Original Paper
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Acta Biochim Biophys
Sin 2007, 39: 915922
doi:10.1111/j.1745-7270.2007.00358.x
Roles of F-box Proteins in Plant
Hormone Responses
Haichuan YU1, Jiao WU1, Nanfei
XU2,
and Ming PENG1*
1 State Key Laboratory of Tropical Crop
Biotechnology, Institute of Tropical Bioscience and Biotechnology, Chinese Academy
of Tropical Agricultural Sciences, Haikou 571101, China;
2 BASF Plant Science L.L.C., Research
Triangle Park, North Carolina 27709-3528, USA
Received: June 16,
2007
Accepted: July 27,
2007
This work was supported
by a grant from the State Key Basic Research and Development Plan of China (No.
2004CB117307)
*Corresponding
author: Tel, 86-898-66890981; Fax, 86-898-66890978; E-mail,
Abstract The F-box protein is an important component
of the E3 ubiquitin ligase Skp1-Cullin-F-box protein complex. It binds specific
substrates for ubiquitin-mediated proteolysis. The F-box proteins contain a
signature F-box motif at their amino-terminus and some protein-protein
interaction motifs at their carboxy-terminus, such as Trp-Asp repeats or
leucine rich repeats. Many F-box proteins have been identified to be involved
in plant hormone response as receptors or important medial components. These
breakthrough findings shed light on our current understanding of the structure
and function of the various F-box proteins, their related plant hormone
signaling pathways, and their roles in regulating plant development.
Keywords F-box protein; plant hormone response; SCF
complex; ubiquitin proteasome pathway
Plant hormones play pivotal roles in almost every aspect of plant
development from embryogenesis to senescence. Plant hormone signaling pathways
can be effectively controlled by modulation of positive and negative regulators
during plant growth and development [1]. Recent research in plant hormone
signaling pathways has shown that the ubiquitin (Ub) proteasome pathway is a
central regulatory mechanism in the signal transduction pathways of different
plant hormones [2,3]. Remarkably, approximately 1300 genes, or 5% of the Arabidopsis
proteome genes have been thought to encode components in the Ub proteasome
pathway, likely the most elaborate and crucial regulatory system in plants.
Molecular genetic analysis has revealed that the Ub proteolytic system is
involved in all aspects of plant biology, including embryogenesis,
photomorphogenesis, circadian rhythms, senescence, disease resistance, and
notably, hormone signaling [4]. The F-box protein is responsible for recruiting
different substrates for ubiquitination in this pathway, and nearly 700 F-box
proteins have been predicted in Arabidopsis [5].The fact that F-box proteins act as important receptors and
signaling components in plant hormone signaling pathways has emerged from
physiological and molecular studies on a multitude of signaling mutants [6]. In
this review, we focus on recent progresses on the structure and function of
F-box proteins, and particularly, the roles of F-box proteins in plant hormonal
responses.
F-box Proteins in the Ub
Proteasome Pathway
Ub proteasome pathway and
Skp1-Cullin-F-box protein (SCF) complex
The Ub proteasome system plays an important role through mediating degradation
of some pivotal proteins in numerous cellular and organismal processes [7]. In
this pathway, the highly conserved 76-amino acid protein Ub serves as a
reusable tag for selective protein breakdown. The Ub conjugation cascade
involves three enzyme families, an E1 Ub-activating enzyme, an E2
Ub-conjugating enzyme, and an E3 Ub ligase that ultimately ligates multiple Ubs
to its substrates. In the initial reaction, E1 enzyme activates the Ub driven
by ATP hydrolysis to form a high-energy thioester intermediate (E1-S~Ub), in
which the C-terminal group of Ub is linked through a thiolester bond to the E1.
Then, activated Ub is transferred to an E2 enzyme by transesterification. The
transfer of Ub from E2-S~Ub to the target protein is mediated by an E3 enzyme.
An isopeptide bond is formed between the C-terminal group of Ub and the e-amino group of
an internal lysine residue in the substrate. Subsequently, a polyubiquitin
chain is synthesized by successively adding Ub moieties to the previously
conjugated Ub molecule in which various Ub lysines (e.g., 29, 48, and 63 sites
in Ub) as the sites for concatenating additional Ubs [8]. Finally,
multi-ubiquitylated proteins are recognized by the 26S proteasome and
proteolyzed into peptides, and Ub is recycled [9,10]. The current understanding
on the general process of the Ub proteasome pathway is shown in Fig. 1(A).
