Skip to main content
Log in

F-Box Genes in Brassica rapa: Genome-Wide Identification, Structural Characterization, Expressional Validation, and Comparative Analysis

  • Original Paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

The F-box genes form one of the largest functionally important, rapidly evolving plant gene families. The encoded proteins mainly function as part of the Skp1–Cullin–F-box complex involved in ubiquitinating and degrading proteins. The F-box proteins also regulate diverse functions, including embryogenesis, organ development, floral organ identity, self-incompatibility, senescence, homeostasis, signaling, and responses to biotic and abiotic stresses. We identified 571 Brassica rapa F-box genes (BrFBX) and mapped approximately 560 genes onto 10 chromosomes. We also classified the duplicated genes. A phylogenetic tree consisting of the B. rapa F-box genes and an analysis of conserved motif sequences enabled us to categorize the identified genes into 11 subgroups based on node support. Additionally, we determined the intron–exon structural characteristics, which helped detect differences among the BrFBX genes. Gene ontology predictions enabled the classification of 431 genes related to biological processes, 63 genes involved in molecular functions, and 40 genes associated with cellular localization. The 69 genes differentially expressed under abiotic stress conditions (i.e., cold, drought, and salt stresses) and 446 genes expressed in specific tissues (i.e., calli, roots, leaves, stems, flowers, and siliques) were further categorized into three groups based on their expression levels. These genes exhibited various spatiotemporal expression patterns during stress treatments and in specific tissues. Based on motif and expression analyses, we selected approximately 30 BrFBX genes for quantitative reverse transcription polymerase chain reaction analysis, which detected differences in expression among eight tissues during B. rapa (Chiifu) growth. The genome-wide study results reveal the relationships among the BrFBX genes regarding evolution, structural variability, potential functions, and these data can be further used as a resource for the gene characterization in relation to growth, development, and during different stress conditions for the development of Brassica rapa.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Bai C, Richman R, Elledge SJ (1994) Human cyclin F. EMBO J 13:6087–6098

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME suite: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bellieny-Rabelo D, Oliveira AEA, Venancio TM (2013) Impact of whole-genome and tandem duplications in the expansion and functional diversification of the F-box family in legumes (Fabaceae). PLoS One 8:e55127

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Binder BM, Walker JM, Gagne JM, Emborg TJ, Hemmann G, Bleecker AB, Vierstra RD (2007) The Arabidopsis EIN3 binding F-box proteins EBF1 and EBF2 have distinct but overlapping roles in ethylene signaling. Plant Cell 19:509–523

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carretero-Paulet L, Galstyan A, Roig-Villanova I, Martínez-García JF, Bilbao-Castro JR, Robertson DL (2010) Genome-wide classification and evolutionary analysis of the bHLH family of transcription factors in Arabidopsis, poplar, rice, moss, and algae. Plant Physiol 153:1398–1412

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cheng F, Mandáková T, Wu J, Xie Q, Lysak MA, Wang X (2013) Deciphering the diploid ancestral genome of the mesohexaploid Brassica rapa. Plant Cell 25:1541–1554

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ciechanover A (1998) The ubiquitin–proteasome pathway: on protein death and cell life. EMBO J 17:7151–7160

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Conte SS, Chu HH, Chan-Rodriguez D, Punshon T, Vasques KA, Salt DE, Walker EL (2013) Arabidopsis thaliana yellow stripe1-like4 and yellow stripe1-like6 localize to internal cellular membranes and are involved in metal ion homeostasis. Front Plant Sci 4:283

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cui H-R, Zhang Z-R, Lv W, Xu J-N, Wang X-Y (2015) Genome-wide characterization and analysis of F-box protein-encoding genes in the Malus domestica genome. Mol Gen Genomics 290:1435–1446

    Article  CAS  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jürgens G, Estelle M (2005) Plant development is regulated by a family of auxin receptor F-box proteins. Dev Cell 9(1):109–119

    Article  PubMed  CAS  Google Scholar 

  • Divol F, Couch D, Conéjéro G, Roschzttardtz H, Mari S, Curie C (2013) The Arabidopsis YELLOW STRIPE LIKE4 and 6 transporters control iron release from the chloroplast. Plant Cell 25:1040–1055

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Doerks T, Copley RR, Schultz J, Ponting CP, Bork P (2002) Systematic identification of novel protein domain families associated with nuclear functions. Genome Res 12:47–56

