TUD1

UniProt ID: Q10PI9
Organism: Oryza sativa subsp. japonica
Review Status: COMPLETE
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Gene Description

TUD1 (Q10PI9; TAIHU DWARF1 / ERECT LEAF1 / OsPUB75; U-box domain-containing protein 75) is a rice plant U-box (PUB) E3 ubiquitin ligase (EC 2.3.2.27) that acts as a positive regulator of brassinosteroid (BR)-mediated growth and plant architecture. The 459-aa, single-exon protein has an N-terminal U-box domain (residues 64-138) required for catalytic E3 activity, followed by ARMADILLO (ARM) repeats that mediate protein-protein interactions and substrate recruitment. Recombinant GST-TUD1 has in vitro ubiquitination (E3 ligase) activity, and loss-of-function point mutants lack this activity, showing it is essential for function (Hu et al. 2013, PMID:23526892; Sakamoto et al. 2013, PMID:24299927). TUD1::sGFP localizes predominantly to the plasma membrane. Mechanistically, TUD1 physically interacts with the rice heterotrimeric G-protein alpha subunit D1/RGA1 (UniProt GPA1) - shown by BiFC, yeast two-hybrid and GST pull-down - and is genetically epistatic to d1, placing TUD1 downstream of D1 in a Galpha-mediated BR signaling pathway that runs parallel to / partly overlaps the canonical OsBRI1/D61 receptor-kinase pathway (tud1 is additive with d61). Unlike a merely BR-responsive gene, TUD1 is therefore a genuine BR signaling-pathway COMPONENT: it transduces the BR/G-protein signal via regulated ubiquitination, and a later mechanistic study reports TUD1 promotes BR-induced degradation of the GSK3/SHAGGY-like kinase GSK2 (a central negative BR regulator) (Liu et al. 2025, deep-research file). tud1/elf1 loss-of-function mutants are BR-insensitive dwarfs with erect, dark-green leaves and short grains (grain length reduced ~30-44%); the dwarfism is due mainly to decreased cell proliferation and disorganized cell files in aerial organs rather than reduced cell elongation. tud1 mutants show normal GA and cytokinin responses, so the function is BR-specific. The protein's core molecular function is U-box/ARM E3 ubiquitin-protein ligase activity; its core biological role is (positive) regulation of the BR-mediated signaling pathway controlling cell proliferation and plant growth.

