Strigolactone perception and D14-MAX2-SMXL signalling in shoot-branching control

Strigolactones (SLs) are carotenoid-derived hormones that inhibit axillary bud outgrowth. In Arabidopsis thaliana, SL is perceived by the alpha/beta-hydrolase receptor DWARF14 (D14), which binds and slowly hydrolyses the butenolide D-ring. SL binding changes the conformation of D14 so that it associates with the F-box protein MORE AXILLARY GROWTH2 (MAX2) in an SCF(MAX2) E3 ubiquitin ligase and with the SMAX1-LIKE co-repressors SMXL6, SMXL7 and SMXL8. The SMXLs are then polyubiquitinated and degraded by the proteasome, and D14 itself is degraded as negative feedback. In the absence of SL, the nuclear SMXL6/7/8 proteins repress target genes by recruiting TOPLESS-related co-repressors through an EAR motif, and SMXL6 can also bind target promoters itself. Their removal de-represses the bud-expressed TCP transcription factor BRANCHED1 (BRC1), which keeps buds dormant, in part by activating HD-ZIP genes that raise abscisic acid in the bud. SL-triggered SMXL degradation also reduces PIN1 accumulation and auxin transport in the stem, which inhibits bud activation in parallel with BRC1. The sister karrikin pathway uses the same F-box protein, MAX2, with the D14 paralog KAI2 and the SMAX1/SMXL2 repressors. That pathway, SL biosynthesis (D27, MAX3, MAX4, MAX1) and the auxin-transport branch are outside this module.

MODULE:strigolactone_signaling_shoot_branchingDRAFTCONCRETESignaling Pathwaymodules/strigolactone_signaling_shoot_branching.yaml
cellular response to strigolactoneGO:1902348 regulation of secondary shoot formationGO:2000032
PMID:26546446
Strigolactone Signaling in Arabidopsis Regulates Shoot Development by Targeting D53-Like SMXL Repressor Proteins for Ubiquitination and Degradation.
The core Arabidopsis mechanism: SL-induced, D14- and MAX2-dependent ubiquitination and degradation of SMXL6/7/8, which repress transcription with TPR2 and repress BRC1.
in the presence of SLs , D14 binds and hydrolyzes the SLs , triggering the formation of a D14-SMXL-SCF MAX2 complex for the ubiquitination and degradation of SMXL6, 7, and 8
PMID:26546447
SMAX1-LIKE/D53 Family Members Enable Distinct MAX2-Dependent Responses to Strigolactones and Karrikins in Arabidopsis.
SMXL6/7/8 mediate SL responses and SMAX1 mediates karrikin responses through the shared F-box protein MAX2.
Our data indicate that SMAX1 and SMXL6,7,8 repress karrikin and strigolactone signaling, respectively, and suggest that all MAX2-dependent growth effects are mediated by degradation of SMAX1/SMXL proteins.
PMID:27479325
DWARF14 is a non-canonical hormone receptor for strigolactone.
SL induces a D14 conformational change and formation of the D14-MAX2/D3-ASK1 complex.
Here we report the crystal structure of the strigolactone-induced AtD14-D3-ASK1 complex
PMID:30643123
Strigolactone perception and deactivation by a hydrolase receptor DWARF14.
A catalytically inactive AtD14 still signals, so intact SL binding can activate the receptor; hydrolysis deactivates SL after signalling.
We also demonstrate that D14 can deactivate SLs by hydrolytic degradation after signal transmission.
PMID:32528176
Transcriptional regulation of strigolactone signalling in Arabidopsis.
SL controls shoot branching mainly through transcriptional activation of BRC1; SMXL6 binds DNA directly and autoregulates SMXL6/7/8.
these plant hormones regulate shoot branching, leaf shape and anthocyanin accumulation mainly through transcriptional activation of the BRANCHED 1, TCP DOMAIN PROTEIN 1 and PRODUCTION OF ANTHOCYANIN PIGMENT 1 genes
PMID:28289131
BRC1 expression regulates bud activation potential but is not necessary or sufficient for bud growth inhibition in Arabidopsis.
SL inhibits bud activation by acting in parallel on BRC1 transcription and on the shoot auxin transport network.
our data suggest a coherent feed-forward loop in which strigolactone treatment reduces the probability of bud activation by parallel effects on BRC1 transcription and the shoot auxin transport network

