Skip to main content
SpringerLink
Log in

Identification and phylogenetic analysis of late embryogenesis abundant proteins family in tomato (Solanum lycopersicum)

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

Abstract

Main conclusion

This study provided a comparative genomic analysis of the LEA gene family, and these may provide valuable information for their functional investigations in the future.

Late embryogenesis abundant (LEA) proteins are a group of proteins that accumulate in response to cellular dehydration in many organisms. Here, we identified 27 LEA genes in tomato. A strong correlation between phylogeny, gene structure, and motif composition was found. The predicted SlLEA genes were non-randomly distributed within their chromosomes, and segmental and tandem duplications were probably important for their expansion. Many cis-elements potentially mediating transcription in response to abiotic stress were also found in the 1,000 bp upstream sequence of the promoter region. An additional intragenic recombination played an important role in the evolution of SlLEA genes. Selection analysis also identified some significant site-specific constraints that acted on the evolution of most LEA paralogs. Expression analysis using both microarray data and quantitative real-time PCR indicated that SlLEA genes were widely expressed in various tissues, and that a few members responded to some abiotic stresses. Our study provides useful information on the LEA genes in tomato and will facilitate their further characterization to better understand their 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

LEA:

Late embryogenesis abundant

MEME:

Multiple EM for Motif Elicitation

MRCA:

The most recent common ancestor

NJ:

Neighbor joining

qRT-PCR:

Quantitative real-time polymerase chain reaction

TSS:

Transcription start site

References

  • Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–W373

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Battaglia M, Covarrubias AA (2013) Late Embryogenesis Abundant (LEA) proteins in legumes. Front Plant Sci 4:190

    Article  PubMed Central  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  PubMed Central  CAS  PubMed  Google Scholar 

  • Cao J (2012) The pectin lyases in Arabidopsis thaliana: evolution, selection and expression profiles. PLoS One 7:e46944

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cao J, Shi F (2012) Evolution of the RALF gene family in plants: gene duplication and selection patterns. Evol Bioinform Online 8:271–292

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cao J, Huang J, Yang Y, Hu X (2011) Analyses of the oligopeptide transporter gene family in poplar and grape. BMC Genom 12:465

    Article  CAS  Google Scholar 

  • Cao J, Shi F, Liu X, Huang G, Zhou M (2012) Phylogenetic analysis and evolution of aromatic amino acid hydroxylase. FEBS Lett 584:4775–4782

    Article  Google Scholar 

  • Chen Y, Cao J (2014) Comparative genomic analysis of the Sm gene family in rice and maize. Gene 539:238–249

    Article  CAS  PubMed  Google Scholar 

  • Chen K, Durand D, Farach-Colton M (2000) NOTUNG: a program for dating gene duplications and optimizing gene family trees. J Comput Biol 7:429–447

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Hao X, Cao J (2014) Small auxin upregulated RNA (SAUR) gene family in maize: identification, evolution, and its phylogenetic comparison with Arabidopsis, rice and sorghum. J Integr Plant Biol 56:133–150

    Article  CAS  PubMed  Google Scholar 

  • Comeron JM (1999) K-Estimator: calculation of the number of nucleotide substitutions per site and the confidence intervals. Bioinformatics 15:763–764

    Article  CAS  PubMed  Google Scholar 

  • Dosztányi Z, Csizmok V, Tompa P, Simon I (2005) IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 21:3433–3434

    Article  PubMed  Google Scholar 

  • Duan J, Cai W (2012) OsLEA3-2, an abiotic stress induced gene of rice plays a key role in salt and drought tolerance. PLoS One 7:e45117

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dure L III, Greenway SC, Galau GA (1981) Developmental biochemistry of cottonseed embryogenesis and germination: changing messenger ribonucleic acid populations as shown by in vitro and in vivo protein synthesis. Biochemistry 20:4162–4168

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Garay-Arroyo A, Colmenero-Flores JM, Garciarrubio A, Covarrubias AA (2000) Highly hydrophilic proteins in prokaryotes and eukaryotes are common during conditions of water deficit. J Biol Chem 275:5668–5674

    Article  CAS  PubMed  Google Scholar 

  • Goyal K, Tisi L, Basran A, Browne J, Burnell A, Zurdo J, Tunnacliffe A (2003) Transition from natively unfolded to folded state induced by desiccation in an anhydrobiotic nematode protein. J Biol Chem 278:12977–12984