Existing Annotations Review

GO Term Evidence Action Reason
GO:0009742 brassinosteroid mediated signaling pathway
IEA
GO_REF:0000043
ACCEPT
Summary: SPKW (GO_REF:0000043) annotation derived from the UniProt keyword "Brassinosteroid signaling pathway"; snapshot-only, removed in the current GOA release when the keyword2GO pipeline was retired for cellular organisms. UNLIKE many keyword-derived hormone-RESPONSE annotations, this one is biologically CORRECT: TUD1 is a bona-fide COMPONENT of the BR signaling pathway, not merely a BR-responsive gene. It physically interacts with the Galpha subunit D1/RGA1 and is genetically epistatic to d1, acting downstream of D1 in a Galpha-mediated BR signaling pathway, and is a positive regulator of BR signaling whose loss makes plants BR-insensitive.
Reason: This is the LEGITIMATE-component case for an SPKW process keyword (cf. DELLA/RHT1 and other genuine signaling-pathway members), and GOA's removal of it was arguably COLLATERAL DAMAGE rather than a justified correction. Multiple orthogonal experiments place TUD1 inside the BR signaling pathway: (i) TUD1 and the Galpha subunit D1 directly interact (BiFC, yeast two-hybrid, GST pull-down) and tud1 is epistatic to d1, so TUD1 acts downstream of D1 in a Galpha-mediated BR pathway [PMID:23526892]; (ii) tud1/elf1 mutants are BR-insensitive (reduced lamina-joint bending and seminal-root inhibition across a 24-eBL dose series) and TUD1/ELF1 is a positive regulator of BR signaling [PMID:23526892, PMID:24299927]; (iii) tud1 mutants have normal GA and cytokinin responses, so the role is BR-specific [PMID:23526892]. The current GOA retains the more precise, experimentally grounded process term "regulation of brassinosteroid mediated signaling pathway" (GO:1900457, IBA+IMP), which is arguably a better representation of TUD1's regulatory role; "brassinosteroid mediated signaling pathway" (GO:0009742) is the broader parent denoting pathway membership. Because GO:1900457 survives in current GOA, removal of the broad GO:0009742 keyword term did NOT leave the gene without BR-process annotation, so this is not catastrophic collateral damage - but the keyword was nonetheless capturing real biology. Retain (ACCEPT) as a correct, if general, pathway-membership annotation; the regulatory framing is better captured by GO:1900457 and by the proposed positive-regulation term GO:1900459 below.
Supporting Evidence:
PMID:23526892
These results demonstrate that D1 and TUD1 act together to mediate a BR-signaling pathway.
PMID:23526892
indicating that tud1-5 was epistatic to d1-c
PMID:23526892
These results showed that TUD1 acts in the same genetic pathway as D1 but different from that involving the rice BRI1 ortholog D61.
PMID:24299927
imply that ELF1 functions as a positive regulator of brassinosteroid signaling in rice.
file:ORYSJ/TUD1/TUD1-deep-research-falcon.md
implying that G-protein signaling modulates a ubiquitination step important for BR growth outputs
GO:0005886 plasma membrane
IBA
GO_REF:0000033
ACCEPT
Summary: IBA annotation (is_active_in) propagated across the PUB phylogenetic group for plasma-membrane localization. Directly confirmed in rice by TUD1::sGFP imaging.
Reason: Well supported. The TUD1::sGFP fusion localizes predominantly to the plasma membrane in rice protoplasts, consistent with the UniProt subcellular location (cell membrane, peripheral membrane protein) and with TUD1 acting together with the plasma-membrane Galpha subunit D1 [PMID:23526892]. The is_active_in qualifier is appropriate because TUD1 carries out its BR-signaling E3 function at the plasma membrane.
Supporting Evidence:
PMID:23526892
The TUD1::sGFP fusion protein in rice protoplasts was mainly associated with the plasma membrane
file:ORYSJ/TUD1/TUD1-deep-research-falcon.md
TUD1::sGFP localized predominantly to the plasma membrane in rice protoplasts
GO:1900457 regulation of brassinosteroid mediated signaling pathway
IBA
GO_REF:0000033
ACCEPT
Summary: IBA annotation (involved_in) for regulation of the BR-mediated signaling pathway. This is the core biological process of TUD1 and is supported by direct rice genetics.
