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"631/449/1741/2672"
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D14–SCFD3-dependent degradation of D53 regulates strigolactone signalling
by
Guo, Xiuping
,
Asami, Tadao
,
Zheng, Ning
in
631/449/1741/2672
,
Agronomy. Soil science and plant productions
,
Biological and medical sciences
2013
Strigolactones (SLs), a newly discovered class of carotenoid-derived phytohormones, are essential for developmental processes that shape plant architecture and interactions with parasitic weeds and symbiotic arbuscular mycorrhizal fungi. Despite the rapid progress in elucidating the SL biosynthetic pathway, the perception and signalling mechanisms of SL remain poorly understood. Here we show that DWARF 53 (D53) acts as a repressor of SL signalling and that SLs induce its degradation. We find that the rice (
Oryza sativa
)
d53
mutant, which produces an exaggerated number of tillers compared to wild-type plants, is caused by a gain-of-function mutation and is insensitive to exogenous SL treatment. The
D53
gene product shares predicted features with the class I Clp ATPase proteins and can form a complex with the α/β hydrolase protein DWARF 14 (D14) and the F-box protein DWARF 3 (D3), two previously identified signalling components potentially responsible for SL perception. We demonstrate that, in a D14- and D3-dependent manner, SLs induce D53 degradation by the proteasome and abrogate its activity in promoting axillary bud outgrowth. Our combined genetic and biochemical data reveal that D53 acts as a repressor of the SL signalling pathway, whose hormone-induced degradation represents a key molecular link between SL perception and responses.
Strigolactones (SLs), key regulators of plant growth, are believed to mediate their responses through a proposed receptor (D14) that interacts with an F-box protein (D3) to form a D14–SCF
D3
protein complex; here the perception of SLs by the D14–SCF
D3
complex and the control of gene expression are linked by the finding that DWARF 53, a repressor protein of SL function, interacts with the D14–SCF
D3
complex and is ubiquitinated and degraded in a SL-dependent manner.
Strigolactone receptor identified
The strigolactones are key regulators of plant growth, controlling the formation of secondary shoots and regulating root branching. Strigolactone responses are mediated through a proposed receptor (D14) that interacts with an F-box protein (D3). Now, in two related publications, Liang Jiang
et al
. and Feng Zhou
et al
. demonstrate a functional link between the perception of strigolactones by D14/D3 and the control of gene expression in rice. They show that the protein DWARF53 (D53), of previously unknown function, acts as a repressor of strigolactone signalling and that strigolactones induce its degradation. D53 interacts with the D14–D3 complex and is ubiquitinated and degraded by the proteasome in a strigolactone-dependent manner.
Journal Article
An ancestral function of strigolactones as symbiotic rhizosphere signals
2022
In flowering plants, strigolactones (SLs) have dual functions as hormones that regulate growth and development, and as rhizosphere signaling molecules that induce symbiosis with arbuscular mycorrhizal (AM) fungi. Here, we report the identification of bryosymbiol (BSB), an SL from the bryophyte
Marchantia paleacea
. BSB is also found in vascular plants, indicating its origin in the common ancestor of land plants. BSB synthesis is enhanced at AM symbiosis permissive conditions and BSB deficient mutants are impaired in AM symbiosis. In contrast, the absence of BSB synthesis has little effect on the growth and gene expression. We show that the introduction of the SL receptor of Arabidopsis renders
M. paleacea
cells BSB-responsive. These results suggest that BSB is not perceived by
M. paleacea
cells due to the lack of cognate SL receptors. We propose that SLs originated as AM symbiosis-inducing rhizosphere signaling molecules and were later recruited as plant hormone.
Strigolactones (SLs) regulate angiosperm development and promote symbiosis with arbuscular mycorrhizae. Here the authors show that bryosymbiol, an SL present in bryophytes and angiosperms, promotes AM symbiosis in
Marchantia paleacea
suggesting an ancestral function of SLs as rhizosphere signals.
