Skip to main content
SpringerLink
Log in

Soybean 14-3-3 gene family: identification and molecular characterization

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The 14-3-3s are a group of proteins that are ubiquitously found in eukaryotes. Plant 14-3-3 proteins are encoded by a large multigene family and are involved in signaling pathways to regulate plant development and protection from stress. Recent studies in Arabidopsis and rice have demonstrated the isoform specificity in 14-3-3s and their client protein interactions. However, detailed characterization of 14-3-3 gene family in legumes has not been reported. In this study, soybean 14-3-3 proteins were identified and their molecular characterization performed. Data mining of soybean genome and expressed sequence tag databases identified 18 14-3-3 genes, of them 16 are transcribed. All 16 SGF14s have higher expression in embryo tissues suggesting their potential role in seed development. Subcellular localization of all transcribed SGF14s demonstrated that 14-3-3 proteins in soybean have isoform specificity, however, some overlaps were also observed between closely related isoforms. A comparative analysis of SGF14s with Arabidopsis and rice 14-3-3s indicated that SGF14s also group into epsilon and non-epsilon classes. However, unlike Arabidopsis and rice 14-3-3s, SGF14s contained only one kind of gene structure belonging to each class. Overall, soybean consists of the largest family of 14-3-3 proteins characterized to date. Our results provide a solid framework for further investigations into the role of SGF14s and their involvement in legume-specific functions.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Abbreviations

DAP:

Days after pollination

EST:

Expressed sequence tag

TC:

Tentative contig

BiFC:

Bimolecular fluorescence complementation assay

BLAST:

Basic local alignment search tool

YFP:

Yellow fluorescent protein

YN:

N-terminal half of yellow fluorescent protein

YC:

C-terminal half of yellow fluorescent protein

MYA:

Million years ago

References

  • Agrawal GK, Thelen JJ (2006) Large scale identification and quantitative profiling of phosphoproteins expressed during seed filling in oilseed rape. Mol Cell Proteomics 5:2044–2059

    Article  CAS  PubMed  Google Scholar 

  • Agrawal GK, Hajduch M, Graham K, Thelen JJ (2008) In-depth investigation of the soybean seed-filling proteome and comparison with a parallel study of rapeseed. Plant Physiol 148:504–518

    Article  CAS  PubMed  Google Scholar 

  • Aitken A (2006) 14-3-3 proteins: a historic overview. Semin Cancer Biol 16:162–172

    Article  CAS  PubMed  Google Scholar 

  • Aksamit A, Korobczak A, Skala J, Lukaszewicz M, Szopa J (2005) The 14-3-3 gene expression specificity in response to stress is promoter-dependent. Plant Cell Physiol 46:1635–1645

    Article  CAS  PubMed  Google Scholar 

  • Alsterfjord M, Sehnke PC, Arkell A, Larsson H, Svennelid F, Rosenquist M, Ferl RJ, Sommarin M, Larsson C (2004) Plasma membrane H(+)-ATPase and 14-3-3 isoforms of Arabidopsis leaves: evidence for isoform specificity in the 14-3-3/H(+)-ATPase interaction. Plant Cell Physiol 45:1202–1210

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Arumuganathan K, Earle ED (1991) Estimation of nuclear DNA content of plants by flow cytometry. Plant Mol Biol Rep 9:229–241

    Article  CAS  Google Scholar 

  • Bai MY, Zhang LY, Gampala SS, Zhu SW, Song WY, Chong K, Wang ZY (2007) Functions of OsBZR1 and 14-3-3 proteins in brassinosteroid signaling in rice. Proc Natl Acad Sci USA 104:13839–13844

    Article  CAS  PubMed  Google Scholar 

  • Bihn EA, Paul AL, Wang SW, Erdos GW, Ferl RJ (1997) Localization of 14-3-3 proteins in the nuclei of Arabidopsis and maize. Plant J 12:1439–1445

    Article  CAS  PubMed  Google Scholar 

  • Blanc G, Wolfe KH (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16:1667–1678

    Article  CAS  PubMed  Google Scholar 

  • Blanc G, Barakat A, Guyot R, Cooke R, Delseny M (2000) Extensive duplication and reshuffling in the Arabidopsis genome. Plant Cell 12:1093–1101