    Article  CAS  PubMed  Google Scholar 

  • Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Grelet J, Benamar A, Teyssier E, Avelange-Macherel M-H, Grunwald D, Macherel D (2005) Identification in pea seed mitochondria of a late-embryogenesis abundant protein able to protect enzymes from drying. Plant Physiol 137:157–167

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Guo R, Xu X, Carole B, Li X, Gao M, Zheng Y, Wang X (2013) Genome-wide identification, evolutionary and expression analysis of the aspartic protease gene superfamily in grape. BMC Genom 14:554

    Article  CAS  Google Scholar 

  • Hand SC, Menze MA, Toner M, Boswell L, Moore D (2011) LEA proteins during water stress: not just for plants anymore. Annu Rev Physiol 73:115–134

    Article  CAS  PubMed  Google Scholar 

  • Hara M, Terashima S, Kuboi T (2001) Characterization and cryoprotective activity of cold-responsive dehydrin from Citrus unshiu. J Plant Physiol 158:1333–1339

    Article  CAS  Google Scholar 

  • Hara M, Fujinaga M, Kuboi T (2005) Metal binding by citrus dehydrin with histidine-rich domains. J Exp Bot 56:2695–2703

    Article  CAS  PubMed  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Honjoh K, Oda Y, Takata R, Miyamoto T, Hatano S (1999) Introduction of the hiC6 gene, which encodes a homologue of a late embryogenesis abundant (LEA) protein, enhances freezing tolerance of yeast. J Plant Physiol 155:509–512

    Article  CAS  Google Scholar 

  • Houde M, Dallaire S, N’Dong D, Sarhan F (2004) Overexpression of the acidic dehydrin WCOR410 improves freezing tolerance in transgenic strawberry leaves. Plant Biotechnol J 2:381–387

    Article  CAS  PubMed  Google Scholar 

  • Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genom 9:118

    Article  Google Scholar 

  • Hurst LD (2002) The Ka/Ks ratio: diagnosing the form of sequence evolution. Trends Genet 18:486–487

    Article  PubMed  Google Scholar 

  • Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403

    Article  CAS  PubMed  Google Scholar 

  • Kong H, Landherr LL, Frohlich MW, Leebens-Mack J, Ma H, dePamphilis CW (2007) Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth. Plant J 50:873–885

    Article  CAS  PubMed  Google Scholar 

  • Kosová K, Vítámvás P, Prášil IT (2007) The role of dehydrins in plant response to cold. Biol Plant 51:601–617

    Article  Google Scholar 

  • Ku HM, Vision T, Liu J, Tanksley SD (2000) Comparing sequenced segments of the tomato and Arabidopsis genomes: large-scale duplication followed by selective gene loss creates a network of synteny. Proc Natl Acad Sci USA 97:9121–9126

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu Y, Zheng Y (2005) PM2, a group 3 LEA protein from soybean, and its 22-mer repeating region confer salt tolerance in Escherichia coli. Biochem Biophys Res Commun 331:325–332

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Zheng Y, Zhang Y, Wang W, Li R (2010) Soybean PM2 protein (LEA3) confers the tolerance of Escherichia coli and stabilization of enzyme activity under diverse stresses. Curr Microbiol 60:373–378

    Article  CAS  PubMed  Google Scholar 

  • Liu G, Xu H, Zhang L, Zheng Y (2011) Fe binding properties of two soybean (Glycine max L.) LEA4 proteins associated with antioxidant activity. Plant Cell Physiol 52:994–1002

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Wang L, Xing X, Sun L, Pan J, Kong X, Zhang M, Li D (2013) ZmLEA3, a multifunctional group 3 LEA protein from maize (Zea mays L.), is involved in biotic and abiotic stresses. Plant Cell Physiol 54:944–959

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Manfre AJ, Lanni LM, Marcotte WRJ (2006) The Arabidopsis group 1 LATE EMBRYOGENESIS ABUNDANT protein ATEM6 is required for normal seed development. Plant Physiol 140:140–149

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martin D, Rybicki E (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563

    Article  CAS  PubMed  Google Scholar 

  • Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Oliveira E, Amara I, Bellido D, Odena MA, Dominguez E, Pagès M, Goday A (2007) LC-MSMS identification of Arabidopsis thaliana heat-stable seed proteins: enriching for LEA-type proteins by acid treatment. J Mass Spectrom 42:1485–1495

