan catabolism (Section 3), the most parsimonious functional annotation for UniProt A0A7G4RN94 is an L-tryptophan dioxygenase entering the kynurenine/ommochrome branch. (crawford2020highlyefficientknockout pages 1-3, alves2024thebiologyand pages 2-5)

2.3 Pathway context: kynurenine pathway → ommochrome pigments

In invertebrates, tryptophan catabolism through the Tryptophan → Ommochrome pathway produces ommochrome pigments (e.g., xanthommatin/ommatins) used in coloration and vision-related tissues. An authoritative synthesis in Biological Reviews identifies TDO (EC 1.13.11.11) as the enzyme catalyzing the first step of this pathway and lists heme as its cofactor in ommochrome biosynthesis contexts. (figon2019ommochromesininvertebrates pages 8-9, figon2019ommochromesininvertebrates pages 9-10)

3. Organism-specific functional evidence in Doryteuthis pealeii

3.1 Expression/localization: pigment-producing tissues

In D. pealeii embryos, fluorescent in situ hybridization detected TDO mRNA in the developing eyes/retina and in punctate signals consistent with developing chromatophores on the mantle/arms. (crawford2020highlyefficientknockout pages 3-5, crawford2020highlyefficientknockout media 7a0753cd)

Complementing embryo spatial expression, adult tissue RNA-seq (as analyzed in the same study) indicated highest expression in retina and in the chromatophore layer of the skin, consistent with a role in local pigment precursor production. (crawford2020highlyefficientknockout pages 3-5)

3.2 Pharmacological perturbation supports enzymatic requirement

Treatment of embryos with the TDO-selective inhibitor 680C91 (reported regimen: 3.15 mM, from stage 20–27) “clearly blocked pigmentation” in both eyes and chromatophores, supporting that enzymatic TDO activity is upstream of ommochrome deposition in these tissues. (crawford2020highlyefficientknockout pages 1-3, crawford2020highlyefficientknockout pages 10-12)

3.3 Genetic perturbation (CRISPR-Cas9) establishes causality

CRISPR-Cas9 disruption of D. pealeii tdo produced a strong and reproducible loss-of-pigmentation phenotype in hatchlings, with near-complete loss of pigmentation in eyes and chromatophores, while the ink sac (melanin-based pigment) was unaffected—supporting specificity for tryptophan-derived ommochromes rather than melanin. (crawford2020highlyefficientknockout pages 1-3, crawford2020highlyefficientknockout pages 3-5, crawford2020highlyefficientknockout media 7a0753cd)

A peer-reviewed research highlight independently summarizes the same core observation: CRISPR targeting of TDO in D. pealeii yields marked loss/reduction of pigment in eyes and chromatophores, with reported knockout efficiencies >90% in genotyped embryos. (neff2020crisprincephalopods pages 1-1)

3.4 Quantitative genotyping statistics (key data)

Amplicon sequencing around CRISPR cut sites showed high on-target editing with quantitative metrics including:
- Individuals with >90% disruption at the tdo locus; across specimens, cumulative disruption about 30%–95%. (crawford2020highlyefficientknockout pages 5-7)
- Many distinct indel outcomes per embryo (mean 38 ± 13 events), with no single dominant allele (most frequent event around 15% ± 8%). (crawford2020highlyefficientknockout pages 5-7)
- Indel size distributions: sgRNA1 median deletion 9 nt / median insertion 2 bp; sgRNA2 median deletion 7 nt / median insertion 3 bp. (crawford2020highlyefficientknockout pages 5-7)

These quantitative results strengthen the genotype–phenotype link supporting TDO’s functional annotation in squid pigmentation. (crawford2020highlyefficientknockout pages 5-7, crawford2020highlyefficientknockout pages 1-3)

4. Cellular compartment and subcellular localization (what can be concluded)

Direct subcellular localization of squid TDO protein (e.g., cytosolic vs organellar) was not established by protein-level localization in the retrieved D. pealeii sources; however, within the ommochrome pathway literature (in insects as the best-established reference), TDO is discussed as acting early in tryptophan catabolism and is contrasted with downstream steps having mitochondrial association (e.g., kynurenine monooxygenase in some systems). (cordell2021biosynthesisofthe pages 4-6)

Therefore, for UniProt A0A7G4RN94, the most supportable localization statement from available evidence is tissue-level localization to retina and chromatophore-bearing skin, with subcellular localization remaining an inference rather than squid-specific experimental fact. (crawford2020highlyefficientknockout pages 3-5, crawford2020highlyefficientknockout media 7a0753cd)

5. Recent developments (prioritizing 2023–2024) and latest research relevant to annotation

5.1 2024 synthesis of KP biochemistry clarifies conserved TDO properties

A 2024 review in International Journal of Molecular Sciences (Aug 2024) explicitly defines TDO (EC 1.13.11.11) as heme-containing and producing N-formyl-L-kynurenine, and emphasizes differences vs IDO enzymes—helpful for avoiding misannotation and for predicting substrate specificity (L-Trp preference) in non-model species. URL: https://doi.org/10.3390/ijms25169082 (alves2024thebiologyand pages 2-5, alves2024thebiologyand pages 5-6)

5.2 2024 chemistry of ommochrome products informs downstream functional context

A 2024 primary research article in JACS Au (Oct 2024) reports gram-scale biomimetic synthesis and characterization of ommatins (xanthommatin family) and compares antioxidant activities among ommatin derivatives; while not a gene study, it underscores continued growth of cephalopod-linked ommochrome chemistry and quantification of functional properties of pathway products. URL: https://doi.org/10.1021/jacsau.4c00667 (paper retrieved; see listing in search results)

