- Background: F-box proteins are substrate-recognition components of the Skp1-Rbx1-Cul1-F-box protein (SCF) ubiquitin ligases. - Studies of F-box proteins from the model plant Arabidopsis and from many additional plant species have demonstrated that they belong to a super gene family, and function across almost all aspects of the plant life cycle. - The genome- wide analysis of the cotton F-box gene family is now possible thanks to the completion of several cotton genome sequencing projects.. - Although the WGD (whole-genome duplication) mode seems play a dominant role during cotton F-box gene expansion process, other duplication modes including TD (tandem duplication), PD (proximal duplication), and TRD (transposed duplication) also contribute significantly to the evolutionary expansion of cotton F-box genes. - 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0. - Full list of author information is available at the end of the article. - The E3 ligase in the Ub/26S proteasome pathway is essential for recognition of target proteins for ubiquitination, and is the specificity determin- ant of the E3 complex for appropriate targets [3]. - To date, several hundred E3 ubiquitin ligases have been identified, one of the best characterized being the SCF protein com- plex consisting of RBX1, SKP1, CULLIN, and F-box pro- teins [4, 5]. - Therefore, F-box proteins play a crucial role for defining the specific substrates of the SCF complexes for destruction [6, 7].. - Functional characterization of a limited number of plant F-box genes have demonstrated. - Gossypium hirsutum is also one of the descendant allotetraploid species and is believed to be derived from polyploidization between a spinnable-fiber- capable A genome species (Gossypium arboreum) and a non-spinnable-fiber-capable D genome species (Gossypium raimondii) [33]. - Collectively, only a few F-box proteins have been functionally explored in Gossypium hir- sutum, including two putative homologues of the MAX2 genes that have been shown to control shoot lateral branching in Arabidopsis [34]. - In our current study, we present the results of a genome-wide analysis of F-box genes in Gossypium hirsu- tum. - 592 F-box protein encoding genes were identified in the Gossypium hirsutume acc.TM-1 genome, and their gene structures, chromosomal locations, syntenic relation- ships across other cotton species, and duplication modes are presented, along with a discussion of the possible evo- lutionary effects on allotetraploid cotton F-box genes. - Our results provide the first overview of the Gossypium hirsutum F-box gene family, which we believe will lay the foundation for future func- tionality studies, particularly the F-box proteins that likely play important roles in hormone signal transduction.. - Identification and classification of F-box genes from Gossypium hirsutum. - After this initial screening, all F-box protein candidates were verified by the Pfam (http://pfam.sanger.ac.uk/search) and SMART (http://smart.embl-heidelberg.de) webserver, with an e-value cut-off of less than 1.0 to ensure each can- didate sequence contained at least one of the F-box motifs (PF00646, PF12937, PF13013, PF04300, PF07734, PF07735, PF08268 and PF08387). - In order to understand the evolution of the expansion of the cotton F-box genes, the F-box protein encoding genes from Gossypium raimondii and Gossypium arboreum were also identified and classified using the same approach.. - Dissection of different duplication modes of F-box genes from Gossypium hirsutum. - F- box genes within the Gossypium hirsutum genome were classified as transposed, proximal, tandem, or whole- genome duplications (WGD). - The func- tional annotations of F-box genes involved in any bio- logical process (BP) were predicted based on putative homologues from Arabidopsis. - The log2 transformed RPKM (reads per kilobase per million) values or TPM (transcripts copies per mil- lion tags) values were used to measure expression levels of the F-box genes, and to generate heat maps. - To identify the Gossypium hirsutum F-box genes which can potentially form the SCF complexes involved in plant hormone signal transduction pathways, we first ob- tained the protein sequences of the Arabidopsis F-box proteins involved in hormone signal transduction based on previous studies, including TIR1 in the auxin signal- ing pathway, SLY1 in the gibberellin signaling pathway,. - EBF2 in the ethylene signaling pathway and the F-box genes that have been proposed to play a role in the ABA signaling pathway [41, 42]. - Identification and classification of F-box genes in Gossypium hirsutum. - After the repetitive se- quences were removed, 2904 sequences were retained, and were submitted to the Pfam and SMART webserver to confirm that the identified F-box proteins contained at least one of the established F-box domains. - The polyploidization between the A-genome and D-genome species leads to the tetraploid AD species con- taining two copies of the entire A and D genomes, which instead of two copies of each genome (one from each par- ent), has four (two from each parent). - In our current studies, we found that Gossypium hir- sutum possesses almost twice the number of F-box genes as compared to its diploid parents Gossypium arboretum and Gossypium raimondii, which indicates that most of the F-box genes are retained after poly- ploidization between the two diploid cotton species, Gossypium raimondii and Gossypium arboreum.. - According to the functional domains found within the C-terminal region of the identified cotton F-box proteins, they can be grouped into 17 different subfam- ilies (Fig. - scaffold proteins supporting