Reason: Core function, strongly supported. TUD1/ELF1 is a positive regulator of BR signaling: tud1/elf1 loss-of-function mutants are BR-insensitive, and the gene acts downstream of the Galpha subunit D1 in a BR signaling pathway [PMID:23526892, PMID:24299927]. This regulation-level process term is more precise and informative than the broad pathway term GO:0009742 (the retired SPKW keyword) and is the right level of specificity. The direction of regulation (positive) is captured by the proposed GO:1900459 below.
Supporting Evidence:
PMID:24299927
imply that ELF1 functions as a positive regulator of brassinosteroid signaling in rice.
PMID:23526892
These results demonstrate that D1 and TUD1 act together to mediate a BR-signaling pathway.
file:ORYSJ/TUD1/TUD1-deep-research-falcon.md
connecting G-protein-associated inputs to BR pathway throughput, likely via regulated degradation of negative regulators (GSK2)
GO:0004842 ubiquitin-protein transferase activity
IEA
GO_REF:0000120
ACCEPT
Summary: IEA annotation from ARBA/InterPro (IPR003613, U-box) for ubiquitin-protein transferase activity. TUD1 is a functional E3 ubiquitin ligase.
Reason: Correct and consistent with the demonstrated E3 ligase activity. Purified GST-TUD1 shows in vitro ubiquitination activity dependent on E1/E2, and the U-box is required [PMID:23526892, PMID:24299927]. "Ubiquitin-protein transferase activity" (GO:0004842) is essentially synonymous in usage with the more specific "ubiquitin protein ligase activity" (GO:0061630, IDA, retained); both correctly describe the EC 2.3.2.27 catalytic function. Accept the IEA as a valid computational corroboration of the experimentally demonstrated E3 activity.
Supporting Evidence:
PMID:23526892
Ubiquitination activity was observed for the purified GST-TUD1
PMID:24299927
ELF1 possessed E3 ubiquitin ligase activity in vitro.
GO:0005886 plasma membrane
IEA
GO_REF:0000044
ACCEPT
Summary: IEA annotation from the UniProt SubCell controlled-vocabulary mapping (SL-0039, Cell membrane) for plasma-membrane localization. Duplicates the IBA and IDA plasma-membrane annotations.
Reason: Correct. Maps the UniProt "Cell membrane" subcellular location to GO plasma membrane; consistent with the direct IDA evidence (TUD1::sGFP at the plasma membrane) [PMID:23526892]. Duplicate annotations with different evidence codes are acceptable.
Supporting Evidence:
PMID:23526892
The TUD1::sGFP fusion protein in rice protoplasts was mainly associated with the plasma membrane
GO:0016567 protein ubiquitination
IEA
GO_REF:0000120
ACCEPT
Summary: IEA annotation from ARBA/InterPro/UniPathway (IPR003613; UPA00143, protein ubiquitination) for the protein ubiquitination process. Duplicates the IDA annotation to the same term.
Reason: Correct. TUD1 is an E3 ubiquitin ligase that catalyzes protein ubiquitination (in vitro ubiquitination activity demonstrated) [PMID:23526892, PMID:24299927]; the UniProt PATHWAY line records "Protein modification; protein ubiquitination." The term accurately captures the molecular process the enzyme performs. Duplicate of the experimentally supported IDA annotation.
Supporting Evidence:
PMID:23526892
Ubiquitination activity was observed for the purified GST-TUD1
PMID:24299927
These results suggest that ELF1 ubiquitinates target proteins through an interaction mediated by ARM repeats.
GO:0061630 ubiquitin protein ligase activity
IEA
GO_REF:0000120
ACCEPT
Summary: IEA annotation from InterPro/EC (IPR045185 PUB22/23/24-like; EC:2.3.2.27) for ubiquitin protein ligase activity. Duplicates the IDA annotation to the same term.
Reason: Correct core molecular function. The E3 ubiquitin ligase activity is demonstrated experimentally (in vitro ubiquitination by GST-TUD1, abolished in catalytically dead mutants) [PMID:23526892, PMID:24299927] and corresponds to the UniProt EC 2.3.2.27. Duplicate of the experimentally supported IDA annotation; accept.
Supporting Evidence:
PMID:23526892
Ubiquitination activity was observed for the purified GST-TUD1
PMID:24299927
ELF1 possessed E3 ubiquitin ligase activity in vitro.
GO:0005886 plasma membrane
IDA
PMID:23526892
The U-box E3 ubiquitin ligase TUD1 functions with a heterotr...
ACCEPT
Summary: IDA annotation: TUD1::sGFP localizes predominantly to the plasma membrane in rice protoplasts. This is the experimentally demonstrated, core subcellular location.