5.3 Recent metabolic engineering and manufacturing directions (application context)

A recent preprint posted 2024-10-04 (bioRxiv record published Oct 2025) describes growth-coupled microbial biosynthesis of xanthommatin and uses a minimal two-gene module (TDO + kynurenine formamidase) as part of the conversion from L-tryptophan toward pigment precursors, illustrating practical implementation of the pathway for production. URL: https://doi.org/10.1101/2024.10.04.616593 (bushin2025growthcoupledmicrobialbiosynthesis pages 3-6)

6. Current applications and real-world implementations

6.1 Functional genetics toolkit in cephalopods

The D. pealeii work demonstrates an operational, high-efficiency CRISPR workflow in cephalopods using TDO pigmentation loss as a visible readout, enabling real-world deployment of genome editing in squid embryos for functional studies. (crawford2020highlyefficientknockout pages 1-3, neff2020crisprincephalopods pages 1-1)

6.2 Pigment pathway engineering and materials/chemistry applications

Ommochrome pigments (derived from the kynurenine branch initiated by TDO) are increasingly targeted for (i) synthetic access and characterization of optical/redox properties and (ii) biomanufacturing approaches for pigments, where upstream enzymes such as TDO define entry into the pathway. (bushin2025growthcoupledmicrobialbiosynthesis pages 3-6)

7. Expert synthesis / authoritative interpretation

An authoritative review of invertebrate ommochromes emphasizes that ommochromes arise from tryptophan catabolism through the “Tryptophan → Ommochrome pathway” and highlights TDO as the entry enzyme that opens the indole ring and governs flux into pigment biogenesis, as well as documenting cellular biology of ommochrome-producing organelles (ommochromasomes) and methodological advances enabling pathway dissection. URL: https://doi.org/10.1111/brv.12441 (figon2019ommochromesininvertebrates pages 8-9, figon2019ommochromesininvertebrates pages 9-10)

8. Visual evidence (from primary squid genetics study)

The retrieved figure panels directly support the two most important organism-specific claims:
- TDO expression in squid embryonic retina and chromatophores by FISH. (crawford2020highlyefficientknockout media 7a0753cd)
- Wild-type vs TDO knockout pigmentation loss in eyes/chromatophores. (crawford2020highlyefficientknockout media 12743825)

9. Consolidated evidence table (with quantitative values)

Evidence type Key findings Source (author year journal) URL Publication date Notes linking to UniProt A0A7G4RN94 and ommochrome/kynurenine pathway
Sequence/phylogeny D. pealeii tdo was identified by BLASTP using human TDO/IDO queries, aligned with MUSCLE, and placed by approximate maximum-likelihood phylogeny to distinguish TDO from related dioxygenases; locus mapped to the squid genome; authors report a single TDO gene with 13 exons spanning >120 kb and deposited the locus as GenBank MT648678 (crawford2020highlyefficientknockout pages 8-10, crawford2020highlyefficientknockout pages 1-3) Crawford et al. 2020, Current Biology https://doi.org/10.1016/j.cub.2020.06.099 Sep 2020 Strongly matches UniProt A0A7G4RN94 annotation as tryptophan 2,3-dioxygenase (EC 1.13.11.11) in Doryteuthis pealeii; phylogeny helps avoid confusion with vertebrate TDO2 or IDO paralogs (crawford2020highlyefficientknockout pages 8-10, crawford2020highlyefficientknockout pages 1-3)
Expression Fluorescent in situ hybridization in stage 22 embryos showed TDO transcript in developing eyes/retina and punctate signal in chromatophores on mantle and arms; adult RNA-seq showed highest expression in retina and the chromatophore layer of the skin (crawford2020highlyefficientknockout pages 3-5, crawford2020highlyefficientknockout media 7a0753cd) Crawford et al. 2020, Current Biology https://doi.org/10.1016/j.cub.2020.06.099 Sep 2020 Expression pattern fits a role in local ommochrome pigment production rather than general melanin synthesis, consistent with the squid UniProt family/domain assignment (crawford2020highlyefficientknockout pages 3-5, crawford2020highlyefficientknockout media 7a0753cd)
Pharmacology Treatment with the TDO-selective inhibitor 680C91 at 3.15 mM from stage 20 to stage 27 blocked pigmentation in both eyes and chromatophores (methods and summarized results reported) (crawford2020highlyefficientknockout pages 1-3, crawford2020highlyefficientknockout pages 10-12) Crawford et al. 2020, Current Biology https://doi.org/10.1016/j.cub.2020.06.099 Sep 2020 Pharmacologic phenocopy supports that squid TDO activity is required upstream of ommochrome deposition; this is consistent with TDO catalyzing entry into the kynurenine/ommochrome branch from tryptophan (crawford2020highlyefficientknockout pages 1-3, crawford2020highlyefficientknockout pages 10-12)
CRISPR phenotype CRISPR-Cas9 knockout of tdo in G0 embryos caused near-complete loss of pigmentation in hatchlings, with greatly reduced or absent pigment in eyes and chromatophores; earlier injections produced stronger whole-animal effects, later injections mosaic phenotypes; ink sac pigmentation was unaffected (crawford2020highlyefficientknockout pages 1-3, crawford2020highlyefficientknockout pages 3-5, crawford2020highlyefficientknockout media 7a0753cd) Crawford et al. 2020, Current Biology; Neff 2020, Lab Animal https://doi.org/10.1016/j.cub.2020.06.099 ; https://doi.org/10.1038/s41684-020-0655-5 Sep 2020; Sep 2020 This is the most direct functional evidence that the D. pealeii protein corresponding to UniProt A0A7G4RN94 is required for ommochrome-based pigmentation in chromatophores/eyes, not melanin in the ink sac (crawford2020highlyefficientknockout pages 1-3, crawford2020highlyefficientknockout pages 3-5, neff2020crisprincephalopods pages 1-1)
Genotyping stats Edited embryos showed >90% disruption in some individuals; cumulative tdo disruption ranged about 30%–95%; mean 38 ± 13 distinct indel events per animal; most frequent single event only about 15% ± 8%; median deletion/insertion sizes: sgRNA1 9 nt / 2 bp, sgRNA2 7 nt / 3 bp (crawford2020highlyefficientknockout pages 5-7, crawford2020highlyefficientknockout pages 3-5) Crawford et al. 2020, Current Biology https://doi.org/10.1016/j.cub.2020.06.099 Sep 2020 High on-target editing efficiency links genotype to pigment-loss phenotype and supports confident functional annotation of the squid TDO locus represented by UniProt A0A7G4RN94 (crawford2020highlyefficientknockout pages 5-7, crawford2020highlyefficientknockout pages 3-5)
Pathway context/biochemistry TDO is a heme-containing enzyme, EC 1.13.11.11, that catalyzes oxidative opening of the indole ring of L-tryptophan to N-formyl-L-kynurenine, the first and often rate-limiting step of the kynurenine pathway; TDO and IDO catalyze the same first reaction, but TDO is structurally distinct and generally more substrate-specific for L-tryptophan (alves2024thebiologyand pages 2-5, alves2024thebiologyand pages 5-6, figon2019ommochromesininvertebrates pages 9-10) de Fátima Alves et al. 2024, Int J Mol Sci; Figon & Casas 2019, Biological Reviews https://doi.org/10.3390/ijms25169082 ; https://doi.org/10.1111/brv.12441 Aug 2024; Jul 2019 For cephalopod pigmentation, this reaction supplies the kynurenine-derived precursors that feed the ommochrome pathway; thus the UniProt annotation of A0A7G4RN94 as TDO is biochemically coherent with the squid pigmentation phenotypes (alves2024thebiologyand pages 2-5, figon2019ommochromesininvertebrates pages 8-9, figon2019ommochromesininvertebrates pages 9-10)