    Article  CAS  PubMed  Google Scholar 

  • Brandt J, Thordal-Christensen H, Vad K, Gregersen PL, Collinge DB (1992) A pathogen-induced gene of barley encodes a protein showing high similarity to a protein kinase regulator. Plant J 2:815–820

    CAS  PubMed  Google Scholar 

  • Bunney TD, van Walraven HS, de Boer AH (2001) 14-3-3 protein is a regulator of the mitochondrial and chloroplast ATP synthase. Proc Natl Acad Sci USA 98:4249–4254

    Article  CAS  PubMed  Google Scholar 

  • Chang I-F, Curran A, Woolsey R, Quilici D, Cushman JC, Mittler R, Harmon A, Harper JF (2009) Proteomic profiling of tandem affinity purified 14-3-3 protein complexes in Arabidopsis thaliana. Proteomics 9:2967–2985

    Article  CAS  PubMed  Google Scholar 

  • Chen F, Li Q, Sun L, He Z (2006) The rice 14-3-3 gene family and its involvement in responses to biotic and abiotic stress. DNA Res 13:53–63

    Article  CAS  PubMed  Google Scholar 

  • Chevalier D, Morris ER, Walker JC (2009) 14-3-3 and FHA domains mediate phosphoprotein interaction. Annu Rev Plant Biol 60:67–91

    Article  CAS  PubMed  Google Scholar 

  • Datta R, Chamusco KC, Chourey PS (2002) Starch biosynthesis during pollen maturation is associated with altered patterns of gene expression in maize. Plant Physiol 130:1645–1656

    Article  CAS  PubMed  Google Scholar 

  • DeLille JM, Sehnke PC, Ferl RJ (2001) The arabidopsis 14-3-3 family of signaling regulators. Plant Physiol 126:35–38

    Article  CAS  PubMed  Google Scholar 

  • Dhaubhadel S, Li X (2010) A new client for 14-3-3 proteins: GmMYB176, an R1 MYB transcription factor. Plant Signal Behav 5:1–3

    Article  Google Scholar 

  • Dhaubhadel S, Farhangkhoee M, Chapman R (2008) Identification and characterisation of isoflavonoid specific glycosyltransferase and malonyltransferase from soybean seeds. J Exp Bot 59:981–994

    Article  CAS  PubMed  Google Scholar 

  • Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545

    CAS  PubMed  Google Scholar 

  • Fu H, Subramanian RR, Masters SC (2000) 14-3-3 proteins: structure, function, and regulation. Annu Rev Pharmacol Toxicol 40:617–647

    Article  CAS  PubMed  Google Scholar 

  • Gampala SS, Kim TW, He JX, Tang W, Deng Z, Bai MY, Guan S, Lalonde S, Sun Y, Gendron JM, Chen H, Shibagaki N, Ferl RJ, Ehrhardt D, Chong K, Burlingame AL, Wang ZY (2007) An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Dev Cell 13:177–189

    Article  CAS  PubMed  Google Scholar 

  • Gill N, Findley S, Wallling JG, Hans C, Ma J, Doyle J, Stacey G, Jackson SA (2009) Molecular and chromosomal evidence for allopolyploidy in soybean. Plant Physiol 151:1167–1174

    Article  CAS  PubMed  Google Scholar 

  • Grant D, Cregan P, Shoemaker RC (2000) Genome organization in dicots: genome duplication in Arabidopsis and synteny between soybean and Arabidopsis. Proc Natl Acad Sci USA 97:468–4173

    Article  Google Scholar 

  • Hadley HH, Hymowitz T (eds) (1973) Speciation and cytogenetics. American Society of Agronomy, Madison, WI

  • Hajduch M, Ganapathy A, Stein JW, Thelen JJ (2005) A systematic proteomic study of seed filling in soybean. Establishment of high-resolution two-dimensional reference maps, expression profiles, and an interactive proteome database. Plant Physiol 137:1397–1419

    Article  CAS  PubMed  Google Scholar 

  • Hirsch S, Aitken A, Bertsch U, Soll J (1992) A plant homologue to mammalian brain 14-3-3 protein and protein kinase C inhibitor. FEBS Lett 296:222–224

