F-Box Protein: History
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Subjects: Agriculture, Dairy & Animal Science
Contributor:
Xu Keheng

F-box genes can regulate plant growth and development, including hormone, root development, self-incompatibility, senescence, and response to abiotic and biotic stress.

  • F-Box Protein
  • Plant
  • Development
  • Biotic Stress

1. The Structure and Action Processes of the F-Box Protein

F-box proteins are a class of proteins that widely exist in eukaryotes with F-box motifs. The F-box motif contains 40–50 amino acids, mainly located at the N-terminal, which can interact with the Skp1 protein [1]. The C-terminal of the F-box protein usually contains a (or several) secondary structure that mediates substrate-specific recognition, which can recruit substrate protein for ubiquitination. In addition, the C-terminal domain is the basis of F-box protein classification [2]. For the convenience of research, researchers divided the enormous F-box family into different subfamilies according to its C-terminal domain. Therefore, the F-box protein family in animals was divided into three subfamilies, namely, the FBXL, which represents leucine-rich repeats at the C-terminal; FBXW, which represents WD40 repeats at the C-terminal; and FBXO, which is a protein with other secondary structures or unknown domains at its C-terminal [3][4]. However, because their families are too large and the number of different species is different in plants, the number of subfamilies is also different. In general, studies generally include nine subfamilies, namely, the FBU, whose C-terminal contains the unknown structure; FBL, whose C-terminal contains leucine-rich repeats; FBK, whose C-terminal contains the Kelch domain; FBA, whose C-terminal contains an F-box associated domain; FBD, whose C-terminal also contains an F-box domain; FBT, whose C-terminal contains the tubby domain; FBP, whose C-terminal contains the phloem protein-2 domain; FBW, whose C-terminal contains the WD40 domain; and FBO, whose C-terminal contains other known domains or more than one known domain. Most of the previous studies upon F-box proteins belong to the FBL, FBK, and FBT subfamilies. These subfamily members participate in various biological processes: the FBL subfamily members mainly participate in phytohormone signaling, for instance, TRANSPORT INHIBITOR RESPONSE1 (TIR1) involved in auxin signaling [5] and CORONA-TINE INSENSITIVE1 (COI1) involved in jasmonic acid signaling [6]; the FBT subfamily members are involved in ethylene-dependent fruit ripening, such as TPL1/TPL [7], and the FBK subfamily members are involved in light signal regulation and phenylpropanoid metabolism, such as AFR/ZTL/FKF1/LKP [8][9] and KFB01/KFB20/KFB50/SAGL1 [10][11].
F-box proteins form SCF complexes through their N-terminal F-box domain and Skp1, Cullin1, and Rbx1 to degrade the C-terminal binding target proteins by the UPP. The UPP can be divided into four steps [12][13][14]: (a) The ubiquitin-activating enzyme, E1, activates ubiquitin to form a thiol-ester linkage between its internal cysteine residue and C-terminal Gly residues of Ub in the presence of ATP. (b) The E1 transfer-activated ubiquitin binding to cysteine of the ubiquitin-conjugating enzyme, E2, to form new thioester. (c) Ubiquitin ligase, E3, catalyzes the formation of an isopeptide between the carboxyl at the C-terminal of Ub and the ε-amine of the substrate (in rare cases, the peptide is formed). (d) Finally, the 26S proteasome degrades the substrate into a polypeptide, after which monomeric ubiquitin is released. In the UPP, the ubiquitin chains formed by ubiqutination of substrates mainly consist of K48-linked polyUb [15]. Previous studies have found that branched K11/K48-linked polyUb not only participates in the UPP but also enhances affinity with proteasome subunit Rpn1 [16]. However, other ubiquitin chains (K6, K29, K63, etc.) formed by the specific Lys (K) sites could not participate in the UPP [17][18].
As mentioned above, the F-box gene family is the largest, with hundreds of members in plants, which indicates that F-box proteins could participate in the regulation of various physiological processes by binding to different target proteins. Studies have shown that F-box proteins are also involved in plant biotic and abiotic stress responses, in addition to regulating plant growth and development.