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dong L, Wang L, Zhang Y, Zhang Y, Deng X, Xue Y (2006) An auxin-inducible F-box protein CEGENDUO negatively regulates auxin-mediated lateral root formation in Arabidopsis. Plant Mol Biol 60:599–615

    Article  PubMed  CAS  Google Scholar 

  • Durfee T, Roe JL, Sessions RA, Inouye C, Serikawa K, Feldmann KA, Weigel D, Zambryski PC (2003) The F-box-containing protein UFO and AGAMOUS participate in antagonistic pathways governing early petal development in Arabidopsis. PNAS 100(14):8571–8576

    Article  PubMed  CAS  Google Scholar 

  • Eshraghi L, Anderson JP, Aryamanesh N, McComb JA, Shearer B, St J, Hardy GE (2014) Suppression of the auxin response pathway enhances susceptibility to Phytophthora cinnamomi while phosphite-mediated resistance stimulates the auxin signaling pathway. BMC Plant Biol 14:68

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Espinosa-Ruiz A, Bellés JM, Serrano R, Culiáñez-MacIà FA (1999) Arabidopsis thaliana AtHAL3: a flavoprotein related to salt and osmotic tolerance and plant growth. Plant J 20:529–539

    Article  PubMed  CAS  Google Scholar 

  • Fonseca S, Chico J, Solano R (2009) The jasmonate pathway: the ligand, the receptor and the core signalling module. Curr Opin Plant Biol 12:539–547

    Article  PubMed  CAS  Google Scholar 

  • Gagne JM, Downes BP, Shiu SH, Durski AM, Vierstra RD (2002) The F-box subunit of the SCF E3 complex is encoded by a diverse super family of genes in Arabidopsis. PNAS 99:11519–11524

    Article  PubMed  CAS  Google Scholar 

  • Goldman N, Yang Z (1994) A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 11:725–736

    PubMed  CAS  Google Scholar 

  • González-Carranza ZH, Rompa U, Peters JL, Bhatt AM, Wagstaff C, Stead AD, Roberts JA (2007) HAWAIIAN SKIRT: an F-box gene that regulates organ fusion and growth in Arabidopsis. Plant Physiol 144:1370–1382

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCF (TIR1)-dependent degradation of AUX/IAA proteins. Nature 414:271–276

    Article  PubMed  CAS  Google Scholar 

  • Gupta S, Garg V, Kant C, Bhatia S (2015) Genome-wide survey and expression analysis of F-box genes in chickpea. BMC Genomics 16:67

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Harmon FG, Kay SA (2003) The F box protein AFR is a positive regulator of phytochrome A-mediated light signaling. Curr Biol 13:2091–2096

    Article  PubMed  CAS  Google Scholar 

  • Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425–479

    Article  PubMed  CAS  Google Scholar 

  • Ho MS, Tsai P-I, Chien C-T (2006) F-box proteins: the key to protein degradation. J Biomed Sci 13:181–191

    Article  PubMed  CAS  Google Scholar 

  • Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8):1296–1297

    Article  PubMed  Google Scholar 

  • Hua Z, Zou C, Shiu S-H, Vierstra RD (2011) Phylogenetic comparison of F-box (FBX) gene super family within the plant kingdom reveals divergent evolutionary histories indicative of genomic drift. PLoS One 6:e16219

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hunter T (2007) The age of crosstalk: phosphorylation, ubiquitination, and beyond. Mol Cell 28:730–738

    Article  PubMed  CAS  Google Scholar 

  • Jain M, Nijhawan A, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi AK, Khurana JP (2007) F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol 143:1467–1483

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jia F, Wu B, Li H, Huang J, Zheng C (2013) Genome-wide identification and characterization of F-box family in maize. Mol Gen Genomics 288:559–577

    Article  CAS  Google Scholar 

  • Jonkers W, Rep M (2009) Lessons from fungal F-box proteins. Eukaryot Cell 8:677–695

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim HS, Delaney TP (2002) Arabidopsis SON1 is an F-box protein that regulates a novel induced defense response independent of both salicylic acid and systemic acquired resistance. Plant Cell 14:1469–1482

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim J, Lee J, Choi J-P, Park I, Yang K, Kim MK, Lee Y, Nou IS, Kim DS, Min S, Park S, Kim HR (2014) Functional innovations of three chronological mesohexaploid Brassica rapa genomes. BMC Genomics 15:606