The Ub proteasome system appears to be hierarchical, only two E1 enzymes, at
least 45 E2 or E2-like proteins, and almost 1200 E3 components are encoded in
the Arabidopsis genome [4]. The Ub protein ligases (or E3 enzymes) are in charge of the
substrate specificity and fall into different categories, such as HECT
(homologous to E6-associated protein carboxyl terminus, which can form a
covalent thiolester), APC (anaphase promoting complex), VBC-Cul2 (the
von-Hippel Lindau-elongins B and C-Cul2 complex), Ring/U-box, and SCF [11,12].
A major type of E3 Ub ligases, the SCF complex is composed of four major
components, Skp1, Cul1/Cdc53, Roc1/Rbx1/Hrt1, and an F-box protein [13,14]. The
scaffold protein Cullin-1 interacts with Skp1 and the F-box protein at the
amino-terminus and associates with the Ring-domain molecule Roc1/Rbx1/Hrt1 at
the carboxyl-terminus, which associates with Ub-conjugated E2 enzyme [Fig.
1(B)]. Different substrates are recognized through the carboxyl-terminus of
F-box protein and Ub is transferred to the substrate from E2 by mediation of E3
enzyme [12,15]. The Arabidopsis genome encodes 11 Cullin homologs, 2
Rbx1 homologs, 21 Arabidopsis Skp1 homologs and at least 700 putative
F-box proteins [16,17].
Characteristics of F-box
proteins
F-box proteins contain a conserved F-box domain (35–60 amino acids)
in the amino-terminus and different substrate-binding domains in the
carboxy-terminus [18]. The F-box domain was first described as a sequence motif
found in human cyclin F by Bai et al. [19]. The F-box domain plays a
role in mediating protein-protein interactions in a variety of processes, such
as polyubiquitination, transcription elongation, centromere binding, and
translation repression. In the Ub proteasome pathway, the F-box motif links the
F-box protein to other components of the SCF complex by binding the core SCF
component Skp1 or Skp1-like proteins. There are very few invariant positions in
the F-box motif and it is difficult to spot the F-box motif by eye. In Fig.
2, we aligned the F-box motif sequences of several F-box proteins involved
in plant hormonal responses. These proteins share some conserved positions, for
example position 9 (in this position, the majority of plant F-box proteins have
isoleucine or valine), 23 (serine or alanine), 25 (valine), 26 (serine or
cysteine), 27 (lysine and arginine), and 29 (tyrosine). The carboxy-terminal
part of F-box proteins has been shown to specifically bind to substrates. These
regions of F-box proteins contain leucine-rich repeats (LRRs) and Trp-Asp
repeats [20,21], but the majority of F-box proteins have unknown association
motifs, and the functions of most of these proteins have not been defined yet.
The diversity of protein-protein interaction domains of F-box proteins
substantially increases the substrate repertoire.
F-box Proteins Involved in
Plant Hormone Responses
F-box protein transport
inhibitor response 1 (TIR1) is an auxin receptor
Auxin tightly regulates many plant growth and developmental
processes throughout the life cycle [22], and its receptor has been found. The
F-box protein TIR1 is an auxin receptor in Arabidopsis thaliana [23,24].
In addition, the auxin signaling F-box proteins 1, 2 and 3 (AFB 1–3) have
displayed in vitro as auxin-dependent Aux/IAA proteins (Aux/IAAs)
binding similar to TIR1 and contributed to auxin responsiveness in vivo
[25]. TIR1 protein consists of an N-terminal F-box motif, a short spacer region
of approximately 40 residues, 16 degenerate LRRs, and a C-terminal tail of
approximately 70 residues [23]. In the auxin signaling
pathway, two closely related protein families, Aux/IAAs and auxin response
factors (ARFs), are key regulators in auxin-modulated gene expression [26]. The
Aux/IAA genes encode short-lived, primary auxin response proteins [27], whereas
ARFs are transcription factors that bind specifically to promoters of primary
auxin response genes [28]. IAA proteins can form heterodimers with ARFs and
negatively regulate the transcriptional activation activity of the ARF proteins
through their potent repressor domains [29]. Auxin promotes Aux/IAAs
ubiquitination by SCFTIR1, triggering their degradation by 26S proteosome,
thereby releasing the ARFs from the repressive effects of the Aux/IAAs [3,7].