Concrete Arabidopsis instance; the rice orthologous pathway is D14-D3-D53 (PMID:24336200, PMID:24336215), and petunia/pea receptors are DAD2/RMS3. Annoton molecular functions match the core_functions of the D14, MAX2, SMXL6, SMXL7, SMXL8 and BRC1 gene reviews. Because GO has no strigolactone-specific receptor term, D14 is typed with signaling receptor activity (GO:0038023), and the D14 review proposes a new term, strigolactone receptor activity. GO also has no strigolactone signalling pathway term, so the module concept is cellular response to strigolactone (GO:1902348). SMXL6, SMXL7 and SMXL8 are modelled as three redundant annotons on one co-repressor node instead of a PANTHER family descriptor: their shared PANTHER family (PTHR43572, CLPD chaperone) is far broader than the SMXL6/7/8 clade. No GO-CAM in gocams/index.tsv contains these proteins. The ASK1 and CUL1 SCF scaffold subunits and the TOPLESS/TPR2 co-repressors are named in prose but not modelled as parts, because they are shared with many other hormone pathways. No Falcon deep research could be generated (all providers failed).

5Nodes
4Parts
0Variant Sets
0Variants
7Annotons
3Connections

Derived QC

Recommended-field compliance

100.0% recommended fields populated

All recommended fields populated.

Module deep research

✗ none found

No MODULE:strigolactone_signaling_shoot_branching deep-research report alongside the module YAML.

Leaf nodes lacking representative members

✓ every leaf node grounds to a representative protein.

Template conformance

✓ every declared conforms_to bundle matches its template motif.

Function consistency and core coverage

7 gene-function check(s) reflected in core functions · 0 conflict(s) · 0 evidence or coverage gap(s) (7 comparison(s))

Retained noncore functions are reported separately; they do not require promotion to core functions. Support from representative genes does not establish conservation across the whole family. Missing reviews or identifiers leave a claim unverified.

AnnotonParticipantFunctionAssessment
d14_sl_receptor D14 (AtD14, At3g03990)
UniProtKB:Q9SQR3
Gene
signaling receptor activity (strigolactone receptor)
GO:0038023
Core Supported
The GO molecular function is reflected in core_functions (exact term or a reviewed subclass).
d14_sl_hydrolase D14 (AtD14, At3g03990)
UniProtKB:Q9SQR3
Gene
carboxylic ester hydrolase activity (SL butenolide hydrolysis)
GO:0052689
Core Supported
The GO molecular function is reflected in core_functions (exact term or a reviewed subclass).
max2_f_box_adaptor MAX2 (ORE9, At2g42620)
UniProtKB:Q9SIM9
Gene
ubiquitin-like ligase-substrate adaptor activity
GO:1990756
Core Supported
The GO molecular function is reflected in core_functions (exact term or a reviewed subclass).
smxl6_corepressor SMXL6 (At1g07200)
UniProtKB:Q9LML2
Gene
transcription corepressor activity
GO:0003714
Core Supported
The GO molecular function is reflected in core_functions (exact term or a reviewed subclass).
smxl7_corepressor SMXL7 (At2g29970)
UniProtKB:O80875
Gene
transcription corepressor activity
GO:0003714
Core Supported
The GO molecular function is reflected in core_functions (exact term or a reviewed subclass).
smxl8_corepressor SMXL8 (At2g40130)
UniProtKB:F4IGZ2
Gene
transcription corepressor activity
GO:0003714
Core Supported
The GO molecular function is reflected in core_functions (exact term or a reviewed subclass).
brc1_tcp_tf BRC1 (TCP18, At3g18550)
UniProtKB:A1YKT1
Gene
DNA-binding transcription factor activity
GO:0003700
Core Supported
The GO molecular function is reflected in core_functions (exact term or a reviewed subclass).

Feedback loops (advisory, prose-driven: a regulator counts as "feedback" when its own description says so)

✓ every negative regulator described as feedback has an upstream edge closing the loop.