Table: This table summarizes the main lines of evidence supporting functional annotation of Doryteuthis pealeii TDO, including identity verification, tissue expression, perturbation phenotypes, and conserved biochemistry. It is useful for linking UniProt A0A7G4RN94 to the kynurenine/ommochrome pigmentation pathway with quantitative support.

10. Summary functional annotation (UniProt A0A7G4RN94; D. pealeii)

Primary molecular function: Heme-dependent dioxygenase catalyzing oxidative cleavage of L-tryptophan → N-formyl-L-kynurenine (EC 1.13.11.11), initiating kynurenine-pathway flux that supplies precursors for ommochrome pigment synthesis. (alves2024thebiologyand pages 2-5, figon2019ommochromesininvertebrates pages 8-9, crawford2020highlyefficientknockout pages 1-3)

Biological process (squid evidence): Required for pigment formation in eyes/retina and chromatophores; disruption causes near-complete loss of pigmentation without affecting melanin-based ink pigment. (crawford2020highlyefficientknockout pages 1-3, crawford2020highlyefficientknockout pages 3-5, crawford2020highlyefficientknockout media 7a0753cd)

Localization (supported level): Enriched expression in pigment tissues (retina; chromatophore skin layer; embryonic chromatophores), consistent with localized pigment precursor biosynthesis. (crawford2020highlyefficientknockout pages 3-5, crawford2020highlyefficientknockout media 7a0753cd)

References (URLs and publication dates)

  • Crawford K. et al. Highly Efficient Knockout of a Squid Pigmentation Gene. Current Biology. Sep 2020. https://doi.org/10.1016/j.cub.2020.06.099 (crawford2020highlyefficientknockout pages 1-3, crawford2020highlyefficientknockout pages 5-7, crawford2020highlyefficientknockout pages 8-10, crawford2020highlyefficientknockout pages 3-5, crawford2020highlyefficientknockout media 7a0753cd, crawford2020highlyefficientknockout media 12743825)
  • Neff E.P. CRISPR in cephalopods yields the first knockout squid. Lab Animal. Sep 2020. https://doi.org/10.1038/s41684-020-0655-5 (neff2020crisprincephalopods pages 1-1)
  • de Fátima Alves L. et al. The Biology and Biochemistry of Kynurenic Acid, a Potential Nutraceutical with Multiple Biological Effects. International Journal of Molecular Sciences. Aug 2024. https://doi.org/10.3390/ijms25169082 (alves2024thebiologyand pages 2-5, alves2024thebiologyand pages 5-6)
  • Figon F., Casas J. Ommochromes in invertebrates: biochemistry and cell biology. Biological Reviews. Jul 2019. https://doi.org/10.1111/brv.12441 (figon2019ommochromesininvertebrates pages 8-9, figon2019ommochromesininvertebrates pages 9-10)
  • Cordell G.A., Daley S.-k. Biosynthesis of the Ommochromes and Papiliochromes. Records of Natural Products. Jun 2021. https://doi.org/10.25135/rnp.238.21.02.1988 (cordell2021biosynthesisofthe pages 4-6)
  • Bushin L.B. et al. Growth-coupled microbial biosynthesis of the animal pigment xanthommatin. bioRxiv (posted 2024-10-04; record Oct 2025). https://doi.org/10.1101/2024.10.04.616593 (bushin2025growthcoupledmicrobialbiosynthesis pages 3-6)