2. The Function of F-Box Proteins in Plant

2.1. Root Development

The root is one of the most important organs of plants. It can not only provide support for plants but also absorb nutrients and water. In addition, roots can perceive the change in external environment. It is difficult to observe roots that are underground, and many factors affect the root system architecture. Thus, there are some challenges in studying the root system. However, a large number of studies have shown that the F-box gene family is involved in root development. Carbonnel et al. found that the F-box protein MAX2 can inhibit the growth of primary roots and promote the growth of root hairs. This growth was possible by increasing the content of ethylene through the Karrikins signaling pathway [19]. Therefore, in the presence of Karrikins, MAX2 will degrade SMAX1 through the UPS and relieve the transcriptional inhibition of the ACS7 gene, which is the rate-limiting enzyme for ethylene biosynthesis in Lotus japonicus. Moreover, Swarbreck et al. found that MAX2 can limit root skewing in Arabidopsis [20][21]. F-box genes can also regulate root development through auxin signals. Similarly, auxin promotes the expression of the F-box geneCEGENDUO (CEG, AtSFL16) in vascular tissue of primary roots, which inhibits lateral root formation [22]. In addition, Arabidopsis T-DNA insertion mutant and RNAi lines produce more lateral roots than WT, and the phenotype of the ceg mutant can be restored by complement. AUXIN UP-REGULATED F-BOX PROTEIN1 (AUF1) is an auxin-responsive F-box protein. Auxin induces AUF1, which can regulate root development by promoting auxin transport [23][24]. Under normal conditions, the roots of auf1 were found to not be different from WT, and this phenotype was not different when indole acetic acid (IAA) was used. However, the root length of auf1 was shorter than that of WT when NPA and TIBA were used. This result indicated that AUF1 can promote auxin transport. Furthermore, auf1 was sensitive to cytokinin. After adding CK, the root of auf1 was also shorter than that of WT. Therefore, Zheng et al. believed that AUF1 had an additional crosstalk between cytokinins and auxins [23]. Furthermore, some F-box proteins are not directly involved in plant hormone signaling control root development, such as ARABIDILLO-1/-2 [25]. Compared with WT, the overexpression of ARABIILLO-1/-2 lines produced more lateral roots, while the arabidillo-1/-2 mutant produced fewer lateral roots.

2.2. Leaf and Stem Development

The leaf is the main place for photosynthesis, respiration, and evapotranspiration, which is crucial to the growth of plants. Leaf morphological structures are closely associated with crop yield and play an important role in response to stress. It was found that the F-box protein FBX92 can affect the leaf development of Arabidopsis thaliana by stimulating cell proliferation [26]. Compared with WT, transgenic plants overexpressing AtFBX92 produce smaller leaves, and synthetic RNA silencing AtFBX92 genes produce larger leaves. Interestingly, the Arabidopsis with heterologous gene of ZmFBX92, AtFBX92 homologous gene, produces bigger leaves than WT. This is because the C-terminal of AtFBX92 protein has one F-box-associated domain more than that of the ZmFBX92 protein. Furthermore, the F-box gene LEAF INCLINATION 4 (LC4) in rice can control the leaf angle of rice [27]. Compared with WT, overexpression LC4 plants increased leaf angle by increasing the expansion and elongation of adaxial parenchyma cells, while the opposite was observed in LC4-Cas9 plants. In addition, LC4 can be induced by IAA but did not interact with the components of the IAA signal pathway. Similarly, the HAWAIIAN SKIRT (HWS) gene plays a certain function in leaf development [28]. In Arabidopsis, HWS deficiency leads to larger leaves, but in tomato, the hws mutant leaves become smaller, and lobule fusion occurs [29].
Leaf development ends in leaf senescence. A study on the F-box gene in leaf senescence has also been reported. In screening the senescence mutants of Arabidopsis thaliana, it was found that the mineralara9 mutant had a delayed senescence phenotype [30]. It was then found in a later study that ORESARA9 (ORE9) was an F-box protein that can regulate leaf senescence by the UPP [31]. ORE9 is regulated by mitogen-activated protein kinase 6 (MPK6). MPK6 can promote the cleavage and nuclear translocation of C-terminal end of ORE3/EIN2 to stabilize EIN3 in the nucleus. This regulation leads to the binding of EIN3 to the TTCAAA element in the ORE9 promoter, thus promoting the expression of ORE9 [32]. Similarly, OsFBK12 can degrade OsSAMS1 by the SCF complex formed with Skp1, affecting ethylene synthesis and histone methylation [33]. Compared with the wild type, the ethylene content of OsFBK12-RNAi and OsSAMS1 overexpression lines increased, resulting in aging. In contrast, overexpression of OsFBK12 and OsSAMS1-RNAi decreased ethylene content, thus delaying senescence.
The stem is one of the six major organs of plants, which can transport water and inorganic salts absorbed by roots, as well as the products of leaf photosynthesis to other organs of plants. Research findings showed that some F-box genes can regulate stem development, in addition to regulating leaf development. Liu et al. found that after silencing SlGID2, an F-box gene, in tomato, the leaf color turned darker, the size became smaller, and the stem cells became smaller and more compact, resulting in dwarfing [34]. However, this dwarfing phenomenon was not caused by the lack of GA in vivo and could not be rescued by exogenous GA. In contrast, the GA content in SlGID2i was higher than that in WT. Similarly, Wang et al. found that the Arabidopsis F-box protein SAP can ubiquitinate PPD proteins to promote the proliferation of meristem cells, which regulates organ size [35]. The sap T-DNA insertion mutant (early termination) therefore generates smaller leaves and shorter plant height than WT. Moreover, SMALL LEAF AND BUSHY1 (SBL1), SAP homologous genes, can regulate leaf size and the number of lateral branches by altering cell proliferation [36]. Leaves of sbl1 are thus smaller than those of WT, but an increase in the number of lateral branches is observed.