    Article  CAS  PubMed  Google Scholar 

  • Huber SC, MacKintosh C, Kaiser WM (2002) Metabolic enzymes as targets for 14-3-3 proteins. Plant Mol Biol 50:1053–1063

    Article  CAS  PubMed  Google Scholar 

  • Igarashi D, Ishida S, Fukazawa J, Takahashi Y (2001) 14-3-3 proteins regulate intracellular localization of the bZIP transcriptional activator RSG. Plant Cell 13:2483–2497

    Article  CAS  PubMed  Google Scholar 

  • Johnson C, Crowther S, Stafford M, Campbell DG, Toth R, Mackintosh C (2010) Bioinformatic and experimental survey of 14-3-3 binding sites. Biochem J. doi:10.1042/BJ20091834

  • Kersten B, Agrawal GK, Durek P, Neigenfind J, Schulze W, Walther D, Rakwal R (2009) Plant phosphoproteomics: an update. Proteomics 9:964–988

    Article  CAS  PubMed  Google Scholar 

  • Kim H-K, Jang Y-H, Baek I-S, Lee J-H, Park MJ, Chung Y-S, Chung J-I, Kim J-K (2005) Polymorphism and expression of isoflavone synthase genes from soybean cultivars. Mol Cells 19:67–73

    CAS  PubMed  Google Scholar 

  • Lapointe G, Luckevich MD, Cloutier M, Seguin A (2001) 14-3-3 gene family in hybrid poplar and its involvement in tree defence against pathogens. J Exp Bot 52:1331–1338

    Article  CAS  PubMed  Google Scholar 

  • Lu G, DeLisle AJ, de Vetten NC, Ferl RJ (1992) Brain proteins in plants: an Arabidopsis homolog to neurotransmitter pathway activators is part of a DNA binding complex. Proc Natl Acad Sci USA 89:11490–11494

    Article  CAS  PubMed  Google Scholar 

  • Lu Q, Tang X, Tian G, Wang F, Liu K, Nguyen N, Kohalmi SE, Keller WA, Tsang EWT, Harada JJ, Rothstein SJ, Cui Y (2010) Arabidopsis homolog of the yeast TREX-2 mRNA export complex: components and anchoring nucleoporin. Plant J 61:259–270

    Article  CAS  PubMed  Google Scholar 

  • MacKintosh C (2004) Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes. Biochem J 381:329–342

    Article  CAS  PubMed  Google Scholar 

  • Moore B, Perez V (1967) Specific acidic proteins of the nervous system. In: Carlson F (ed) Physiological and biochemical aspects of nervous integration. Prentice–Hall, Woods Hole, MA, pp 343–359

    Google Scholar 

  • Muslin AJ, Tanner JW, Allen PM (1996) Interaction of 14-3-3 with signalling proteins is mediated by the recognition of phosphoserine. Cell 84:889–897

    Article  CAS  PubMed  Google Scholar 

  • Obsil T, Ghirlando R, Klien DC, Ganguly S, Dyda F (2001) Crystal structure of the 14-3-3 zeta: serotonin N-acetyltransferase complex. A role for scaffolding in enzyme regulation. Cell 105:257–267

    Article  CAS  PubMed  Google Scholar 

  • Ohad N, Shichrur K, Yalovsky S (2007) The analysis of protein–protein interactions in plants by bimolecular fluorescence complementation. Plant Physiol 145:1090–1099

    Article  CAS  PubMed  Google Scholar 

  • Paul AL, Sehnke PC, Ferl RJ (2005) Isoform-specific subcellular localization among 14-3-3 proteins in Arabidopsis seems to be driven by client interactions. Mol Biol Cell 16:1735–1743

    Article  CAS  PubMed  Google Scholar 

  • Paul AL, Folta KM, Ferl RJ (2008) 14-3-3 proteins, red light and photoperiodic flowering. Plant Signal Behav 3:511–515

    Article  PubMed  Google Scholar 

  • Roberts MR (2003) 14-3-3 proteins find new partners in plant cell signalling. Trends Plant Sci 8:218–223