References

  1. (crawford2020highlyefficientknockout pages 8-10): Karen Crawford, Juan F. Diaz Quiroz, Kristen M. Koenig, Namrata Ahuja, Caroline B. Albertin, and Joshua J.C. Rosenthal. Highly efficient knockout of a squid pigmentation gene. Current Biology, 30:3484-3490.e4, Sep 2020. URL: https://doi.org/10.1016/j.cub.2020.06.099, doi:10.1016/j.cub.2020.06.099. This article has 83 citations and is from a highest quality peer-reviewed journal.

  2. (crawford2020highlyefficientknockout pages 1-3): Karen Crawford, Juan F. Diaz Quiroz, Kristen M. Koenig, Namrata Ahuja, Caroline B. Albertin, and Joshua J.C. Rosenthal. Highly efficient knockout of a squid pigmentation gene. Current Biology, 30:3484-3490.e4, Sep 2020. URL: https://doi.org/10.1016/j.cub.2020.06.099, doi:10.1016/j.cub.2020.06.099. This article has 83 citations and is from a highest quality peer-reviewed journal.

  3. (alves2024thebiologyand pages 2-5): Luana de Fátima Alves, J. B. Moore, and D. Kell. The biology and biochemistry of kynurenic acid, a potential nutraceutical with multiple biological effects. International Journal of Molecular Sciences, Aug 2024. URL: https://doi.org/10.3390/ijms25169082, doi:10.3390/ijms25169082. This article has 31 citations.

  4. (alves2024thebiologyand pages 5-6): Luana de Fátima Alves, J. B. Moore, and D. Kell. The biology and biochemistry of kynurenic acid, a potential nutraceutical with multiple biological effects. International Journal of Molecular Sciences, Aug 2024. URL: https://doi.org/10.3390/ijms25169082, doi:10.3390/ijms25169082. This article has 31 citations.

  5. (figon2019ommochromesininvertebrates pages 8-9): Florent Figon and Jérôme Casas. Ommochromes in invertebrates: biochemistry and cell biology. Biological Reviews, 94:156-183, Jul 2019. URL: https://doi.org/10.1111/brv.12441, doi:10.1111/brv.12441. This article has 119 citations and is from a domain leading peer-reviewed journal.

  6. (figon2019ommochromesininvertebrates pages 9-10): Florent Figon and Jérôme Casas. Ommochromes in invertebrates: biochemistry and cell biology. Biological Reviews, 94:156-183, Jul 2019. URL: https://doi.org/10.1111/brv.12441, doi:10.1111/brv.12441. This article has 119 citations and is from a domain leading peer-reviewed journal.

  7. (crawford2020highlyefficientknockout pages 3-5): Karen Crawford, Juan F. Diaz Quiroz, Kristen M. Koenig, Namrata Ahuja, Caroline B. Albertin, and Joshua J.C. Rosenthal. Highly efficient knockout of a squid pigmentation gene. Current Biology, 30:3484-3490.e4, Sep 2020. URL: https://doi.org/10.1016/j.cub.2020.06.099, doi:10.1016/j.cub.2020.06.099. This article has 83 citations and is from a highest quality peer-reviewed journal.

  8. (crawford2020highlyefficientknockout media 7a0753cd): Karen Crawford, Juan F. Diaz Quiroz, Kristen M. Koenig, Namrata Ahuja, Caroline B. Albertin, and Joshua J.C. Rosenthal. Highly efficient knockout of a squid pigmentation gene. Current Biology, 30:3484-3490.e4, Sep 2020. URL: https://doi.org/10.1016/j.cub.2020.06.099, doi:10.1016/j.cub.2020.06.099. This article has 83 citations and is from a highest quality peer-reviewed journal.

  9. (crawford2020highlyefficientknockout pages 10-12): Karen Crawford, Juan F. Diaz Quiroz, Kristen M. Koenig, Namrata Ahuja, Caroline B. Albertin, and Joshua J.C. Rosenthal. Highly efficient knockout of a squid pigmentation gene. Current Biology, 30:3484-3490.e4, Sep 2020. URL: https://doi.org/10.1016/j.cub.2020.06.099, doi:10.1016/j.cub.2020.06.099. This article has 83 citations and is from a highest quality peer-reviewed journal.

  10. (neff2020crisprincephalopods pages 1-1): Ellen P. Neff. Crispr in cephalopods yields the first knockout squid. Lab Animal, 49:292-292, Sep 2020. URL: https://doi.org/10.1038/s41684-020-0655-5, doi:10.1038/s41684-020-0655-5. This article has 0 citations and is from a peer-reviewed journal.