    Article  PubMed  PubMed Central  Google Scholar 

  • Lai CP, Lee CL, Chen PH, Wu SH, Yang CC, Shaw JF (2004) Molecular analyses of the Arabidopsis TUBBY-like protein gene family. Plant Physiol 134:1586–1597

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H et al (2007) Clustal W and clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Lechner E, Achard P, Vansiri A, Potuschak T, Genschik P (2006) F-box proteins everywhere. Curr Opin Plant Biol 9:631–638

    Article  PubMed  CAS  Google Scholar 

  • Lee SC, Lim MH, Kim JA, Lee SI, Kim JS, Jin M, Kwon SJ, Mun JH, Kim YK, Kim HU, Hur Y, Park BS (2008) Transcriptome analysis in Brassica rapa under the abiotic stresses using Brassica 24K oligo microarray. Mol Cell 26:595–605

    CAS  Google Scholar 

  • Li X, Duan X, Jiang H, Sun Y, Tang Y, Yuan Z, Guo J, Liang W, Chen L, Yin J, Ma H, Wang J, Zhang D (2006) Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice and Arabidopsis. Plant Physiol 141:1167–1184

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lohmann D, Stacey N, Breuninger H, Jikumaru Y, Müller D, Sicard A et al (2010) SLOW MOTION is required for within-plant auxin homeostasis and normal timing of lateral organ initiation at the shoot meristem in Arabidopsis. Plant Cell 22:335–348

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Long M, de Souza SJ, Gilbert W (1995) Evolution of the intron-exon structure of eukaryotic genes. Curr Opin Genet Dev 5:774–778

    Article  PubMed  CAS  Google Scholar 

  • Lyzenga WJ, Stone SL (2012) Abiotic stress tolerance mediated by protein ubiquitination. J Exp Bot 63:599–616

    Article  PubMed  CAS  Google Scholar 

  • Maldonado-Calderón MT, Sepúlveda-García E, Rocha-Sosa M (2012) Characterization of novel F-box proteins in plants induced by biotic and abiotic stress. Plant Sci 185–186:208–217

    Article  PubMed  CAS  Google Scholar 

  • Mazzucotelli E, Belloni S, Marone D, De Leonardis A, Guerra D, Di Fonzo N et al (2006) The e3 ubiquitin ligase gene family in plants: regulation by degradation. Curr Genomics 7:509–522

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Milia G, Camiolo S, Avesani L, Porceddu A (2015) The dynamic loss and gain of introns during the evolution of the Brassicaceae. Plant J 82:915–924

    Article  PubMed  CAS  Google Scholar 

  • Morello L, Breviario D (2008) Plant spliceosomal introns: not only cut and paste. Curr Genomics 9:227–238

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Navarro-Quezada A, Schumann N, Quint M (2013) Plant F-box protein evolution is determined by lineage-specific timing of major gene family expansion waves. PLoS One 8:e68672

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Paquis S, Mazeyrat-Gourbeyre F, Fernandez O, Crouzet J, Clément C, Baillieul F, Dorey S (2011) Characterization of a F-box gene up-regulated by phytohormones and upon biotic and abiotic stresses in grapevine. Mol Biol Rep 38:3327–3337

    Article  PubMed  CAS  Google Scholar 

  • Parrya G, Calderon-Villalobosb LI, Priggeb M, Peretc B, Dharmasiria S, Itohd H (2009) Complex regulation of the TIR1/AFB family of auxin receptors. PNAS 106:22540–22545

    Article  Google Scholar 

  • Paul P, Dhandapani V, Rameneni JJ, Li X, Sivanandhan G, Choi SR, Pang W, Im S, Lim YP (2016) Genome-wide analysis and characterization of Aux/IAA family genes in Brassica rapa. PLoS One 11:e0151522

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Perales L, Peñarrubia L, Cornejo MJ (2008) Induction of a polyubiquitin gene promoter by dehydration stresses in transformed rice cells. J Plant Physiol 165:159–171

    Article  PubMed  CAS  Google Scholar 

  • Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S, Koncz C, Genschik P (2003) EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F-box proteins: EBF1 and EBF2. Cell 115:679–689