    Article  CAS  PubMed  Google Scholar 

  • Olvera-Carrillo Y, Campos F, Reyes JL, Garciarrubio A, Covarrubias AA (2010) Functional analysis of the group 4 late embryogenesis abundant proteins reveals their relevance in the adaptive response during water deficit in Arabidopsis. Plant Physiol 154:373–390

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Olvera-Carrillo Y, Luis Reyes J, Covarrubias AA (2011) Late embryogenesis abundant proteins: versatile players in the plant adaptation to water limiting environments. Plant Signal Behav 6:586–589

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Padidam M, Sawyer S, Fauquet CM (1999) Possible emergence of new geminiviruses by frequent recombination. Virology 265:218–225

    Article  CAS  PubMed  Google Scholar 

  • Posada D, Crandall KA (2001) Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci USA 98:13757–13762

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Prince VE, Pickett FB (2002) Splitting pairs: the diverging fates of duplicated genes. Nat Rev Genet 3:827–837

    Article  CAS  PubMed  Google Scholar 

  • Puhakainen T, Hess MW, Mäkelä P, Svensson J, Heino P, Palva ET (2004) Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Mol Biol 54:743–753

    Article  CAS  PubMed  Google Scholar 

  • Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD (2012) The Pfam protein families database. Nucleic Acids Res 40:D290–D301

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Reyes JL, Campos F, Wei H, Arora R, Yang Y, Karlson DT, Covarrubias AA (2008) Functional dissection of hydrophilins during in vitro freeze protection. Plant Cell Environ 31:1781–1790

    Article  CAS  PubMed  Google Scholar 

  • Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37:501–506

    Article  CAS  PubMed  Google Scholar 

  • Stern A, Doron-Faigenboim A, Erez E, Martz E, Bacharach E, Pupko T (2007) Selecton 2007: advanced models for detecting positive and purifying selection using a Bayesian inference approach. Nucleic Acids Res 35:W506–W511

    Article  PubMed Central  PubMed  Google Scholar 

  • Sturn A, Quackenbush J, Trajanoski Z (2002) Genesis: cluster analysis of microarray data. Bioinformatics 18:207–208

    Article  CAS  PubMed  Google Scholar 

  • Swire-Clark GA, Marcotte WR (1999) The wheat LEA protein Em functions as an osmoprotective molecule in Saccharomyces cerevisiae. Plant Mol Biol 39:117–128

    Article  CAS  PubMed  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 Central  CAS  PubMed  Google Scholar 

  • Tolleter D, Hincha DK, Macherel D (2010) A mitochondrial late embryogenesis abundant protein stabilizes model membranes in the dry state. Biochim Biophys Acta 1798:1926–1933

    Article  CAS  PubMed  Google Scholar 

  • Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641

    Article  Google Scholar 

  • Tunnacliffe A, Wise MJ (2007) The continuing conundrum of LEA proteins. Naturwissenschaften 94:791–812

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Diehl A, Wu F, Vrebalov J, Giovannoni J, Siepel A, Tanksley SD (2008a) Sequencing and comparative analysis of a conserved syntenic segment in the Solanaceae. Genetics 180:391–408

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang Y, Zhang WZ, Song LF, Zou JJ, Su Z, Wu WH (2008b) Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol 148:1201–1211

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wolkers WF, McCready S, Brandt WF, Lindsey GG, Hoekstra FA (2001) Isolation and characterization of a D-7 LEA protein from pollen that stabilizes glasses in vitro. Biochim Biophys Acta 1544:196–206

    Article  CAS  PubMed  Google Scholar 

  • Yang Z, Nielsen R, Goldman N, Pedersen AM (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yu CS, Lin CJ, Hwang JK (2004) Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions. Protein Sci 13:1402–1406

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This project is supported by grants from the National Science Foundation of China (No. 31100923), the National Science Foundation of Jiangsu Province (BK2011467), the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD), and Jiangsu University “Youth Backbone Teacher Training Project” (2012-2016) to JC.

Conflict of interest

The authors declare that they have no competing interests.

Author information

Authors and Affiliations

  1. Institute of Life Science, Jiangsu University, Zhenjiang, 212013, Jiangsu, People’s Republic of China

    Jun Cao & Xiang Li

Authors
  1. Jun Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jun Cao.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cao, J., Li, X. Identification and phylogenetic analysis of late embryogenesis abundant proteins family in tomato (Solanum lycopersicum). Planta 241, 757–772 (2015). https://doi.org/10.1007/s00425-014-2215-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-014-2215-y

Keywords

Search

Navigation