  11. (crawford2020highlyefficientknockout pages 5-7): Karen Crawford, Juan F. Diaz Quiroz, Kristen M. Koenig, Namrata Ahuja, Caroline B. Albertin, and Joshua J.C. Rosenthal. Highly efficient knockout of a squid pigmentation gene. Current Biology, 30:3484-3490.e4, Sep 2020. URL: https://doi.org/10.1016/j.cub.2020.06.099, doi:10.1016/j.cub.2020.06.099. This article has 83 citations and is from a highest quality peer-reviewed journal.

  12. (cordell2021biosynthesisofthe pages 4-6): Geoffrey A. Cordell and Sharna-kay Daley. Biosynthesis of the ommochromes and papiliochromes. Records of Natural Products, 15:420-432, Jun 2021. URL: https://doi.org/10.25135/rnp.238.21.02.1988, doi:10.25135/rnp.238.21.02.1988. This article has 5 citations and is from a peer-reviewed journal.

  13. (bushin2025growthcoupledmicrobialbiosynthesis pages 3-6): Leah B. Bushin, Tobias B. Alter, María V.G. Alván-Vargas, Lara Dürr, Elina C. Olson, Mariah J. Avila, Òscar Puiggené, Taehwan Kim, Leila F. Deravi, Adam M. Feist, Pablo I. Nikel, and Bradley S. Moore. Growth-coupled microbial biosynthesis of the animal pigment xanthommatin. bioRxiv, Oct 2025. URL: https://doi.org/10.1101/2024.10.04.616593, doi:10.1101/2024.10.04.616593. This article has 9 citations.

  14. (crawford2020highlyefficientknockout media 12743825): Karen Crawford, Juan F. Diaz Quiroz, Kristen M. Koenig, Namrata Ahuja, Caroline B. Albertin, and Joshua J.C. Rosenthal. Highly efficient knockout of a squid pigmentation gene. Current Biology, 30:3484-3490.e4, Sep 2020. URL: https://doi.org/10.1016/j.cub.2020.06.099, doi:10.1016/j.cub.2020.06.099. This article has 83 citations and is from a highest quality peer-reviewed journal.

Citations

  1. alves2024thebiologyand pages 2-5
  2. alves2024thebiologyand pages 5-6
  3. crawford2020highlyefficientknockout pages 3-5
  4. neff2020crisprincephalopods pages 1-1
  5. crawford2020highlyefficientknockout pages 5-7
  6. cordell2021biosynthesisofthe pages 4-6
  7. bushin2025growthcoupledmicrobialbiosynthesis pages 3-6
  8. crawford2020highlyefficientknockout pages 8-10
  9. crawford2020highlyefficientknockout pages 1-3
  10. figon2019ommochromesininvertebrates pages 8-9
  11. figon2019ommochromesininvertebrates pages 9-10
  12. crawford2020highlyefficientknockout pages 10-12
  13. https://doi.org/10.3390/ijms25169082
  14. https://doi.org/10.1021/jacsau.4c00667
  15. https://doi.org/10.1101/2024.10.04.616593
  16. https://doi.org/10.1111/brv.12441
  17. https://doi.org/10.1016/j.cub.2020.06.099
  18. https://doi.org/10.1038/s41684-020-0655-5
  19. https://doi.org/10.25135/rnp.238.21.02.1988
  20. https://doi.org/10.1016/j.cub.2020.06.099,
  21. https://doi.org/10.3390/ijms25169082,
  22. https://doi.org/10.1111/brv.12441,
  23. https://doi.org/10.1038/s41684-020-0655-5,
  24. https://doi.org/10.25135/rnp.238.21.02.1988,
  25. https://doi.org/10.1101/2024.10.04.616593,