Journal Article
Transcriptional regulation of strigolactone signalling in Arabidopsis
2020
Plant hormones known as strigolactones control plant development and interactions between host plants and symbiotic fungi or parasitic weeds
1
–
4
. In
Arabidopsis thaliana
and rice, the proteins DWARF14 (D14), MORE AXILLARY GROWTH 2 (MAX2), SUPPRESSOR OF MAX2-LIKE 6, 7 and 8 (SMXL6, SMXL7 and SMXL8) and their orthologues form a complex upon strigolactone perception and play a central part in strigolactone signalling
5
–
10
. However, whether and how strigolactones activate downstream transcription remains largely unknown. Here we use a synthetic strigolactone to identify 401 strigolactone-responsive genes in
Arabidopsis
, and show that 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. We find that SMXL6 targets 729 genes in the
Arabidopsis
genome and represses the transcription of
SMXL6
,
SMXL7
and
SMXL8
by binding directly to their promoters, showing that SMXL6 serves as an autoregulated transcription factor to maintain the homeostasis of strigolactone signalling. These findings reveal an unanticipated mechanism through which a transcriptional repressor of hormone signalling can directly recognize DNA and regulate transcription in higher plants.
Many of the molecular targets of strigolactones—plant hormones involved in development and in interactions with symbiotic and parasitic organisms—are uncovered, revealing how strigolactones function and an intriguing role for self-regulation of a downstream transcription factor.
Journal Article
Strigolactone perception and deactivation by a hydrolase receptor DWARF14
2019
The perception mechanism for the strigolactone (SL) class of plant hormones has been a subject of debate because their receptor, DWARF14 (D14), is an α/β-hydrolase that can cleave SLs. Here we show via time-course analyses of SL binding and hydrolysis by
Arabidopsis thaliana
D14, that the level of uncleaved SL strongly correlates with the induction of the active signaling state. In addition, we show that an AtD14
D218A
catalytic mutant that lacks enzymatic activity is still able to complement the
atd14
mutant phenotype in an SL-dependent manner. We conclude that the intact SL molecules trigger the D14 active signaling state, and we also describe that D14 deactivates bioactive SLs by the hydrolytic degradation after signal transmission. Together, these results reveal that D14 is a dual-functional receptor, responsible for both the perception and deactivation of bioactive SLs.
Cleavage of strigolactone by the D14 receptor was assumed to produce an active intermediate that promotes signaling. Here the authors show that D14 activity is not dependent on cleavage activity and propose a new model whereby ligand hydrolysis serves to deactivate strigolactone signaling.
Journal Article
The apocarotenoid metabolite zaxinone regulates growth and strigolactone biosynthesis in rice
2019
Carotenoid cleavage dioxygenases (CCDs) form hormones and signaling molecules. Here we show that a member of an overlooked plant CCD subfamily from rice, that we name Zaxinone Synthase (ZAS), can produce zaxinone, a novel apocarotenoid metabolite in vitro. Loss-of-function mutants (
zas
) contain less zaxinone, exhibit retarded growth and showed elevated levels of strigolactones (SLs), a hormone that determines plant architecture, mediates mycorrhization and facilitates infestation by root parasitic weeds, such as
Striga
spp. Application of zaxinone can rescue
zas
phenotypes, decrease SL content and release and promote root growth in wild-type seedlings. In conclusion, we show that zaxinone is a key regulator of rice development and biotic interactions and has potential for increasing crop growth and combating
Striga
, a severe threat to global food security.
Strigolactone and abscisic acid are carotenoid-derived plant hormones. Here the authors describe the identification of zaxinone, a further apocarotenoid metabolite, which down-regulates strigolactone content and is required for normal growth and development in rice.