Reason: Directly supported. In an in-vivo targeting assay the TUD1::sGFP fusion in rice protoplasts was mainly associated with the plasma membrane, the same compartment as its interactor D1 [PMID:23526892]. This is a core cellular-component annotation consistent with TUD1 acting at the plasma membrane in BR/G-protein signaling.
Supporting Evidence:
PMID:23526892
The TUD1::sGFP fusion protein in rice protoplasts was mainly associated with the plasma membrane
GO:0016567 protein ubiquitination
IDA
PMID:24299927
An E3 ubiquitin ligase, ERECT LEAF1, functions in brassinost...
ACCEPT
Summary: IDA annotation: ELF1/TUD1 catalyzes protein ubiquitination, demonstrated by in vitro E3 ligase activity. Core molecular process of the gene.
Reason: Well supported by direct experimental evidence. ELF1/TUD1 possesses E3 ubiquitin ligase activity in vitro and is proposed to ubiquitinate target proteins through an ARM-repeat-mediated interaction [PMID:24299927]; Hu et al. independently showed ubiquitination activity of purified GST-TUD1 [PMID:23526892]. Protein ubiquitination is the core process performed by this E3 enzyme.
Supporting Evidence:
PMID:24299927
ELF1 possessed E3 ubiquitin ligase activity in vitro.
PMID:24299927
These results suggest that ELF1 ubiquitinates target proteins through an interaction mediated by ARM repeats.
GO:0061630 ubiquitin protein ligase activity
IDA
PMID:24299927
An E3 ubiquitin ligase, ERECT LEAF1, functions in brassinost...
ACCEPT
Summary: IDA annotation: ELF1/TUD1 has E3 ubiquitin ligase activity in vitro. This is the core molecular function of the gene.
Reason: Core function, directly demonstrated. ELF1 possessed E3 ubiquitin ligase activity in vitro [PMID:24299927]; Hu et al. likewise showed ubiquitination activity for purified GST-TUD1, abolished in tud1-1/tud1-3/tud1-4 mutant proteins, establishing that the E3 activity is essential for function [PMID:23526892]. This is the central MF for TUD1.
Supporting Evidence:
PMID:24299927
ELF1 possessed E3 ubiquitin ligase activity in vitro.
PMID:23526892
tud1-1, tud1-3 and tud1-4 proteins did not possess any apparent E3 ligase activity
PMID:23526892
showing that the ubiquination activity of TUD1 is essential for its function
GO:1900457 regulation of brassinosteroid mediated signaling pathway
IMP
PMID:24299927
An E3 ubiquitin ligase, ERECT LEAF1, functions in brassinost...
ACCEPT
Summary: IMP annotation: elf1/tud1 loss-of-function mutants are BR-insensitive, demonstrating that the gene regulates the BR signaling pathway. Core biological process.
Reason: Core function, supported by mutant phenotype. The spontaneous elf1-1 mutant produces a BR-insensitive dwarf phenotype with erect leaves and short grains, and physiological analyses indicate ELF1 is a positive regulator of BR signaling [PMID:24299927]; Hu et al. independently showed tud1 mutants are BR-insensitive and act downstream of D1 [PMID:23526892]. The IMP correctly captures the gene's regulatory role in the BR pathway. The positive direction is captured by the proposed GO:1900459 below.
Supporting Evidence:
PMID:24299927
Physiological analyses suggested that elf1-1 is brassinosteroid-insensitive, so we hypothesized that ELF1 encodes a positive regulator of brassinosteroid signaling.
PMID:24299927
imply that ELF1 functions as a positive regulator of brassinosteroid signaling in rice.
GO:0005515 protein binding
IPI
PMID:23526892
The U-box E3 ubiquitin ligase TUD1 functions with a heterotr...
MODIFY
Summary: IPI annotation (with UniProtKB:Q0DJ33, the rice heterotrimeric G-protein alpha subunit D1/RGA1/GPA1) using the uninformative generic term "protein binding". The specific, experimentally demonstrated interaction is with the Galpha subunit.
Reason: "Protein binding" (GO:0005515) is an uninformative catch-all term and is discouraged by curation guidelines. The actual binding partner is well defined: TUD1 directly and physically interacts with the rice heterotrimeric G-protein alpha subunit D1 (UniProtKB:Q0DJ33; UniProt name GPA1), shown by BiFC, yeast two-hybrid and GST pull-down [PMID:23526892]. This interaction is the mechanistic basis for TUD1's role downstream of D1 in BR signaling. The annotation should be MODIFIED to the specific, informative term "G-protein alpha-subunit binding" (GO:0001965), which precisely captures the demonstrated interaction.