other components of the E3 ubiquitin ligase complexes. - The genomic distribution and gene expansion events of Gossypium hirsutum F-box genes. - Notably, longer chromosomes do not necessarily contain more F-box gene family members, indicating that the number of F-box genes on each. - 1 The number and classicization of F-box genes identified in G. - All the F-box genes were classified into different subfamilies based on their C-terminus functional domains (Pfam domains). - This result demonstrates that cotton F-box protein encoding genes, like the F-box genes in other plant species, are unevenly distributed on the 26 chromosomes of Gos- sypium hirsutum . - When the genome from Gossypium arboreum (A- genome) and the genome from Gossypium raimondii (D-genome) were combined to produce the allotetra- ploid cotton AD genome, most of the cotton genes appear to have been duplicated at the whole genome level. - To elucidate the evolutionary genome re- arrangement and duplication patterns of the F-box protein encoding genes in Gossypium hirsutum, we performed a gene duplication event analysis includ- ing whole genome duplication (WGD), tandem duplication (TD), proximal duplication (PD) and transposed duplication (TRD) (Fig. - A total of 303 WGD F-box genes, corresponding to 166 duplicated gene pairs, were identified in Gossypium hirsutum which represents the largest portion of F-box genes in allotetraploid cotton, the number of WGD dupli- cated genes on each of the 26 Gossypium hirsutum chromosomes ranging from 0 on chromosomes 4 and 17 to 22 on chromosome 5 (Additional file 1:. - The results also indicate that the F-box genes of Gossypium hirsutum (AD-genome) mainly originated from interspecific hybridization spe- cies Gossypium arboreum (A-genome) and the species Gossypium raimondii (D-genome).. - In previous studies, major efforts were spent on identifi- cation of the contributions of WGD or TD duplications to the expansion of gene families in Gossypium hirsutum. - As some recent studies have suggested potential roles of transposed and dispersed gene duplication to plant genome evolution [14], in the present study, we explored all possible duplica- tion modes of the cotton F-box genes, in order to deter- mine their potential contributions to F-box gene family expansion. - 2 The distribution of F-box genes on the 26 G. - To further explore the dynamics of evolution of Gossy- pium hirsutum F-box genes, comparative studies of the different modes of gene duplication were carried out.. - This involved estimation of the Ka (non-synonymous substitutions per site), Ks (synonymous substitutions per site) and Ka/Ks ratios for each duplication pair, resulting in a measure of the divergence of cotton F-box gene family members. - 3 The synteny pairs of cotton F-box genes from different duplication mode diagrams. - We calculated that the average timing of the divergence of WGD, TD, PD, and TRD mapped back to and 2.2 million years ago (MYA), respectively. - 1), which further demonstrates that cotton F-box genes. - To further predict the biological functions of the F- box protein encoding genes in Gossypium hirsutum, Gene Ontology (GO) analysis was performed to probe orthologous genes function based on previous pub- lished F-box protein studies. - Most of the cotton F-box proteins were identified as involved in the molecular function (GO:0005515) of protein binding, consistent with the established roles that F-box proteins play in post-translational modifications. - In addition, 15 of the F-box genes are involved in specific biological pro- cesses (BP) (Table 1). - The tissue-specific expression profiles of the 592 cot- ton F-box protein encoding genes are publicly accessible from a collection of Gossypium hirsutum gene expres- sion databases. - A further 440 genes with FPKM values greater than 2 and being expressed in at least one of the selected tissues (Additional file 5:. - K-means analysis resulted in classification of the high expression genes into 5 clusters (high expression in. - In each cluster, we noticed that several F-box genes exhibited differential expression in one or more of the cotton plant tissues. - Identification of possible F-box genes in the SCF. - Most of the F-box proteins can form SCF complexes by binding with the Skp1 protein, and Skp1 further inter- acts with the scaffold proteins Cullin1 and Rbx1 to form the major components of classic SCF E3 complexes.. - Among all the components, F-box proteins serve as the protein recruiting components of the SCF type E3 ubi- quitin ligase to determine the specificities of the sub- strate proteins for ubiquitination and degradation [55].. - Studies performed on the model plant Arabidopsis reveal that the common strategy used by plants to precisely re- spond to hormone signals is by the modulation of the stabilities of key transcription factors by an F-box pro- tein containing ubiquitin ligase [41]. - By the end of the course of IAA and GA treatments, representa- tive AtTIR1 homologous genes (Gh_A08G0662, Gh_. - F-box family proteins are one of the super protein fam- ilies in plants, and studies on a limited number of plant F-box proteins have demonstrated that they play diverse roles in various key plant development and physiological processes, including germination [18], floral meristem identity and organ development photo- morphogenesis, the circadian clock, flowering time regulation of hormone signaling transduction plant response to stress conditions plant nutrition usage [77], plant reproductive processes [16, 17], and plant primary and secondary metabolism . - Compared with the vast number of plant F-box genes that have been identified, functional