2.3. Flower and Fruit Development

UNUSUAL FLORAL ORGANS (UFO) was the first identified F-box gene in plants, one that can regulate floral organ development [37]. Flower development is mainly controlled by ABC genes, wherein A genes control the growth of sepals and petals, B genes control the growth of petals and stamens, and C genes control the growth of stamens and carpels. The AtUFO can mediate the protein hydrolysis of inhibitors of APETALA3 (AP3) and PISTILLATA (PI), class B functional genes, by interacting with AtASK to promote the expression of AP3 and PI [38]. In Arabidopsis, the Atufo mutation causes a series of floral abnormalities, such as in the number of sepals, flower size, and so on [37]. Similarly, the ufo mutation in Cymose Aquilegia coerulea results in small flowers, increased sepals, and decreased petals and stamens [39]. In rice, the functions of class B genesOsMADS4 and OsMADS16 are largely conservative, being regulated by the F-box geneDDF1 [40]. Previous studies have also shown that the palea and lemma of ddf1-1 mutant spikelets were deformed, resulting in untight closure aberrant pistil-like organs. The OsMADS4 and OsMADS16 genes were also significantly downregulated, whereas the DL gene was significantly upregulated in ddf1-1. This result indicates that DDF1 can promote OsMADS4 and OsMADS16 gene expression and inhibit DL gene expression. Similarly, the photo-responsive F-box proteinFOF2 adjusts flowering time by promoting the expression of the FLC gene [41]. Overexpression of FOF2 in Arabidopsis can delay flowering, while the dominant-negative mutant results in early flowering. In addition, FOF2 transgenic plants retained a photoperiod response. Compared with long-day conditions, overexpression of FOF2 bloomed late under short-day conditions. HWS can regulate flower and fruit development in addition to the above-mentioned function that controls leaf development [28]. The sepals of Arabidopsis thaliana mutant hws showed fusion, while anther filaments were fused to the side of the silique. Moreover, the siliques of hws were bigger than WT due to aberrant septum development. Later, it was found that HWS controlled flower size and floral organ number by regulating the expression of CUC1 and CUC2 genes [42]. Furthermore, the tomato hws mutants not only cause abnormal flower development but also promote parthenocarpy [29].

3. The F-Box Proteins and Biotic Stress

Biotic stress has adverse effects on plant growth and development. In the process of plant growth, pathogens and pests attack plants. As a result, plants have developed many defense mechanisms to protect themselves during the process of evolution. Stomatal closure is an important part of plant resistance to bacterial innate immune response. When pathogens come into contact with leaves, plants resist the pathogens by closing their stomata [43]. In addition to affecting plant growth and development, MAX2 is a protein that is essential for resisting pathogen invasion in plants. Previous studies have shown that the stomatal closure function of Arabidopsis mutant max2 was impaired, and stomatal conductance was enhanced, which allows more pathogens to enter the plant plastids, leading to enhanced susceptibility [44]. Furthermore, the F-box-Nictaba protein is a plant lectin that plays an important role in plant defense [45][46]. Pseudomonas syringae can also induce the expression of F-box-Nictaba gene in Arabidopsis thaliana. Compared with WT and F-box-Nictaba knock-out plants, overexpression of F-box-Nictaba plants showed relatively slight disease symptoms after infection with Pst DC3000. OsDRF1 also increases plant tolerance to Pseudomonas syringae. It can also increase tolerance to viruses [47]. The heterologous expression of OsDRF1 in tobacco increased the expression of defense genes; for instance, PR-1a and Sar8.2b in vivo increases the resistance of plants to cauliflower virus after tomato cauliflower virus infection. Similarly, Verticillium dahlia can induce the expression of GhACIF1 gene, which can interact with SKP1 to form the SCF complex to mediate the PevD1-HR/SAR pathway [48]. Overexpression of GhACIF1 enhances resistance to Verticillium dahliae in Arabidopsis, while silencing of GhACIF1 confers sensitivity to Verticillium dahliae in cotton. VpEIFP1 can also form SCF complexes with SKP1 and CUL1 to mediate the degradation of Trxz, thus inducing ROS accumulation and activating defense reactions, thereby inhibiting the growth and development of PM [49]. The heterologous expression of VpEIFP1 in Arabidopsis accelerated the accumulation of H2O2 in vivo as well, as well as upregulating the expression of ICS2, NPR1, and HSP genes, resulting in plant tolerance to powdery mildew.