  • smxl_ubiquitination ⊣ smxl_corepression [closed]
    smxl_ubiquitination is regulated by sl_perception: feedback loop closed
  • smxl_corepression ⊣ brc1_output [input]
    smxl_corepression is a negative regulator with no upstream edge (not described as feedback)

Gene-review completeness (6/6 grounded genes reviewed)

6 complete review(s) · 0 with deep research · 0 missing review · 6 reviewed but lacking deep research

Gene Review Complete Deep research
D14 Q9SQR3 ✓ ✓ ✗
MAX2 Q9SIM9 ✓ ✓ ✗
SMXL6 Q9LML2 ✓ ✓ ✗
SMXL7 O80875 ✓ ✓ ✗
SMXL8 F4IGZ2 ✓ ✓ ✗
TCP18 A1YKT1 ✓ ✓ ✗

Details

Context
Arabidopsis thalianaNCBITaxon:3702
nucleusGO:0005634 cytoplasmGO:0005737
Strigolactone D14-MAX2-SMXL signalling controlling shoot branchingSignaling Pathwaystrigolactone_signaling_shoot_branching

SL perception by D14 leads to SCF(MAX2)-dependent degradation of SMXL6/7/8 co-repressors, de-repressing the TCP factor BRC1 to keep axillary buds dormant.

cellular response to strigolactoneGO:1902348 regulation of secondary shoot formationGO:2000032
Context
Arabidopsis thalianaNCBITaxon:3702
nucleusGO:0005634 cytoplasmGO:0005737

Connections

sl_perception -> smxl_ubiquitination Positively Regulates
SL-bound D14 recruits MAX2 and the SMXLs, so SCF(MAX2) can ubiquitinate the SMXLs.
PMID:26546446
SMXL6 ubiquitination after GR24 treatment is lost in d14-1 and max2-1.
the ubiquitination of SMXL6-GFP was detected in 35S:SMXL6-GFP seedlings but not in 35S:SMXL6-GFP/max2-1 and 35S:SMXL6-GFP/d14-1 seedlings
smxl_ubiquitination -> smxl_corepression Negatively Regulates
Ubiquitination leads to proteasomal degradation of the SMXL co-repressors.
PMID:26546446
GR24 causes ubiquitination and degradation of SMXL6/7/8 that requires D14 and MAX2.
Exogenous application of the SL analog rac-GR24 causes ubiquitination and degradation of SMXL6, 7, and 8; this requires D14 and MAX2.
smxl_corepression -> brc1_output Negatively Regulates
SMXL6/7/8 repress BRC1 transcription in axillary buds.
PMID:26546446
BRC1 is repressed in max mutants and induced in smxl6/7/8 mutants.
the BRC1 gene was strongly repressed in max2-1 and max3-9 but was induced in smxl6/7/8
Part 1: strigolactone perception
Strigolactone perception by the D14 hydrolase-receptorRegulatory Stepsl_perception

D14 binds SL in its alpha/beta-hydrolase pocket and switches to a conformation that associates with MAX2 and the SMXL co-repressors. D14 also hydrolyses SL, which deactivates the hormone. Whether hydrolysis is needed to activate the receptor is still debated.

Annotons

D14: strigolactone receptor
d14_sl_receptor
Participant: Gene Product: D14 (AtD14, At3g03990)
Gene Product:
D14 (AtD14, At3g03990)UniProtKB:Q9SQR3

Function

signaling receptor activity (strigolactone receptor)GO:0038023

Processes

cellular response to strigolactoneGO:1902348

Locations

nucleusGO:0005634 cytoplasmGO:0005737

Receptor; the SL-bound conformation recruits MAX2 and the SMXL6/7/8 co-repressors.

D14: strigolactone hydrolase
d14_sl_hydrolase
Participant: Gene Product: D14 (AtD14, At3g03990)
Gene Product:
D14 (AtD14, At3g03990)UniProtKB:Q9SQR3

Function

carboxylic ester hydrolase activity (SL butenolide hydrolysis)GO:0052689
Substrates: strigolactone (GR24 analog in vitro)
Products: ABC-ring product and hydroxy-butenolide D-ring

Processes

cellular response to strigolactoneGO:1902348

Locations

nucleusGO:0005634 cytoplasmGO:0005737

Hydrolyses SL slowly, which deactivates the hormone after signalling and may help activate the receptor.

