Skip to main content
Log in

The F-box family genes as key elements in response to salt, heavy mental, and drought stresses in Medicago truncatula

  • Original Paper
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

F-box protein is a subunit of Skp1-Rbx1-Cul1-F-box protein (SCF) complex with typically conserved F-box motifs of approximately 40 amino acids and is one of the largest protein families in eukaryotes. F-box proteins play critical roles in selective and specific protein degradation through the 26S proteasome. In this study, we bioinformatically identified 972 putative F-box proteins from Medicago truncatula genome. Our analysis showed that in addition to the conserved motif, the F-box proteins have several other functional domains in their C-terminal regions (e.g., LRRs, Kelch, FBA, and PP2), some of which were found to be M. truncatula species-specific. By phylogenetic analysis of the F-box motifs, these proteins can be classified into three major families, and each family can be further grouped into more subgroups. Analysis of the genomic distribution of F-box genes on M. truncatula chromosomes revealed that the evolutional expansion of F-box genes in M. truncatula was probably due to localized gene duplications. To investigate the possible response of the F-box genes to abiotic stresses, both publicly available and customer-prepared microarrays were analyzed. Most of the F-box protein genes can be responding to salt and heavy metal stresses. Real-time PCR analysis confirmed that some of the F-box protein genes containing heat, drought, salicylic acid, and abscisic acid responsive cis-elements were able to respond to the abiotic stresses.

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

Access this article

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

Similar content being viewed by others

References

  • Aloui A, Recorbet G, Gollotte A, Robert F, Valot B, Gianinazzi-Pearson V, Aschi-Smiti S, Dumas-Gaudot E (2009) On the mechanisms of cadmium stress alleviation in Medicago truncatula by arbuscular mycorrhizal symbiosis: a root proteomic study. Proteomics 9:420–433

    Article  CAS  PubMed  Google Scholar 

  • Andrade MA, Gonzalez-Guzman M, Serrano R, Rodriguez PL (2001) A combination of the F-box motif and Kelch repeats defines a large Arabidopsis family of F-box proteins. Plant Mol Biol 46:603–614

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bellieny-Rabelo D, Oliveira AA, 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  CAS  PubMed Central  PubMed  Google Scholar 

  • Benedito VA, Torres-Jerez I, Murray JD, Andriankaja A, Allen S et al (2008) A gene expression atlas of the model legume Medicago truncatula. Plant J 55:504–513

    Article  CAS  PubMed  Google Scholar 

  • Bonhomme M, Andre O, Badis Y, Ronfort J, Burgarella C et al (2014) High-density genome-wide association mapping implicates an F-box encoding gene in Medicago truncatula resistance to Aphanomyces euteiches. New Phytol 201:1328–1342

    Article  CAS  PubMed  Google Scholar 

  • Cardozo T, Pagano M (2004) The SCF ubiquitin ligase: insights into a molecular machine. Nat Rev Mol Cell Biol 5:739–751

    Article  CAS  PubMed  Google Scholar 

  • Cenciarelli C, Chiau DS, Guardavaccaro D, Parks W, Vidal M, Pagano M (1999) Identification of a family of human F-box proteins. Curr Biol 9:1177–1179

    Article  CAS  PubMed  Google Scholar 

  • Chae E, Tan QKG, Hill TA, Irish VF (2008) An Arabidopsis F-box protein acts as a transcriptional co-factor to regulate floral development. Development 135:1235–1245

    Article  CAS  PubMed  Google Scholar 

  • Cui X, Xu SM, Mu DS, Yang ZM (2009) Genomic analysis of rice microRNA promoters and clusters. Gene 431:61–66

    Article  CAS  PubMed  Google Scholar 

  • De Lorenzo L, Merchan F, Blanchet S, Megias M, Frugier F, Crespi M, Sousa C (2007) Differential expression of the TFIIIA regulatory pathway in response to salt stress between Medicago truncatula genotypes. Plant Physiol 145:1521–1532

    Article  PubMed Central  PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    Article  CAS  PubMed  Google Scholar 

  • Dinant S, Clark AM, Zhu Y, Vilaine F, Palauqui JC, Kusiak C, Thompson GA (2003) Diversity of the superfamily of phloem lectins (phloem protein 2) in angiosperms. Plant Physiol 131:114–128