    Article  PubMed  CAS  Google Scholar 

  • Rameneni JJ, Dhandapani V, Paul P, Im S, Oh M-H, Choi SR, Lim YP (2014) Genome-wide identification, characterization, and comparative phylogeny analysis of MADS-box transcription factors in Brassica rapa. Genes Genomics 36:509–525

    Article  CAS  Google Scholar 

  • Rameneni JJ, Lee Y, Dhandapani V, Yu X, Choi SR, Oh M-H, Lim YP (2015) Genomic and posttranslational modification analysis of leucine-rich repeat receptor-like kinases in Brassica rapa. PLoS One 10:e0142255

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Robinson PA, Ardley HC (2004) Ubiquitin-protein ligases. J Cell Sci 117:5191–5194

    Article  PubMed  CAS  Google Scholar 

  • Rogozin IB, Sverdlov AV, Babenko VN, Koonin EV (2005) Analysis of evolution of exon–intron structure of eukaryotic genes. Brief Bioinform 6:118–134

    Article  PubMed  CAS  Google Scholar 

  • Samach A, Klenz JE, Kohalmi SE, Risseeuw E, Haughn GW, Crosby WL (1999) The UNUSUAL FLORAL ORGANS gene of Arabidopsis thaliana is an F-box protein required for normal patterning and growth in the floral meristem. Plant J 20:433–445

    Article  PubMed  CAS  Google Scholar 

  • Schranz ME, Lysak MA, Mitchell-Olds T (2006) The ABC’s of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci 11:535–542

    Article  PubMed  CAS  Google Scholar 

  • Schumann N, Navarro-Quezada A, Ullrich K, Kuhl C, Quint M (2011) Molecular evolution and selection patterns of plant f-box proteins with C-terminal kelch repeats. Plant Physiol 155:835–850

    Article  PubMed  CAS  Google Scholar 

  • Schwager KM, Calderon-Villalobos LI, Dohmann EM, Willige BC, Knierer S, Nill C et al (2007) Characterization of the VIER F-box protein genes from Arabidopsis reveals their importance for plant growth and development. Plant Cell 19:1163–1178

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sharma M, Pandey GK (2016) Expansion and function of repeat domain proteins during stress and development in plants. Front Plant Sci 6:1218

    PubMed  PubMed Central  Google Scholar 

  • Shen H, Zhu L, Bu QY, Huq E (2012) MAX2 affects multiple hormones to promote photomorphogenesis. Mol Plant 5:750–762

    Article  PubMed  CAS  Google Scholar 

  • Skaar JR, Pagan JK, Pagano M (2009) SnapShot: F-box proteins I. Cell 137:1160–1161

    Article  PubMed  CAS  Google Scholar 

  • Somers DE, Kim WY, Geng R (2004) The F-box protein ZEITLUPE confers dosage-dependent control on the circadian clock, photomorphogenesis, and flowering time. Plant Cell 16:769–782

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stone SL, Callis J (2007) Ubiquitin ligases mediate growth and development by promoting protein death. Curr Opin Plant Biol 10:624–632

    Article  PubMed  CAS  Google Scholar 

  • Stothard P (2000) The sequence manipulation suite: Javascript programs for analyzing and formatting protein and DNA sequences. BioTechniques 28:1102–1104

    Article  PubMed  CAS  Google Scholar 

  • Su L, Shan J-X, Gao J-P, Lin H-X (2016) OsHAL3, a blue light-responsive protein, interacts with the floral regulator Hd1 to activate flowering in Rice. Mol Plant 9:233–244

    Article  PubMed  CAS  Google Scholar 

  • Sun SY, Chao DY, Li XM, Shi M, Gao JP, Zhu MZ, Yang HQ, Luan S, Lin HX (2009) OsHAL3 mediates a new pathway in the light-regulated growth of rice. Nat Cell Biol 11:845–851

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tong C, Wang X, Yu J, Wu J, Li W, Huang J, Dong C, Hua W, Liu S (2013) Comprehensive analysis of RNA-seq data reveals the complexity of the transcriptome in Brassica rapa. BMC Genomics 14:689

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ushijima K, Sassa H, Dandekar AM, Gradziel TM, Tao R, Hirano H (2003) Structural and transcriptional analysis of the self-incompatibility locus of almond: identification of a pollen-expressed F-box gene with haplotype-specific polymorphism. Plant Cell 15:771–781