Journal Article
Arabidopsis FHY3 and FAR1 integrate light and strigolactone signaling to regulate branching
2020
Branching/tillering is an important parameter of plant architecture and is tightly regulated by both internal factors (such as plant hormones) and external factors (such as light conditions). How the various signaling pathways converge to coordinately regulate branching is not well understood. Here, we report that in
Arabidopsis
, FHY3 and FAR1, two homologous transcription factors essential for phytochrome A-mediated light signaling, and SMXL6/SMXL7/SMXL8, three key repressors of the strigolactone (SL) signaling pathway, directly interact with SPL9 and SPL15 and suppress their transcriptional activation of
BRC1
, a key repressor of branching, thus promoting branching. In addition, FHY3 and FAR1 also directly up-regulate the expression of
SMXL6
and
SMXL7
to promote branching. Simulated shade treatment reduces the accumulation of FHY3 protein, leading to increased expression of
BRC1
and reduced branching. Our results establish an integrated model of light and SL coordinately regulating
BRC1
expression and branching through converging at the
BRC1
promoter.
In plants, branching is regulated by both hormones and external cues such as light. Here the authors show that in
Arabidopsis
, the phytochrome A-signaling components FHY3 and FAR1, and SMXL proteins that repress strigolactone signaling, both interact with SPL proteins to control expression of the branching regulator
BRC1
.
Journal Article
DWARF 53 acts as a repressor of strigolactone signalling in rice
2013
Strigolactones (SLs) are a group of newly identified plant hormones that control plant shoot branching. SL signalling requires the hormone-dependent interaction of DWARF 14 (D14), a probable candidate SL receptor, with DWARF 3 (D3), an F-box component of the Skp–Cullin–F-box (SCF) E3 ubiquitin ligase complex. Here we report the characterization of a dominant SL-insensitive rice (
Oryza sativa
) mutant
dwarf 53
(
d53
) and the cloning of
D53
, which encodes a substrate of the SCF
D3
ubiquitination complex and functions as a repressor of SL signalling. Treatments with GR24, a synthetic SL analogue, cause D53 degradation via the proteasome in a manner that requires D14 and the SCF
D3
ubiquitin ligase, whereas the dominant form of D53 is resistant to SL-mediated degradation. Moreover, D53 can interact with transcriptional co-repressors known as TOPLESS-RELATED PROTEINS. Our results suggest a model of SL signalling that involves SL-dependent degradation of the D53 repressor mediated by the D14–D3 complex.
Strigolactones (SLs), key regulators of plant growth, are believed to mediate their responses through a proposed receptor (D14) that interacts with an F-box protein (D3) to form a D14–SCF
D3
protein complex; here the perception of SLs by the D14–SCF
D3
complex and the control of gene expression are linked by the finding that DWARF 53, a repressor protein of SL signalling, interacts with the D14–SCF
D3
complex and is ubiquitinated and degraded in a SL-dependent manner.
Strigolactone receptor identified
The strigolactones are key regulators of plant growth, controlling the formation of secondary shoots and regulating root branching. Strigolactone responses are mediated through a proposed receptor (D14) that interacts with an F-box protein (D3). Now, in two related publications, Liang Jiang
et al
. and Feng Zhou
et al
. demonstrate a functional link between the perception of strigolactones by D14/D3 and the control of gene expression in rice. They show that the protein DWARF53 (D53), of previously unknown function, acts as a repressor of strigolactone signalling and that strigolactones induce its degradation. D53 interacts with the D14–D3 complex and is ubiquitinated and degraded by the proteasome in a strigolactone-dependent manner.