characterizations of the ma- jority of F-box proteins still lags far behind.. - 5 Heat map showing high expression F-box genes in 5 clusters based on K-means classification. - However, information available for cotton F-box genes and for their roles in the cotton plant life cycle is lim- ited. - Here, we first conducted a genome-wide survey of the cotton F-box gene family. - identified in the new version of the Gossypium hirsutum genome database (http://mascotton.njau.edu.cn). - In addition to the analysis of contribution of WGD for cotton F-box gene expansion, we also analyzed other modes of gene duplication such as transposed or dispersed gene duplications for their potential contribu- tions to the expansion of the cotton F-box gene family.. - As compared to the 592 F-box genes found in the Gossy- pium hirsutum genome, the 300 F-box genes we found. - The well-established Arabidopsis hormone related SCF complexes were colored as pink blocks while the green color blocks represent the protein substrates or the down-stream target genes of the selected SCF ubiquitin ligases. - Domain analysis of the cotton F-box proteins revealed that a large portion (54%. - 320 out of 592) of the predicted proteins did not have any other known functional domain beyond the F- box motif itself, and this group of F-box proteins was thereafter designated as Fbox. - 7 Expression dynamics of the candidate F-box genes under IBA, GA3, ABA, ACC treatments. - There are no previous reports of the characterizations of cotton KFBs, and it will therefore be interesting to explore the biological functions played by cotton KFBs for their potential contributions to important agricultural traits.. - 592) of the cotton F-box proteins belong to FBA sub- family and, based on the established model, the func- tional significance of this F-box protein subfamily is also worthy to be further explored experimentally in the future.. - Plant F-box proteins also have been shown to play critical roles during most of the known hormone signal transduc- tion processes, either serving as the hormone receptors, or as key transcription regulators during hormone perception [41]. - Functional characterization of most of the F-box genes so far has been limited in the model plants, such as Arabi- dopsis, and their homologues in other crop species likely play similar functions. - 50%) of the F-box genes carried out in our study confirmed the presence of cotton homologues of classic Arabidopsis hormone related F- box proteins suggesting their probable involvement in similar or identical biological pathways. - To investigate the po- tential functions of these homologues in cotton plants responding to major hormone signaling changes, we per- formed quantitative RT PCR analysis of the expressions of the representative genes after the cotton leaves were treated with IAA, JA, GA, ABA, and ACC. - We analyzed the potential effects of GA treatment on the expression of the 4 cotton homologues of Arabi- dopsis SLY1. - Two (Gh_A05G2244 and Gh_D05G2503) of the three selected genes showed steady increases over the course of GA treatment. - Further protein-protein interaction experiments will be needed to verify whether any of these SLY1 homologues can interact with the cot- ton DELLA protein, in order to directly determine whether they are serving as the F-box protein component of the cotton SCFS LY1 complex participating in the cotton GA signaling pathway. - The Arabidopsis F-box protein MORE AXILLARY GROWTH2 (MAX2) has previously been characterized for its role in plant branching and MAX2 appears essential for the perception of the newly- characterized phytohormone strigolactone, a negative regulator of polar auxin transport in Arabidopsis. - A number of studies also have indicated that MAX2 contributes to plant responses to both biotic and abiotic stresses through modulation of the ABA signaling pathway and that MAX2 gene expression can be influenced by ABA treatment . - Digital expression profiles of the F-box genes across different tissues were also explored and several F- box genes were identified with tissue specific expression patterns implying their possible involvement in the growth and development of selected organs. - The expansion modes of F-box genes in upland cotton. - a: The number of F-box genes of different duplication modes. - Organ specific expression of F-box genes in the G. - Organ-specific expression patterns of F-box genes. - Protein quality control and elimination of protein waste: the role of the ubiquitin-proteasome system. - Structure of the Cul1-Rbx1-Skp1-F box (Skp2) SCF ubiquitin ligase complex. - Evolution of F-box genes in plants: different modes of sequence divergence and their relationships with functional diversification. - Genome-wide analyses of the soybean F-box gene family in response to salt stress. - Genome-wide survey and expression analysis of F-box genes in chickpea. - The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. - Genome sequence of the cultivated cotton Gossypium arboreum. - Taxonomy and evolution of the cotton genus, Gossypium. - Genome-wide identification and expression analyses of the pectate lyase (PEL) gene family in cotton ( Gossypium hirsutum L. - A genome-wide analysis of the small auxin-up RNA (SAUR) gene family in cotton. - Genome-wide identification and functional analyses of the CRK gene family in cotton reveals GbCRK18 confers Verticillium wilt resistance in Gossypium barbadense. - JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. - The role of the F-box gene TaFBA1 from wheat (Triticum aestivum L.) in drought tolerance.
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