Proposed replacements: G-protein alpha-subunit binding
Supporting Evidence:
PMID:23526892
Based on these results, we concluded that TUD1 physically interacts with D1.
PMID:23526892
Furthermore, we found that D1 directly interacts with TUD1.
PMID:23526892
We subsequently detected that both the GDP- and GTPΞ³S-bound forms of D1 have similar binding ability to GST-TUD1, whereas no binding occurred to GST alone
file:ORYSJ/TUD1/TUD1-deep-research-falcon.md
TUD1 binds both GDP- and GTPΞ³S-bound D1 similarly; tud1 is epistatic to d1, placing TUD1 downstream of D1 in a BR-related G-protein pathway
GO:1900459 positive regulation of brassinosteroid mediated signaling pathway
IMP
PMID:24299927
An E3 ubiquitin ligase, ERECT LEAF1, functions in brassinost...
NEW
Summary: TUD1/ELF1 is a POSITIVE regulator of BR signaling; the direction of regulation is not captured by the existing GO:1900457 (unsigned "regulation of...") annotations and should be added.
Reason: Both primary studies conclude TUD1/ELF1 is a positive regulator of the BR signaling pathway: loss-of-function mutants are BR-insensitive dwarfs, and ELF1 "functions as a positive regulator of brassinosteroid signaling in rice" [PMID:24299927]; TUD1 acts as a BR-signaling activator downstream of D1 [PMID:23526892]. The current GOA only has the unsigned regulation term (GO:1900457); the more specific "positive regulation of brassinosteroid mediated signaling pathway" (GO:1900459) better captures the demonstrated activating role. IMP is justified by the BR-insensitivity of the loss-of-function tud1/elf1 alleles.
Supporting Evidence:
PMID:24299927
imply that ELF1 functions as a positive regulator of brassinosteroid signaling in rice.
PMID:23526892
TUD1 is a functional E3 ligase and acts as a BR signaling activator.
GO:0001965 G-protein alpha-subunit binding
IPI
PMID:23526892
The U-box E3 ubiquitin ligase TUD1 functions with a heterotr...
NEW
Summary: TUD1 directly binds the rice Galpha subunit D1/RGA1. This specific molecular function replaces the vague "protein binding" IPI and should be added explicitly.
Reason: The single experimentally demonstrated protein interactor of TUD1 is the heterotrimeric G-protein alpha subunit D1 (UniProtKB:Q0DJ33 / GPA1), confirmed by three orthogonal assays (BiFC, yeast two-hybrid, GST pull-down) [PMID:23526892]. "G-protein alpha-subunit binding" (GO:0001965) is the accurate, informative MF and is the proposed replacement for the generic GO:0005515 "protein binding". IPI is justified by the physical-interaction assays with D1.
Supporting Evidence:
PMID:23526892
Based on these results, we concluded that TUD1 physically interacts with D1.
PMID:23526892
We subsequently detected that both the GDP- and GTPΞ³S-bound forms of D1 have similar binding ability to GST-TUD1, whereas no binding occurred to GST alone
GO:0042127 regulation of cell population proliferation
IMP
PMID:23526892
The U-box E3 ubiquitin ligase TUD1 functions with a heterotr...
NEW
Summary: The dwarf phenotype of tud1 is caused mainly by decreased cell proliferation (reduced cell number) in aerial organs, implicating TUD1 in (positive) regulation of cell proliferation downstream of BR signaling.
Reason: Histological analysis showed the dwarfism of tud1 is due mainly to decreased cell proliferation and disorganized cell files in aerial organs - cell number was reduced (e.g. ~43% in the third leaf sheath, ~67% in the third internode) while average cell length was largely unchanged [PMID:23526892]. This links TUD1 (via BR signaling) to the control of cell proliferation, a process not captured by the existing annotations. "Regulation of cell population proliferation" (GO:0042127) is the appropriate term; this is a downstream developmental consequence of TUD1's BR-signaling role and would be classified as non-core. IMP is justified by the loss-of-function cell-number phenotype.
Supporting Evidence:
PMID:23526892
the dwarf phenotype of tud1 is mainly due to decreased cell proliferation and disorganized cell files in aerial organs
PMID:23526892
These results indicated that tud1 has a significantly reduced cell number in these aerial plant organs.