📄 View Raw YAML

id: A0A7G4RN94
gene_symbol: TDO
product_type: PROTEIN
status: IN_PROGRESS
taxon:
  id: NCBITaxon:1051067
  label: Doryteuthis pealeii
description: >-
  Tryptophan 2,3-dioxygenase (TDO) is a heme-dependent oxidoreductase that catalyzes
  the first committed step in ommochrome pigment biosynthesis in D. pealeii, converting
  L-tryptophan to N-formylkynurenine via oxidative cleavage of the indole ring. TDO
  is expressed in the retina and chromatophore layer of the skin, the two principal
  ommochrome-pigmented tissues. Crawford et al. (2020) demonstrated that CRISPR-Cas9
  knockout of TDO in D. pealeii embryos efficiently eliminated pigmentation in both
  eyes and chromatophores with >90% disruption efficiency, while ink sac melanin
  pigmentation was unaffected. This was the first gene knockout achieved in any
  cephalopod. TDO inhibition with 680C91 also completely blocked pigmentation,
  confirming the enzyme is required for ommochrome synthesis. Notably, D. pealeii
  lacks an IDO (indoleamine 2,3-dioxygenase) ortholog, unlike Euprymna berryi where
  IDO can compensate for TDO loss. TDO belongs to the PANTHER family PTHR10138
  (Tryptophan 2,3-dioxygenase), is predicted to function as a homotetramer (dimer
  of dimers), and contains a single heme cofactor per subunit. The gene spans 13
  exons over 120 kb of genomic DNA.
existing_annotations:
- term:
    id: GO:0004833
    label: L-tryptophan 2,3-dioxygenase activity
  evidence_type: IEA
  original_reference_id: GO_REF:0000120
  review:
    summary: >-
      L-tryptophan 2,3-dioxygenase activity (EC 1.13.11.11) is the defining enzymatic
      function of TDO. This IEA annotation is based on combined automated methods
      (InterPro, ARBA, PANTHER, UniRule). In D. pealeii, Crawford et al. (2020)
      demonstrated that CRISPR-Cas9 knockout of TDO eliminated ommochrome pigmentation,
      and pharmacological inhibition with 680C91 (a TDO-selective inhibitor) blocked
      pigmentation in both eyes and chromatophores [PMID:32735817]. The UniProt entry
      confirms TDO catalyzes L-tryptophan + O2 = N-formylkynurenine (Rhea:RHEA:24536).
      Phylogenetic analysis confirmed this gene as a bona fide TDO (distinct from IDO)
      [PMID:32735817].
    action: ACCEPT
    reason: >-
      This is the core enzymatic function of TDO, supported by sequence homology,
      PANTHER family assignment (PTHR10138), HAMAP rule MF_03020, and functional
      knockout data in this species showing loss of ommochrome pigmentation.
    supported_by:
      - reference_id: PMID:32735817
        supporting_text: >-
          In invertebrates, Tryptophan, 2,3 Dioxygenase (TDO) catalyzes the first
          committed step in ommochrome biosynthesis, converting Tryptophan to
          N-Formylkyneurenine.
      - reference_id: PMID:32735817
        supporting_text: >-
          A phylogenetic comparison of this sequence with diverse TDOs, and
          indolamine-2,3-dioxygenases (a different enzyme that catalyzes the same
          reaction), supported its identity as TDO.
- term:
    id: GO:0006569
    label: L-tryptophan catabolic process
  evidence_type: IEA
  original_reference_id: GO_REF:0000117
  review:
    summary: >-
      L-tryptophan catabolic process is annotated via ARBA machine learning. TDO
      catalyzes the oxidative cleavage of L-tryptophan as the first step in the
      kynurenine pathway. Crawford et al. (2020) showed that TDO knockout eliminates
      ommochrome biosynthesis from tryptophan in D. pealeii [PMID:32735817]. This
      term is correct but could be more specific. The UniProt record lists both
      GO:0019441 (L-tryptophan catabolic process to kynurenine) and GO:0019442
      (L-tryptophan catabolic process to acetyl-CoA), and GO:0019441 more precisely
      captures TDO function as it catalyzes the first step to kynurenine specifically.
    action: ACCEPT
    reason: >-
      L-tryptophan catabolic process correctly describes the biological process TDO
      participates in. While a more specific term like L-tryptophan catabolic process
      to kynurenine (GO:0019441) would be ideal, that term is now obsolete in GO.
      GO:0006569 is the most appropriate active term for this function. Crawford et al.
      (2020) showed TDO knockout eliminates the tryptophan-to-ommochrome pathway in
      D. pealeii [PMID:32735817].
    supported_by:
      - reference_id: PMID:32735817
        supporting_text: >-
          TDO catalyzes the first committed step in ommochrome biosynthesis, converting
          Tryptophan to N-Formylkyneurenine.
- term:
    id: GO:0020037
    label: heme binding
  evidence_type: IEA
  original_reference_id: GO_REF:0000120
  review:
    summary: >-
      Heme binding is annotated by combined IEA methods (InterPro, ARBA, PANTHER,
      UniRule). The UniProt record explicitly states: "Binds 1 heme group per subunit"
      (HAMAP-Rule:MF_03020), and lists heme as a cofactor (ChEBI:30413). TDO is a
      heme-dependent dioxygenase, and heme is essential for its catalytic mechanism.
      This is well-established for TDO family members across all species.
    action: ACCEPT
    reason: >-
      Heme binding is integral to TDO catalytic function. The enzyme requires bound
      heme to catalyze oxidative cleavage of the tryptophan indole ring. This is
      confirmed by UniProt cofactor annotation and is a defining feature of the
      TDO family (HAMAP MF_03020, Pfam PF03301 Trp_dioxygenase).
    supported_by:
      - reference_id: PMID:32735817
        supporting_text: >-
          we determined whether a TDO-selective inhibitor
          (680C91) impeded pigmentation in developing embryos.
- term:
    id: GO:0046872
    label: metal ion binding
  evidence_type: IEA
  original_reference_id: GO_REF:0000002
  review:
    summary: >-
      Metal ion binding is annotated via InterPro2GO mapping (IPR037217). This is
      correct as TDO binds iron through its heme prosthetic group. However, this
      term is very generic and redundant with the more informative heme binding
      (GO:0020037) annotation already present, which more precisely captures the
      nature of the metal cofactor interaction.
    action: MARK_AS_OVER_ANNOTATED
    reason: >-