ARF-ARF dimers are formed and mediate rapid auxin-induced gene expression [Fig.
3(A)].Two research groups have revealed that an auxin receptor co-purifies
with TIR1 by immunoprecipitation of TIR1, and by using a protein pull-down
assay with tagged Aux/IAAs, that the interaction between SCFTIR1 and Aux/IAAs involves direct auxin binding [23,24]. They proved
that tritiated IAA ([3H]IAA) binds to the SCFTIR1
complex rather than to Aux/IAAs, using the radiolabeled method, and the
apparent dissociation constant Kd should be within the range of 20–80 nM. To
testify the fact that TIR1 binds auxin directly, the TIR1 gene from Arabidopsis
was expressed in Xenopus laevis oocytes and insect cells, then the TIR1
reacted to [3H]IAA and the interaction curve of TIR1 and [3H]IAA accorded with the characteristics of receptor-ligand
association. Afterward, the Myc-tagged TIR1 protein was treated with auxin and
mixed with GST-tagged Aux/IAA protein. It proved that the TIR1-Aux/IAAs
interaction depended on auxin and the ability of interaction was enhanced with
the increased dosage of IAA in a limited concentration range. Recently, the
crystal structure of TIR1 has been presented and shows that the LRR domain of
TIR1 contains an unexpected inositol hexakisphosphate co-factor and recognizes
auxin and the Aux/IAAs polypeptide substrate through a single surface pocket.
By filling in a hydrophobic cavity at the protein interface, auxin enhances the
TIR1-substrate interactions by acting as a “molecular glue” [30].
F-box proteins involved in
gibberellin signaling
Gibberellins are tetracyclic diterpenoid hormones that induce a wide
range of plant growth responses including seed germination, hypocotyl
elongation, stem elongation, leaf expansion, pollen maturation, and induction
of flowering [31]. The F-box proteins SLEEPY1 (SLY1) and SNEEZY (SNE) can
regulate the gibberellin signaling pathway in Arabidopsis [32–34] and
gibberellin-insensitive dwarf 2 (GID2) in Oryza sativa [35]. Mutations
in both the SLY1 gene in Arabidopsis (AtSLY1) and the GID2
gene in O. sativa (OsGID2) result in a recessive,
gibberellin-insensitive dwarfed phenotype and the accumulation of DELLA
proteins. AtSLY1 and OsGID2 amino acid sequences are 36.8% identical and 56%
similar to each other. The high levels of homology and correspondence of
function between dicot and monocot species indicate that the role of the SCFAtSLY1/OsGID2 complex is highly conserved in the plant kingdom [36]. Significant progress has been made in understanding the gibberellin
signaling pathway in rice and many components have been identified, for
example, the receptor GID1 (a soluble receptor for gibberellin) [37], GID2 (an
F-box protein) [36], and the negative regulator SLR1 (a DELLA protein) [38].
DELLA proteins negatively function in the gibberellin signaling cascade as
pivotal regulators [39,40]. GID1 physically interacts with SLR1 in a gibberellin-dependent
manner and induces phosphorylation of SLR1 [41]. The F-box protein GID2
directly interacts with the phosphorylated SLR1, bringing it to the SCFGID2 complex for ubiquitination, and subsequent degradation through the
26S proteasome [35]. But recent results suggested that phosphorylation of SLR1
was not needed when GID1 triggered association of active SLR1 with the SCFGID2 complex in a gibberellin-dependent manner [42]. Disappearance of
the DELLA protein releases its suppression of gibberellin signaling and
promotes transcription of the gibberellin response genes [Fig. 3(B)]. In
Arabidopsis, the DELLA family has five members (GAI, RGA, RGL1, RGL2,
and RGL3) [41]. Similar to GID2 in rice, SLY1 interacts with DELLA proteins for
controlling gibberellin response in Arabidopsis [34]. There is an
interesting parallel between the auxin and gibberellin response because both
appear to induce rapid degradation of the negative regulator by interaction
with the SCF complex.Both OsGID2 and AtSLY1 contain three conserved domains, the F-box,
GGF, and LSL domains. In addition to these domains, GID2 has a unique
N-terminal variable
region (VR1) [32]. All the conserved domains are
essential for the function of GID2 except the VR1. Gomi et al. carried
out a yeast two-hybrid screen and revealed that GID2 associated with rice
OsSkp15 and OsCul1 to assemble the SCF complex. RNA gel blot analysis and
reverse transcription-polymerase chain reaction assay of the GID2 gene
in different rice organs revealed that GID2 was expressed in all organs
examined, with higher levels in elongation stem, shoot apex, and unopened
flower, and lower levels in the leaf blade, leaf sheath, root, and rachis. This
expression pattern coincided with the locations in which gibberellin is
actively produced. An in vitro binding assay showed that GID2
specifically interacted with the phosphorylated SLR1 protein but not with the
unphosphorylated one [41].