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gachomo EW, Jimenez-Lopez JC, Baptiste LB, Kotchoni SO (2014) GIGANTUS1 (GTS1), a member of Transducin/WD40 protein superfamily, controls seed germination, growth and biomass accumulation through ribosome-biogenesis protein interactions in Arabidopsis thaliana. BMC Plant Biol 14:37

    Article  PubMed Central  PubMed  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 superfamily of genes in Arabidopsis. Proc Natl Acad Sci U S A 99:11519–11524

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Giraudat J (1995) Abscisic acid signaling. Curr Opin Cell Biol 7:232–238

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Gu Z, Cavalcanti A, Chen FC, Bouman P, Li WH (2002) Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Mol Biol Evol 19:256–262

    Article  CAS  PubMed  Google Scholar 

  • Hepworth SR, Klenz JE, Haughn GW (2006) UFO in the Arabidopsis inflorescence apex is required for floral-meristem identity and bract suppression. Planta 223:769–778

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Imaizumi T, Tran HG, Swartz TE, Briggs WR, Kay SA (2003) FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426:302–306

    Article  CAS  PubMed  Google Scholar 

  • Irizarry RA, Hobbs B, Speed TP (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249–264

    Article  PubMed  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 duringpPanicle and seed development, and regulation by light and abiotic stress. Plant Physiol 143:1467–1483

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jin J, Cardozo T, Lovering RC, Elledge SJ, Pagano M, Harper JW (2004) Systematic analysis and nomenclature of mammalian F-box proteins. Genes Dev 18:2573–2580

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451

    Article  CAS  PubMed  Google Scholar 

  • Kim SJ, Ryu MY, Kim WT (2012) Suppression of Arabidopsis RING-DUF1117 E3 ubiquitin ligases, AtRDUF1 and AtRDUF2, reduces tolerance to ABA-mediated drought stress. Biochem Biophys Res Commun 420:141–147

    Article  CAS  PubMed  Google Scholar 

  • Kipreos ET, Pagano M (2000) The F-box protein family. Genome Biol 1. REVIEW S3002

  • Kuroda H, Takahashi N, Shimada H, Seki M, Shinozaki K, Matsui M (2002) Classification and expression analysis of Arabidopsis F-box-containing-protein genes. Plant Cell Physiol 43:1073–1108

    Article  CAS  PubMed  Google Scholar 

  • Laufs P, Coen E, Kronenberger J, Traas J, Doonan J (2003) Separable roles of UFO during floral development revealed by conditional restoration of gene function. Development 130:785–796

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Levin JZ, Meyerowitz EM (1995) UFO: an Arabidopsis gene involved in both floral meristem and floral organ development. Plant Cell 7:529–548

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li D, Zhang Y, Hu X, Shen X, Ma L, Su Z, Wang T, Dong J (2011) Transcriptional profiling of Medicago truncatula under salt stress identified a novel CBF transcription factor MtCBF4 that plays an important role in abiotic stress responses. BMC Plant Biol 11:109

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li D, Su Z, Dong J, Wang T (2009) An expression database for roots of the model legume Medicago truncatula under salt stress. BMC Genomics 10:517

    Article  PubMed Central  PubMed  Google Scholar 

  • Li H, Wang L, Yang ZM (2015) Co-expression analysis reveals a group of genes potentially involved in regulation of plant response to iron-deficiency. Gene 554:16–24

    Article  CAS  PubMed  Google Scholar 

  • Moon J, Parry G, Estelle M (2004) The ubiquitin-proteasome pathway and plant development. Plant Cell 16:3181–3195

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mukhopadhyay S, Jackson PK (2011) The tubby family proteins. Genome Biol 12:225

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nelson DC, Lasswell J, Rogg LE, Cohen MA, Bartel B (2000) FKF1, a clockcontrolled gene that regulates the transition to flowering in Arabidopsis. Cell 101:331–340

    Article  CAS  PubMed  Google Scholar 

  • Njälsson R, Norgren S (2005) Physiological and pathological aspects of GSH metabolism. Acta Paediatr 94:132–137

    Article  PubMed  Google Scholar 

  • Patton EE, Willems AR, Tyers M (1998) Combinatorial control in ubiquitindependent proteolysis: don’t Skp the F-box hypothesis. Trends Genet 14:236–243