Core Functions

TUD1/ELF1/OsPUB75 is a plant U-box (PUB) E3 ubiquitin ligase. Via its N-terminal U-box domain it catalyzes the transfer of ubiquitin to substrate proteins (EC 2.3.2.27), with the ARM repeats providing substrate-recognition/interaction surfaces. This E3 ligase activity is essential for the gene's biological function.

Directly Involved In:
Cellular Locations:
Supporting Evidence:

TUD1 is a positive regulator and bona-fide component of the brassinosteroid-mediated signaling pathway in rice. It binds the heterotrimeric G-protein alpha subunit D1/RGA1 at the plasma membrane and acts genetically downstream of D1, transducing the BR/G-protein signal through regulated ubiquitination (a candidate substrate being the negative regulator GSK2). Loss of TUD1 renders plants BR-insensitive.

Supporting Evidence:
  • PMID:23526892
    These results demonstrate that D1 and TUD1 act together to mediate a BR-signaling pathway.
  • PMID:24299927
    imply that ELF1 functions as a positive regulator of brassinosteroid signaling in rice.
  • file:ORYSJ/TUD1/TUD1-deep-research-falcon.md
    implying that G-protein signaling modulates a ubiquitination step important for BR growth outputs

Through its role in BR signaling, TUD1 promotes cell proliferation and normal plant growth and architecture (stature, leaf angle, grain length). Loss-of-function tud1/elf1 mutants are dwarfs with erect leaves and short grains, with the dwarfism caused mainly by reduced cell number in aerial organs. This is a downstream developmental output of the core BR-signaling function and is non-core.

Supporting Evidence:
  • PMID:23526892
    the dwarf phenotype of tud1 is mainly due to decreased cell proliferation and disorganized cell files in aerial organs
  • PMID:24299927
    A spontaneous rice mutant, erect leaf1 (elf1-1), produced a dwarf phenotype with erect leaves and short grains.

References

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Suggested Questions for Experts

Q: What is the full in vivo substrate set of TUD1, beyond the candidate GSK2, and which substrates mediate the cell-proliferation versus cell-organization defects?

Suggested experts: Yongbiao Xue

Q: How does D1/RGA1 (which binds both GDP- and GTP-bound) regulate TUD1 E3 ligase activity at the plasma membrane - does nucleotide state modulate substrate ubiquitination?

Suggested experts: Hongning Tong

Suggested Experiments

Experiment: Identify TUD1 ubiquitination substrates in vivo by combining ubiquitin-pulldown proteomics in tud1 versus wild type with in vitro ubiquitination assays, and test BR- and D1-dependence of GSK2 turnover in tud1 mutants.

Hypothesis: TUD1 ubiquitinates GSK2 (and possibly other negative BR regulators), and BR-induced GSK2 degradation requires functional TUD1.

Type: ubiquitinome proteomics and in vitro/in vivo degradation assay

Experiment: Reconstitute the TUD1-D1 module and test whether D1 nucleotide state (GDP vs GTPgammaS) alters TUD1 E3 ligase activity or substrate selection in vitro, and whether membrane association is required.

Hypothesis: D1 binding modulates TUD1 catalytic output, coupling G-protein signaling to substrate ubiquitination in the BR pathway.

Type: in vitro reconstituted ubiquitination assay

Deep Research

Falcon

(TUD1-deep-research-falcon.md)

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