Roles of F-box proteins in
ethylene signaling
The phytohormone ethylene is a gaseous hydrocarbon molecule that can
trigger a wide range of physiological and morphological responses, including
inhibition of cell expansion, promotion of leaf and flower senescence,
induction of fruit ripening and abscission, and adaptation to external stress
factors [43]. In the signaling pathway of ethylene, two Arabidopsis
F-box proteins, ethylene insensitive 3 (EIN3)-binding F-box protein 1 (EBF1)
and EBF2, target the transcriptional activator EIN3 for degradation [44–46]. Mutation in
either gene shows enhanced ethylene response by stabilizing EIN3, whereas efb1
and efb2 double mutants show constitutive ethylene phenotypes. Plants
overexpressing either F-box gene display ethylene insensitivity and destabilization
of EIN3 protein. These results indicate that the Ub proteasome pathway
negatively regulates ethylene responses by targeting EIN3 for degradation [44].Genetic studies have identified several components of the ethylene signaling
pathway, including the receptor family ETR1 (ETHYLENE RESPONSE), ETR2, ERS1
(ETHYLENE RESPONSE SENSOR), ERS2, and EIN4, and other components CTR1
(CONSTITUTIVE TRIPLE RESPONSE 1), EIN2, and EIN3 [47]. Arabidopsis EIN3
protein is a key transcription factor that modulates ethylene-regulated gene
expression and morphological responses [48], which is expressed constitutively
and acts on its target promoters only upon perception of ethylene. In the
absence of ethylene, EIN3 is ubiquitinated by the SCFEBF1/2 complex, and
degraded by the 26S proteasome [Fig. 3(C)]. In the presence of ethylene,
EIN2 prevents EIN3 from being ubiquitinated by SCFEBF1/2, leading to EIN3
accumulation and the activation of ethylene-response gene expression [44,45].
It is worth noting that EIN3 is degraded in ethylene signaling as a
transcription activator, differing from Aux/IAA and DELLA proteins in responses
to auxin and gibberellin as repressors.
Coronatine insensitive 1
(COI1): pivotal regulator in jasmonate signaling
Jasmonates (JAs), including jasmonic acid and its cyclopentanone
derivatives, are essential plant hormones that are involved in the regulation
of many physiological and developmental processes, including root growth, fruit
ripening, senescence, pollen development, and adaptation to environmental
stresses [49,50]. The F-box protein COI1 is a pivotal factor in the JA signal
response [Fig. 3(D)] and is required for all JA-dependent responses in Arabidopsis
[19,51]. The coi1 mutant is male sterile, less resistant to insect
attack, and less responsive to wounding damage [52]. The COI1 protein has an
F-box motif and 16 LRRs that selectively recruit regulators of JA response for
polyubiquination and proteolysis [19]. COI1 has been shown to form a functional
E3-type Ub ligase complex. Moreover, plants that are deficient in other
components of SCF complexes also show impaired JA responses [16,53]. Thus, SCFCOI1 is a central component of all JA-dependent responses, the activity
of which is presumably modulated by several Ub proteasome pathway genes (e.g., AXR1,
SGT1b, and CSN) that are also involved in the modulation of other
SCF complexes [54]. It has been suggested that SCFCOI1 is
associated with the COP9 signalosome in vivo to mediate JA responses
together [55].Putative targets of COI1 have been identified and their functional
analysis will be instrumental to furthering our understanding of the molecular
mechanisms that regulate JA responses [56,57]. Using a two-hybrid strategy,
researchers have identified RPD3b, a histone deacetylase, as a COI1 target
[56]. Because histone deacetylation is believed to decrease the accessibility
of chromatin to the transcription machinery [58], COI1-dependent proteasome
degradation of RPD3b would be a probable mechanism for derepression of
JA-dependent transcription. Another putative target of COI1 is COS1. The mutant
cos1 has been identified as a suppressor of coi1 mutant,
restoring some JA-regulated responses, such as root growth, senescence, and
defense [57]. COS1 encodes lumazine synthase, and lumazine is a key component
of the riboflavin pathway, which suggests the involvement of this pathway in
the modulation of JA signaling. By analogy, COI1, the closest F-box protein to
TIR1 in the Arabidopsis genome, could be the JA receptor. Certainly,
further research on JA signaling responses will clarify this point and extend
our understanding of the JA signaling response.