    Article  CAS  PubMed  Google Scholar 

  • Rosenquist M, Alsterfjord M, Larsson C, Sommarin M (2001) Data mining the Arabidopsis genome reveals fifteen 14-3-3 genes. Expression is demonstrated for two out of five novel genes. Plant Physiol 127:142–149

    Article  CAS  PubMed  Google Scholar 

  • Ryu H, Kim K, Cho H, Park J, Choe S, Hwang I (2007) Nucleocytoplasmic shuttling of BZR1 mediated by phosphorylation is essential in Arabidopsis brassinosteroid signaling. Plant Cell 19:2749–2762

    Article  CAS  PubMed  Google Scholar 

  • Schiltz S, Gallardo K, Huart M, Negroni L, Sommerer N, Burstin J (2004) Proteome reference maps of vegetative tissues in pea. An investigation of nitrogen mobilization from leaves during seed filling. Plant Physiol 135:2241–2260

    Article  CAS  PubMed  Google Scholar 

  • Schlueter JA, Dixon P, Granger C, Grant D, Clark L, Doyle JJ, Shoemaker RC (2004) Mining EST databases to resolve evolutionary events in major crop species. Genome 47:868–876

    Article  CAS  PubMed  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    Article  CAS  PubMed  Google Scholar 

  • Schoonheim PJ, Costa Pereira DD, De Boer AH (2009) Dual role for 14-3-3 proteins and ABF transcription factors in gibberellic acid and abscisic acid signalling in barley (Hordeum vulgare) aleurone cells. Plant Cell Environ 32:439–447

    Article  CAS  PubMed  Google Scholar 

  • Schwarz R, Dayhoff M (1979) Matrices for detecting distant relationships. In: Dayhoff M (ed) Atlas of protein sequences. National Biomedical Research Foundation, pp 383–358

  • Seehaus K, Tenhaken R (1998) Cloning of genes by mRNA differential display induced during the hypersensitive reaction of soybean after inoculation with Pseudomonas syringae pv. glycinea. Plant Mol Biol 38:1225–1234

    Article  CAS  PubMed  Google Scholar 

  • Sehnke PC, Henry R, Cline K, Ferl RJ (2000) Interaction of a plant 14-3-3 protein with a signal peptide of a thylakoid-targeted chloroplast precursor protein and the presence of 14-3-3 isoforms in the chloroplast stroma. Plant Physiol 122:235–242

    Article  CAS  PubMed  Google Scholar 

  • Sehnke PC, DeLille JM, Ferl RJ (2002) Consummating signal transduction: the role of 14-3-3 proteins in the completion of signal-induced transitions in protein activity. Plant Cell 14(Suppl):S339–S354

    CAS  PubMed  Google Scholar 

  • Sehnke PC, Laughner B, Cardasis H, Powell D, Ferl RJ (2006) Exposed loop domains of complexed 14-3-3 proteins contribute to structural diversity and functional specificity. Plant Physiol 140:647–660

    Article  CAS  PubMed  Google Scholar 

  • Shoemaker RC, Polzin K, Labate J, Specht J, Brummer EC, Olson T, Young N, Concibido V, Wilcox J, Tamulonis JP, Kochert G, Boerma HR (1996) Genome duplication in soybean (Glycine subgenus soja). Genetics 144:329–338

    CAS  PubMed  Google Scholar 

  • Sparkes IA, Runions J, Kearns A, Hawes C (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc 1:2019–2025

    Article  CAS  PubMed  Google Scholar 

  • Subramanian RR, Zhang H, Wang H, Ichijo H, Miyashita T, Fu H (2004) Interaction of apoptosis signal regulating kinase 1 with isoforms of 14-3-3 proteins. Exp Cell Res 294:581–591

    Article  CAS  PubMed  Google Scholar 

  • Sumioka A, Nagaishi S, Yoshida T, Lin A, Miura M, Sujuki T (2005) Role of 14-3-3 gamma in FE65-dependent gene transactivation mediated by the amyloid beta-protein precursor cytoplasmic fragment. J Biol Chem 280:42364–42374