Part 2: SCF(MAX2)-mediated ubiquitination of SMXL co-repressors
SCF(MAX2) recruitment and SMXL6/7/8 ubiquitinationRegulatory Stepsmxl_ubiquitination

MAX2, the F-box subunit of SCF(MAX2), binds SL-activated D14 and the SMXL6/7/8 proteins. The SMXLs are polyubiquitinated and degraded by the proteasome within minutes of SL treatment. D14 is degraded in an SL- and MAX2-dependent manner as negative feedback.

Annotons

MAX2: SCF F-box substrate adaptor
max2_f_box_adaptor
Participant: Gene Product: MAX2 (ORE9, At2g42620)
Gene Product:
MAX2 (ORE9, At2g42620)UniProtKB:Q9SIM9

Function

ubiquitin-like ligase-substrate adaptor activityGO:1990756

Processes

SCF-dependent proteasomal ubiquitin-dependent protein catabolic processGO:0031146

Locations

nucleusGO:0005634

F-box subunit of SCF(MAX2). It brings D14-bound SMXL6/7/8 to the E3 ligase for polyubiquitination. MAX2 also serves the KAI2-SMAX1 karrikin pathway, which is outside this module.

Part 3: SMXL6/7/8 co-repression of branching-inhibitor genes
SMXL6/7/8 transcriptional co-repressionRegulatory Stepsmxl_corepression

Without SL, the redundant nuclear SMXL6, SMXL7 and SMXL8 proteins recruit TOPLESS-related co-repressors (TPR2) through an EAR motif and repress BRC1 and other SL-responsive genes. SMXL6 can also bind target promoters directly. Degradation of the SMXLs after SL perception lifts this repression.

Annotons

SMXL6: SL-labile co-repressor
smxl6_corepressor
Participant: Gene Product: SMXL6 (At1g07200)
Gene Product:
SMXL6 (At1g07200)UniProtKB:Q9LML2

Function

transcription corepressor activityGO:0003714

Processes

cellular response to strigolactoneGO:1902348 regulation of secondary shoot formationGO:2000032

Locations

nucleusGO:0005634

Redundant co-repressor. It also binds the SMXL6/7/8 promoters itself, acting as an autoregulated transcription factor (PMID:32528176).

SMXL7: SL-labile co-repressor
smxl7_corepressor
Participant: Gene Product: SMXL7 (At2g29970)
Gene Product:
SMXL7 (At2g29970)UniProtKB:O80875

Function

transcription corepressor activityGO:0003714

Processes

cellular response to strigolactoneGO:1902348 regulation of secondary shoot formationGO:2000032

Locations

nucleusGO:0005634

The major branching-relevant paralog. It acts in the nucleus, and deleting its RGKT motif makes it resistant to degradation (PMID:26546447, PMID:27317673).

SMXL8: SL-labile co-repressor
smxl8_corepressor
Participant: Gene Product: SMXL8 (At2g40130)
Gene Product:
SMXL8 (At2g40130)UniProtKB:F4IGZ2

Function

transcription corepressor activityGO:0003714

Processes

cellular response to strigolactoneGO:1902348 regulation of secondary shoot formationGO:2000032

Locations

nucleusGO:0005634

Redundant co-repressor with SMXL6 and SMXL7.

Part 4: BRC1 transcriptional output in axillary buds
BRC1-mediated bud dormancyRegulatory Stepbrc1_output

BRC1 is a TCP transcription factor expressed in axillary buds. It is induced when the SMXLs are degraded, and it promotes bud dormancy, partly by directly activating HB21/HB40/HB53 and so raising abscisic acid in the bud. BRC1 sets how likely a bud is to activate, working in parallel with SL effects on auxin transport.

Annotons

BRC1 (TCP18): bud dormancy transcription factor
brc1_tcp_tf
Participant: Gene Product: BRC1 (TCP18, At3g18550)
Gene Product:
BRC1 (TCP18, At3g18550)UniProtKB:A1YKT1

Function

DNA-binding transcription factor activityGO:0003700

Processes

regulation of secondary shoot formationGO:2000032 bud dormancy processGO:0097207 response to strigolactoneGO:1902347

Locations

nucleusGO:0005634

Output transcription factor. SL induces BRC1 by removing SMXL repression, and BRC1 arrests bud development.