F-box proteins in other plant
responses
So far we have discussed F-box proteins involved in plant hormone
response and their related signal transduction pathways individually. Many
F-box proteins have also been identified in plants that are involved in other
cellular and organismal processes. These F-box proteins include: the proteins
regulating lateral root formation, such as MAX2 [59], ARABIDILLO-1/2 [60], and
CEGENDUO [61]; in light signaling, such as EMPFINDLICHER IM DUNKELROTEN LICHT
(EID1) [62], ATTENUATED FAR-RED RESPONSE (AFR) [63]; in the circadian system,
such as ZEITLUPE (ZTL) [64], LOV KELCH PROTEIN2 (LKP2), FLAVIN-BINDING,
KELCH-REPEAT, F-box1 (FKF1) [65]; influencing self-incompatibility, such as
AhSLF-S2 [66]; and controlling floral development, such as UNUSUAL FLORAL
ORGANS (UFO) and FIMBRIATA (FIM) [67]. F-box proteins might also participate in
stress response and regulation of leaf senescence ORE9 [68] in plants. Given
the large number of F-box proteins in the plant kingdom, we can envision that
more F-box proteins will be found involved in other plant processes.
Conclusions and Prospects
Recent research in plant hormone responses has enhanced our two
major understandings. First, plant hormone signaling pathways are a series of
complex networks and these networks often cross-talk with each other. Second,
Ub-mediated protein degradation is a central regulatory mechanism involving
many different hormonal pathways. F-box proteins play crucial roles in the
ubiquitination system by specifically recruiting target regulatory proteins to
the Ub complex. Although considerable progresses have been made in
understanding the roles of F-box proteins in plant hormone responses, great
challenges remain in deciphering the mechanisms of each F-box protein that
regulates plant hormone responses. We are of the opinion that the following
questions regarding F-box proteins and plant hormone signaling transduction
should be taken into account in the future and will be resolved gradually.Genomic analysis has indicated a large number of uncharacterized
F-box proteins in plants, and there are many questions about these proteins.
For example, how can we obtain and characterize the corresponding mutants of
unknown F-box proteins? What are the target substrates for the putative F-box
proteins in plants? What are the biological functions of these predicted plant
F-box proteins? These questions remain to be intriguing issues within the field
of protein degradation. On the encouraging side, methods of genetic mutant and
reversed genetics are available for studying these genes. Different screens can
be used for physiological and molecular characterization of mutants. The
related genes can be cloned using Map-based cloning or insertion of T-DNA. The
functions of the genes can be analyzed by combining techniques of functional
genomics and proteomics. Microarray technique can help us comprehend the change
in genes after transcription and identify the unknown genes. New
high-throughput gene expression analysis techniques and system-wide approaches
will also be important in investigating these questions.
In the SCF complex, the F-box motif binds to Skp1 or Skp1-like
proteins, however, so far there is no evidence of F-box proteins binding to
other types of proteins. Whether there are other F-box-binding proteins remains
as an interesting question. The F-box protein family is the largest protein superfamily. Much
research has focused on the model plants A. thaliana or O. sativa
that help us best understand the processes involved in hormonal perception.
F-box protein research on other plant species is relatively weak. Our
laboratory is currently studying F-box proteins in Gossypium hirsutum
and we believe that many important F-box proteins involved in hormone signaling
responses in cotton will be identified in the near future.Overall, we are still far from having an integrated picture of F-box
protein functional repertory. Searching the new F-box proteins in the plant
kingdom and determining the functions of these uncharacterized F-box proteins
will prove to be an important area of future research.
Acknowledgement
The authors thank Dr. Thomas W. OKITA for
reviewing the manuscript and providing valuable comments and suggestions.
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