4. The F-Box Proteins and Abiotic Stress

Abiotic stress is also one of the key factors affecting plant growth and development. Abiotic stress mainly includes water stress (drought, flood), salt stress (salt, alkali), temperature stress (high temperature, low temperature), and toxic metal stress [50][51][52]. As sessile organisms, plants adapt to the environment only by a self-regulation system under abiotic stress conditions. Previous studies have shown that the F-box gene family members can participate in various abiotic stress responses. Drought stress adversely affects plant growth and development and is the main reason for crop failure [52]. Facing drought stress, plants reduce the damage caused by drought stress by regulating stomatal conductance and decreasing the transpiration rate to reduce moisture loss. Li et al. also found that the F-box gene SITLFP8, induced by osmotic stress in tomato, can change the stomatal density of leaves by affecting endoduplication and cell size [53]. Furthermore, overexpression of SILFP8 enhances drought resistance of tomato by reducing stomatal density and decreasing the transpiration rate to improve water use efficiency. In contrast, SITLFP8-Cas9 plants increased stomatal density and transpiration rate, showing sensitivity to drought. Similarly, MdMAX2 enhances drought resistance of plants by promoting stomatal closure to reduce water loss [54]. Overexpression of TaFBA1 in Arabidopsis enhances drought resistance by decreasing the content of H2O2, O2−, and MDA in vivo. However, interestingly, the transpiration rate and stomatal conductance of transgenic plants increased significantly. This increase in rate is proposed to be because increased stomatal opening can enhance CO2 absorption to maintain high-carbon fixation in leaves, further reducing ROS accumulation [55][56]. In addition, TaFBA1 can participate in the regulation of salt stress, oxidative stress, and high-temperature stress [57][58][59]. Compared with the wild type, the germination rate, root length, chlorophyll content, the net photosynthetic rate, and antioxidant enzyme activity of TaFBA1-overexpressing tobacco was significantly increased under oxidative and salt stress conditions.
Aluminum is the most abundant metal element in the crust. Under acidic conditions, some trivalent aluminum ion was dissolved to inhibit root growth of plants, thereby affecting the growth of plants. Acid soils account for more than 30% of arable land in the world, and therefore aluminum toxicity is also considered the second largest abiotic stress after drought [60][61]. F-box protein RAE1 can change plant tolerance to aluminum stress by regulating the stability of the transcription factor STOP1 [62]. The STOP1 transcription factor is a key regulator of the malic acid transporter AtALMT1 (a critical Al-tolerance gene). Mutation in STOP1 greatly suppress the expression of AtALMT1 gene [63]. RAE1 ubiquitinates STOP1 by the ubiquitin-26S proteasome pathway. STOP1 can positively regulate the expression of RAE1 by binding to the promoter region of RAE1. Thus, a negative feedback loop was formed. However, the ubiquitination of STOP1 mediated by RAE1 was inhibited under Al stress. This inhibition is proposed to be because of the post-translational modification of STOP1 caused by Al stress.
In addition to the above two abiotic stresses, salt and low-temperature stresses are also main factors limiting plant growth. The F-box protein EST1 is a negative regulator of salt stress. It can interact with Skp1 to form an SCF complex for MKK4 ubiquitination degradation, which decreases the activity of MKK4-MPK6 cascade reactions, decreasing in Na+/H+ antiporter activity [59]. The Na+/H+ antiporter activity of the loss-of-function mutant was significantly increased, which reduced Na+ accumulation in vivo, resulting in more tolerance to salt. In contrast, overexpression of EST1 plants was more sensitive to salt stress than WT. The F-box gene OsMsr9 in rice was induced by various stresses, and it can increase the salt tolerance of plants [64]. Under salt stress, the root length and plant height of OsMsr9-overexpressed plants were significantly higher than those of WT, and the content of proline and soluble sugars were improved in vivo. Similarly, the F-box protein LTSF1/2 in pepper is the key subunit of the SCF complex, which can regulate tolerance to low-temperature stress by activating antioxidant enzyme activity [65]. Under low-temperature stress, the growth of transgenic tobacco with heterologous expression of LTSF1 was found to be significantly higher than that of WT, and the expression of antioxidant enzyme genes such as GST and CAT in vivo was also significantly increased. In addition, the inhibition of CaF-box (GenBank, JX402925) gene by VIGS (virus-induced gene silencing) decreased the expression levels of the cold-induced genes (ERD15 and KIN1) [66]. In summary, these results suggest that the CaF-box affects cold tolerance in plant by regulating the expression of ERD15 and KIN1.

This entry is adapted from the peer-reviewed paper 10.3390/agronomy11112360

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