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Trevaskis B, Maren W, Clebatch G, Udvardi M (2002) The soybean GmN6L gene encodes a late nodulin expressed in the infected zone of nitrogen-fixing nodules. Mol Plant Microbe Interact 15:630–636

    Article  CAS  PubMed  Google Scholar 

  • Uchida S, Kuma A, Ohtsubo M, Shimura M, Hirata M, Nakagama H, Matsumura T, Ishizaka Y, Yamashita K (2004) Binding of 14-3-3 beta but not 14-3-3 sigma controls the cytoplasmic localization of CDC25B: binding site preference of 14-3-3 subtypes and the subcellular localization of CDC25B. J Cell Sci 117:1411–1420

    Article  Google Scholar 

  • Walter M, Chaban C, Schütze K, Batistic O, Weckermann K, Näke C, Blazevic D, Grefen C, Schumacher K, Oecking C, Harter K, Kudla J (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40:428–438

    Article  CAS  PubMed  Google Scholar 

  • Wang CS, Vodkin LO (1994) Extraction of RNA from tissues containing high levels of procyanidins that bind RNA. Plant Mol Biol 12:132–145

    Article  CAS  Google Scholar 

  • Wobus U, Weber H (1999) Seed maturation: genetic programs and control signals. Curr Opin Plant Biol 2:33–38

    Article  CAS  PubMed  Google Scholar 

  • Wolfe KH, Gouy M, Yang YW, Sharp PM, Li WH (1989) date of the monocot–dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci USA 86:6201–6205

    Article  CAS  PubMed  Google Scholar 

  • Wurtele M, Jelich-Ottmann C, Wittinghofer A, Oecking C (2003) Structural view of a fungal toxin acting on a 14-3-3 regulatory complex. EMBO J 22:987–994

    Article  PubMed  Google Scholar 

  • Xu WF, Shi WM (2006) Expression profiling of the 14-3-3 gene family in response to salt stress and potassium and iron deficiencies in young tomato (Solanum lycopersicum) roots: analysis by real-time RT-PCR. Ann Bot (Lond) 98:965–974

    Article  CAS  Google Scholar 

  • Yaffe MB, Rittinger K, Volinia S, Caron PR, Aitken A, Leffers H, Gamblin SJ, Smerdon SJ, Cantley LC (1997) The structural basis for 14-3-3: phosphopeptide binding specificity. Cell 91:961–971

    Article  CAS  PubMed  Google Scholar 

  • Yao Y, Du Y, Jiang L, Liu JY (2007a) Interaction between ACC synthase 1 and 14-3-3 proteins in rice: a new insight. Biochemistry (Mosc) 72:1003–1007

    Article  CAS  Google Scholar 

  • Yao Y, Du Y, Jiang L, Liu JY (2007b) Molecular analysis and expression patterns of the 14-3-3 gene family from Oryza sativa. J Biochem Mol Biol 40:349–357

    CAS  PubMed  Google Scholar 

  • Yi J, Derynck MR, Li X, Telmer P, Marsolais F, Dhaubhadel S (2010) A single repeat MYB transcription factor, GmMYB176, regulates CHS8 gene expression and affects isoflavonoid biosynthesis in soybean. Plant J 62:1019–1034

    CAS  PubMed  Google Scholar 

  • Yu J, Wang J, Lin W, Li S, Li H et al (2005) The Genomes of Oryza sativa: a history of duplications. PLoS Biol 3:e38

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. Yuhai Cui (Agriculture and Agri-Food Canada, London) for BiFC vectors and Alex Molnar for assistance with the figures. This research was supported by Agriculture and Agri-Food Canada’s Abase grant to SD.

Author information

Authors and Affiliations

  1. Southern Crop Protection and Food Research Center, Agriculture and Agri-Food Canada, 1391 Sandford Street, London, ON, N5V 4T3, Canada

    Xuyan Li & Sangeeta Dhaubhadel

Authors
  1. Xuyan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sangeeta Dhaubhadel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sangeeta Dhaubhadel.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 498 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, X., Dhaubhadel, S. Soybean 14-3-3 gene family: identification and molecular characterization. Planta 233, 569–582 (2011). https://doi.org/10.1007/s00425-010-1315-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-010-1315-6

Keywords

Search

Navigation