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • van Nocker S, Ludwig P (2003) The WD-repeat protein super family in Arabidopsis: conservation and divergence in structure and function. BMC Genomics 4:50

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang L, Dong L, Zhang Y, Wu W, Deng X, Xue Y (2004) Genome-wide analysis of S-locus F-box-like genes in Arabidopsis thaliana. Plant Mol Biol 56:929–945

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Wang H, Wang J et al (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039

    Article  PubMed  CAS  Google Scholar 

  • Wang A, Fu M, Jiang X, Mao Y, Li X, Tao S (2014) Evolution of the F-box gene family in Euarchontoglires: gene number variation and selection patterns. PLoS One 9:e94899

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xiao W, Jang J (2000) F-box proteins in Arabidopsis. Trends Plant Sci 5:454–457

    Article  PubMed  CAS  Google Scholar 

  • Xing L, Li Z, Khalil R, Ren Z, Yang Y (2012) Functional identification of a novel F-box/FBA gene in tomato. Physiol Plant 144:161–168

    Article  PubMed  CAS  Google Scholar 

  • Xu G, Ma H, Nei M, Kong H (2009) Evolution of F-box genes in plants: different modes of sequence divergence and their relationships with functional diversification. PNAS 106:835–840

    Article  PubMed  Google Scholar 

  • Yan YS, Chen XY, Yang K, Sun ZX, Fu YP, Zhang YM, Fang RX (2011) Over-expression of an F-box protein gene reduces abiotic stress tolerance and promotes root growth in rice. Mol Plant 4:190–197

    Article  PubMed  CAS  Google Scholar 

  • Yang X, Kalluri UC, Jawdy S, Gunter LE, Yin T, Tschaplinski TJ, Weston DJ, Ranjan P, Tuskan GA (2008) The F-box gene family is expanded in herbaceous annual plants relative to woody perennial plants. Plant Physiol 148:1189–1200

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang Y, Xu W, Li Z, Deng XW, Wu W, Xue Y (2008) F-box protein DOR functions as a novel inhibitory factor for abscisic acid-induced stomatal closure under drought stress in Arabidopsis. Plant Physiol 148:2121–2133

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Gou M, Liu C-J (2013) Arabidopsis kelch repeat F-box proteins regulate phenylpropanoid biosynthesis via controlling the turnover of phenylalanine ammonia-lyase. Plant Cell 25:4994–5010

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou S, Sun X, Yin S, Kong X, Zhou S, Xu Y, Luo Y, Wang W (2014) The role of the F-box gene TaFBA1 from wheat (Triticum aestivum L.) in drought tolerance. Plant Physiol Biochem 84:213–223

    Article  PubMed  CAS  Google Scholar 

  • Zhou S-M, Kong X-Z, Kang H-H, Sun X-D, Wang W (2015) The involvement of wheat F-box protein gene in the oxidative stress tolerance of plants. PLoS One 10:e0122117

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Funding

This research was supported by Golden Seed Project (No. 213002-04-4-SB130), Ministry of Agriculture, Food and Rural Affairs (MAFRA), Ministry of Oceans and Fisheries (MOF), Rural Development Administration (RDA) and Korea Forest Service (KFS).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yong Pyo Lim.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Electronic Supplementary Material

Table S1

(DOCX 12 kb)

Table S2

(XLSX 59 kb)

Table S3

(XLSX 10 kb)

Table S4

(XLS 46 kb)

Table S5

(DOCX 13 kb)

Table S6

(XLSX 28 kb)

Fig. S1

(PDF 79 kb)

Fig. S2

(PDF 416 kb)

Fig. S3

(PDF 1507 kb)

Fig. S4

(GIF 182 kb)

High resolution image (TIF 6565 kb)

Fig. S5 (PDF 1.68 MB)

Fig. S6 (PDF 2.43 MB)

Fig. S7

(PDF 502 kb)

Fig. S8

(PDF 635 kb)

Fig. S9

(GIF 162 kb)

High resolution image (TIF 1276 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rameneni, J.J., Dhandapani, V., Paul, P. et al. F-Box Genes in Brassica rapa: Genome-Wide Identification, Structural Characterization, Expressional Validation, and Comparative Analysis. Plant Mol Biol Rep 36, 500–517 (2018). https://doi.org/10.1007/s11105-018-1083-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-018-1083-1

Keywords

Profiles

  1. Man-Ho Oh