    Article  CAS  PubMed  Google Scholar 

  • Peifer M, Berg S, Reynolds AB (1994) A repeating amino acid motif shared by proteins with diverse cellular roles. Cell 76:789–791

    Article  CAS  PubMed  Google Scholar 

  • Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401

    Article  CAS  PubMed  Google Scholar 

  • Schultz TF, Kiyosue T, Yanovsky M, Wada M, Kay SA (2001) A role for LKP2 in the circadian clock of Arabidopsis. Plant Cell 13:2659–2670

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shen Q, Jiang M, Li H, Che LL, Yang ZM (2011) Expression of a Brassica napus heme oxygenase confers plant tolerance to mercury toxicity. Plant Cell Environ 34:752–763

    Article  CAS  PubMed  Google Scholar 

  • Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 55:555–559

    Article  CAS  PubMed  Google Scholar 

  • Smith TF, Gaitatzes C, Saxena K, Neer EJ (1999) The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 24:181–185

    Article  CAS  PubMed  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  CAS  PubMed Central  PubMed  Google Scholar 

  • Song JB, Gao S, Sun D, Li H, Shu XX, Yang ZM (2013) miR394 and LCR are involved in Arabidopsis salt and drought stress responses in an abscisic acid-dependent manner. BMC Plant Biol 13:210

    Article  PubMed Central  PubMed  Google Scholar 

  • Song JB, Huang SQ, Dalmay T, Yang ZM (2012) Regulation of leaf morphology by microRNA394 and its target LEAF CURLING RESPONSIVENESS. Plant Cell Physiol 53:1283–1294

    Article  CAS  PubMed  Google Scholar 

  • Sullivan JA, Shirasu K, Deng XW (2003) The diverse roles of ubiquitin and the 26S proteasome in the life of plants. Nat Rev Genet 4:948–958

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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  CAS  PubMed Central  PubMed  Google Scholar 

  • Yang S, Zhang X, Yue JX, Tian D, Chen JQ (2008a) Recent duplications dominateNBS-encoding gene expansion in two woody species. Mol Genet Genomics 280:187–198

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Kalluri UC, Jawdy S, Gunter LE, Yin T et al (2008b) The F-Box gene family is expanded in herbaceous annual plants relative to woody perennial plants. Plant Physiol 148:1189–1200

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yang ZM, Wang J, Wang SW, Xu LL (2003) Salicylic acid-induced aluminum tolerance by modulation of citrate efflux from roots of Cassia tora L. Planta 217:168–174

    CAS  PubMed  Google Scholar 

  • Zhou ZS, Huang SQ, Guo K, Mehta SK, Zhang PC, Yang ZM (2007) Metabolic adaptations to mercury-induced oxidative stress in roots of Medicago sativa L. J Inorg Biochem 101:1–9

    Article  CAS  PubMed  Google Scholar 

  • Zhou ZS, Guo K, Elbaz AA, Yang ZM (2009) Salicylic acid alleviates mercury toxicity by preventing oxidative stress in roots of Medicago sativa. Environ Exp Bot 65:27–34

    Article  CAS  Google Scholar 

  • Zhou ZS, Zeng HQ, Liu ZP, Yang ZM (2012) Genome-wide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal. Plant Cell Environ 35:86–99

    Article  PubMed  Google Scholar 

  • Zhou ZS, Yang SN, Li H, Zhu CC, Liu ZP, Yang ZM (2013) Molecular dissection of mercury-responsive transcriptome and sense/antisense genes in Medicago truncatula by high-throughput sequencing. J Hazard Mater 252–253:123–131

    Article  PubMed  Google Scholar 

Download references

Funding

This study was funded by the National Natural Science Foundation of China (31071343 and 31200204) and Colleges and Universities in Jiangsu Province plans to graduate research and innovation (KYZZ_0181).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Zhao Sheng Zhou or Zhi Min Yang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(XLS 468 kb)

ESM 2

(PPT 229 kb)

ESM 3

(XLS 142 kb)

ESM 4

(XLS 230 kb)

ESM 5

(DOC 42 kb)

ESM 6

(DOC 44 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Song, J.B., Wang, Y.X., Li, H.B. et al. The F-box family genes as key elements in response to salt, heavy mental, and drought stresses in Medicago truncatula . Funct Integr Genomics 15, 495–507 (2015). https://doi.org/10.1007/s10142-015-0438-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-015-0438-z

Keywords

Navigation