      While technically correct (TDO binds iron via heme), GO:0046872 (metal ion
      binding) is too generic to be informative. The heme binding annotation
      (GO:0020037) already captures this function at a more appropriate level of
      specificity. The metal ion binding term does not add useful functional
      information beyond what heme binding conveys.
- term:
    id: GO:0006727
    label: ommochrome biosynthetic process
  evidence_type: IDA
  original_reference_id: PMID:32735817
  review:
    summary: >-
      NEW annotation. Crawford et al. (2020) demonstrated by CRISPR-Cas9 knockout
      that TDO is required for ommochrome biosynthesis in D. pealeii. TDO knockout
      eliminated pigmentation in both chromatophores and eyes, which contain ommochrome
      pigments. The TDO-selective inhibitor 680C91 also blocked pigmentation.
      In situ hybridization confirmed TDO expression in chromatophore precursors
      and eyes. This is the most biologically meaningful annotation for this gene
      in cephalopods, as ommochrome pigmentation is the primary downstream
      biological process served by TDO in this organism.
    action: NEW
    reason: >-
      Ommochrome biosynthesis is the key biological process requiring TDO in
      cephalopods. CRISPR knockout and pharmacological inhibition both demonstrate
      TDO is essential for ommochrome production. This annotation is not present
      in the existing GOA set but is strongly supported by direct experimental
      evidence in this species.
    supported_by:
      - reference_id: PMID:32735817
        supporting_text: >-
          In cephalopods, the pigments in the eyes
          and chromatophores are ommochromes, a derivative of tryptophan
      - reference_id: PMID:32735817
        supporting_text: >-
          Knocking out TDO in squid embryos efficiently eliminated pigmentation. By
          precisely timing CRISPR-Cas9 delivery during early development, the degree
          of pigmentation could be finely controlled. Genotyping revealed knockout
          efficiencies routinely greater than 90%.
      - reference_id: PMID:32735817
        supporting_text: >-
          We added 680C91 to developing embryos at stage 20, and it clearly blocked
          pigmentation in both the eyes and chromatophores, with animals developing
          normally otherwise.
      - reference_id: PMID:29989284
        supporting_text: >-
          Ommochromes are widely occurring coloured molecules of invertebrates, arising
          from tryptophan catabolism through the so-called Tryptophan → Ommochrome pathway.
- term:
    id: GO:0043473
    label: pigmentation
  evidence_type: IMP
  original_reference_id: PMID:32735817
  review:
    summary: >-
      NEW annotation. Crawford et al. (2020) showed that TDO knockout by CRISPR-Cas9
      resulted in loss of pigmentation in D. pealeii embryos, with chromatophore and
      eye pigmentation eliminated. Ink sac melanin was unaffected, demonstrating TDO
      specifically contributes to ommochrome-based pigmentation. Ahuja et al. (2023)
      further showed in E. berryi that TDO knockout delays pigmentation and TDO+IDO
      double knockout produces complete albinism [PMID:37343558].
    action: NEW
    reason: >-
      Pigmentation is the primary phenotype affected by TDO loss of function. The
      knockout phenotype directly demonstrates involvement in pigmentation. This
      is a core biological role for TDO in cephalopods, where ommochrome pigments
      color the chromatophores and retina.
    supported_by:
      - reference_id: PMID:32735817
        supporting_text: >-
          pigmentation is completely absent from the chromatophores and is
          minimal in the eyes which are light red
      - reference_id: PMID:37343558
        supporting_text: >-
          The knockout of tdo in D. pealeii completely inhibited pigmentation but had
          little to no effect in E. berryi.
core_functions:
- description: >-
    TDO catalyzes the oxidative cleavage of L-tryptophan to N-formylkynurenine,
    the first committed step in the kynurenine pathway and ommochrome biosynthesis
    in D. pealeii. CRISPR-Cas9 knockout eliminated ommochrome pigmentation in both
    eyes and chromatophores with >90% efficiency, and pharmacological inhibition
    with 680C91 confirmed the enzyme is required. D. pealeii lacks an IDO ortholog,
    making TDO the sole enzyme for this reaction. TDO is a heme-dependent dioxygenase
    that binds one heme group per subunit. The downstream kynurenine pathway
    intermediates 3-hydroxykynurenine and xanthurenic acid serve as precursors for
    xanthommatin and related ommatin pigments deposited in specialized ommochromasomes
    within chromatophore and retinal pigment cells (PMID:29989284). The TDO-selective
    inhibitor 680C91 at 3.15 mM from stage 20-27 phenocopied the CRISPR knockout,
    confirming enzymatic activity is required upstream of ommochrome deposition.
    Genotyping of CRISPR-edited embryos showed a mean of 38 +/- 13 distinct indel
    events per animal, with no dominant allele, yet produced near-complete pigmentation
    loss, demonstrating the strong genotype-phenotype link. In E. berryi, TDO knockout
    alone produced only slightly delayed pigmentation due to IDO compensation, but
    TDO+IDO double knockout yielded complete albinism enabling the first in vivo
    calcium imaging of neural activity in a cephalopod (PMID:37343558).
  molecular_function:
    id: GO:0004833
    label: L-tryptophan 2,3-dioxygenase activity
  directly_involved_in:
  - id: GO:0006727
    label: ommochrome biosynthetic process
  - id: GO:0006569
    label: L-tryptophan catabolic process
  - id: GO:0043473
    label: pigmentation
  supported_by:
    - reference_id: PMID:32735817
      supporting_text: >-
        Tryptophan, 2,3 Dioxygenase (TDO) catalyzes
        the first committed step in ommochrome biosynthesis, converting Tryptophan to
        N-Formylkyneurenine
    - reference_id: PMID:32735817
      supporting_text: >-
        Knocking out TDO in squid embryos efficiently eliminated pigmentation
    - reference_id: PMID:37343558
      supporting_text: >-
        The knockout of tdo in D. pealeii completely inhibited pigmentation but had
        little to no effect in E. berryi.