Journal Article
Effects of strigolactone on photosynthetic and physiological characteristics in salt-stressed rice seedlings
2020
Saline stress has been identified as the primary factor inhibiting rice seedling growth, which represents a complex abiotic stress process. Most plant hormones have been shown to alleviate the plant damage caused by salt stress. The effects of synthetic strigolactone (GR24) on Jinongda 667 rice seedlings treated with 200 mM NaCl were studied. Photosynthesis and its related physiological characteristics were analyzed in salt-stressed rice seedlings treated with GR24. NaCL stress inhibited the growth of the rice, including plant height and root length, by approximately 14% and 40%, respectively. Compared to the control check group (CK), the adverse effects of salt stress on the growth status, leaf photosynthesis, and physiological/biochemical indices in the rice seedlings were alleviated in the GR24 treatment group. With increases in the GR24 concentration, the plant height and root length of the seedlings increased. The plant height in the groups treated with 1/2 Hoagland’s complete nutrient solution + 200 mM NaCl +1 μM GR24 (T4) and 1/2 Hoagland’s complete nutrient solution + 200 mM NaCl +5 μM GR24 (T5) were significantly different than the 1/2 Hoagland’s complete nutrient solution + 200 mM NaCl group (T1) (P < 0.05), and there were significant differences between the T5 and T1 groups in root length (P < 0.05).The chlorophyll content in the rice seedling leaves was significantly different between the T1 group and all other groups (P < 0.05). The net photosynthetic rate of the T1 group was not significantly different from the T2 group (P > 0.05). The transpiration rate, stomatal conductance, and intercellular CO
2
concentrations showed the same trends as the net photosynthetic rate. The MAD, POD, and SOD activities were significantly increased by 68%, 60%, 14%, respectively, compared to the CK group (P < 0.01). When the GR24 concentration was 1 μM, the rice seedlings were resistant to the adverse effects of high salt stress. Therefore, the addition of proper concentrations of GR24 could improve the rice yield in saline-alkali land.
Journal Article
Strigolactones are chemoattractants for host tropism in Orobanchaceae parasitic plants
2022
Parasitic plants are worldwide threats that damage major agricultural crops. To initiate infection, parasitic plants have developed the ability to locate hosts and grow towards them. This ability, called host tropism, is critical for parasite survival, but its underlying mechanism remains mostly unresolved. To characterise host tropism, we used the model facultative root parasite
Phtheirospermum japonicum
, a member of the Orobanchaceae. Here, we show that strigolactones (SLs) function as host-derived chemoattractants. Chemotropism to SLs is also found in
Striga hermonthica
, a parasitic member of the Orobanchaceae, but not in non-parasites. Intriguingly, chemotropism to SLs in
P. japonicum
is attenuated in ammonium ion-rich conditions, where SLs are perceived, but the resulting asymmetrical accumulation of the auxin transporter PIN2 is diminished.
P. japonicum
encodes putative receptors that sense exogenous SLs, whereas expression of a dominant-negative form reduces its chemotropic ability. We propose a function for SLs as navigators for parasite roots.
Parasitic plants are able to grow towards potential hosts. Here the authors show that strigolactones produced by the host plants can act as chemoattractants for the root parasites
Phtheirospermum japonicum
and
Striga hermonthica
.
Journal Article
Nutrient regulation of lipochitooligosaccharide recognition in plants via NSP1 and NSP2
2022
Many plants associate with arbuscular mycorrhizal fungi for nutrient acquisition, while legumes also associate with nitrogen-fixing rhizobial bacteria. Both associations rely on symbiosis signaling and here we show that cereals can perceive lipochitooligosaccharides (LCOs) for activation of symbiosis signaling, surprisingly including Nod factors produced by nitrogen-fixing bacteria. However, legumes show stringent perception of specifically decorated LCOs, that is absent in cereals. LCO perception in plants is activated by nutrient starvation, through transcriptional regulation of
Nodulation Signaling Pathway
(
NSP
)
1
and
NSP2
. These transcription factors induce expression of an LCO receptor and act through the control of strigolactone biosynthesis and the karrikin-like receptor
DWARF14-LIKE
. We conclude that LCO production and perception is coordinately regulated by nutrient starvation to promote engagement with mycorrhizal fungi. Our work has implications for the use of both mycorrhizal and rhizobial associations for sustainable productivity in cereals.
Lipochitooligosaccharide (LCO) perception by legumes is required to establish symbiotic relationships with nitrogen fixing bacteria. Here the authors show that nutrient starvation can activate LCO perception in cereals to promote symbiotic association with arbuscular mycorrhizal fungi.
Journal Article