references:
- id: GO_REF:0000002
  title: Gene Ontology annotation through association of InterPro records with GO terms
  findings: []
- id: GO_REF:0000117
  title: Electronic Gene Ontology annotations created by ARBA machine learning models
  findings: []
- id: GO_REF:0000120
  title: Combined Automated Annotation using Multiple IEA Methods
  findings: []
- id: PMID:32735817
  title: Highly Efficient Knockout of a Squid Pigmentation Gene
  findings:
    - statement: >-
        TDO was selected as a knockout target because ommochromes pigment cephalopod
        eyes and chromatophores, and TDO catalyzes the first committed step in their
        biosynthesis.
    - statement: >-
        A single TDO gene was identified in the D. pealeii genome, spanning 13 exons
        over 120 kb. Phylogenetic analysis confirmed the gene as a bona fide TDO
        distinct from IDO.
    - statement: >-
        In situ hybridization showed TDO expression in chromatophore precursors on
        arms and mantle, and in eyes; RNAseq confirmed highest expression in retina
        and chromatophore layer of skin.
    - statement: >-
        TDO-selective inhibitor 680C91 completely blocked pigmentation in both eyes
        and chromatophores, with animals developing normally otherwise.
    - statement: >-
        CRISPR-Cas9 knockout with two sgRNAs targeting exons 1 and 2 eliminated
        pigmentation with >90% disruption efficiency. Ink sac melanin was unaffected,
        confirming specificity for the ommochrome pathway.
    - statement: >-
        This was the first gene knockout achieved in any cephalopod.
- id: PMID:29989284
  title: "Ommochromes in invertebrates: biochemistry and cell biology"
  findings:
    - statement: >-
        Ommochromes are widely occurring coloured molecules of invertebrates, arising
        from tryptophan catabolism through the Tryptophan → Ommochrome pathway. They
        are mainly known to mediate compound eye vision, as well as reversible and
        irreversible colour patterning.
      supporting_text: >-
        Ommochromes are widely occurring coloured molecules of invertebrates, arising
        from tryptophan catabolism through the so-called Tryptophan to Ommochrome
        pathway.
    - statement: >-
        Ommochromasomes are the organelles where ommochromes are synthesised and stored,
        playing an important role in mediating ommochrome functions. They are part of
        the lysosome-related organelles (LROs) family, which includes vertebrate
        melanosomes.
      supporting_text: >-
        Ommochromasomes are the organelles where ommochromes are synthesised and stored.
        Hence, they play an important role in mediating ommochrome functions.
    - statement: >-
        Ommochromes may also be involved in cell homeostasis by detoxifying free
        tryptophan and buffering oxidative stress, in addition to their roles in
        pigmentation and vision.
      supporting_text: >-
        Ommochromes might also be involved in cell homeostasis by detoxifying free
        tryptophan and buffering oxidative stress.
- id: PMID:37343558
  title: Creation of an albino squid line by CRISPR-Cas9 and its application for
    in vivo functional imaging of neural activity
  findings:
    - statement: >-
        In E. berryi, TDO knockout alone did not eliminate pigmentation despite >90%
        disruption efficiency, due to compensation by IDO. D. pealeii genome lacks
        IDO orthologs, explaining why TDO knockout alone is sufficient in that species.
    - statement: >-
        E. berryi homozygous TDO knockout showed slightly delayed pigmentation during
        development. TDO+IDO double knockout produced complete albinism.
    - statement: >-
        TDO expression in E. berryi is approximately 20-fold higher than IDO in
        stage 24 embryos. TDO is expressed in eyes and chromatophores, similar to
        D. pealeii.
    - statement: >-
        Albino E. berryi enabled the first in vivo calcium imaging of neural activity
        in a cephalopod using two-photon microscopy.
suggested_questions:
  - question: >-
      Does D. pealeii TDO have any role in tryptophan catabolism beyond ommochrome
      biosynthesis (e.g. kynurenine pathway metabolites for immune or neural signaling)?
    experts:
      - Rosenthal JJC
      - Albertin CB
  - question: >-
      What are the consequences of partial TDO loss on chromatophore function and
      dynamic color change in adult squid?
    experts:
      - Crawford K
  - question: >-
      Is there any post-translational regulation of TDO activity in cephalopods, as
      seen with substrate activation in mammalian TDO?
    experts: []
suggested_experiments:
  - description: >-
      Characterize the enzymatic kinetics of recombinant D. pealeii TDO, including
      heme stoichiometry and substrate specificity, to confirm in vitro activity.
    experiment_type: biochemistry
    hypothesis: >-
      D. pealeii TDO has similar catalytic properties to mammalian TDO, with
      strict specificity for L-tryptophan over other indoleamine substrates.
  - description: >-
      Use single-cell RNA-seq to map TDO expression across chromatophore subtypes
      and developmental stages in D. pealeii embryos.
    experiment_type: transcriptomics
    hypothesis: >-
      TDO expression is restricted to ommochrome-producing cell types (chromatophores
      and retinal pigment cells) and onset correlates with pigmentation timing.
  - description: >-
      Measure kynurenine pathway metabolite levels (N-formylkynurenine, kynurenine,
      3-hydroxykynurenine, xanthurenic acid) in TDO knockout vs wildtype D. pealeii
      embryos by LC-MS/MS.
    experiment_type: metabolomics
    hypothesis: >-
      TDO knockout eliminates kynurenine pathway flux entirely in D. pealeii due to
      the absence of IDO, unlike in E. berryi where IDO provides compensation.
  - description: >-
      Test whether partial TDO knockout in adult squid affects chromatophore
      expansion dynamics and camouflage behavior using video analysis.
    experiment_type: behavioral/physiological
    hypothesis: >-
      Reduced ommochrome content from partial TDO loss impairs chromatophore
      opacity and dynamic range of color change.