Skip to main content

Inventory, evolution and expression profiling diversity of the LEA (late embryogenesis abundant) protein gene family in Arabidopsis thaliana

Plant Molecular Biology volume 67, pages 107–124 (2008)Cite this article

Abstract

We analyzed the Arabidopsis thaliana genome sequence to detect Late Embryogenesis Abundant (LEA) protein genes, using as reference sequences proteins related to LEAs previously described in cotton or which present similar characteristics. We selected 50 genes representing nine groups. Most of the encoded predicted proteins are small and contain repeated domains that are often specific to a unique LEA group. Comparison of these domains indicates that proteins with classical group 5 motifs are related to group 3 proteins and also gives information on the possible history of these repetitions. Chromosomal gene locations reveal that several LEA genes result from whole genome duplications (WGD) and that 14 are organized in direct tandem repeats. Expression of 45 of these genes was tested in different plant organs, as well as in response to ABA and in mutants (such as abi3, abi5, lec2 and fus3) altered in their response to ABA or in seed maturation. The results demonstrate that several so-called LEA genes are expressed in vegetative tissues in the absence of any abiotic stress, that LEA genes from the same group do not present identical expression profile and, finally, that regulation of LEA genes with apparently similar expression patterns does not systematically involve the same regulatory pathway.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

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

Abbreviations

ABA:

Abscisic acid

DAP:

Days after pollination

EST:

Expressed sequence tag

LEA:

Late embryogenesis abundant

WGD:

Whole genome duplication

References

  • Abba S, Ghignone S, Confidante P (2006) A dehydration-inducible gene in the truffle Tuber borchii identifies a novel group of dehydrins. BMC Genomics 7:39

    PubMed  Article  Google Scholar 

  • AGI (Arabidopsis Genome Initiative) (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Alsheikh MK, Heyen BJ, Randall SK (2003) Ion binding properties of the dehydrin ERD14 are dependent upon phosphorylation. J Biol Chem 278:40882–40889

    PubMed  Article  CAS  Google Scholar 

  • Altschul S, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    PubMed  Article  CAS  Google Scholar 

  • Arenas-Mena C, Raynal M, Borell A, Varoquaux F, Cutanda MC, Stacy RA, Pages M, Delseny M, Culianez-Macia FA (1999) Expression and cellular localization of Atrab28 during Arabidopsis embryogenesis. Plant Mol Biol 40:355–363

    PubMed  Article  CAS  Google Scholar 

  • Artus N, Gilmour S, Thomashow M (1991) Evidence for a cold-regulated Arabidopsis gene COR66 that is highly homologous with the cold-induced gene KIN1. Plant Physiol 96:82

    Google Scholar 

  • Bensmihen S, Rippa S, Lambert G, Jublot D, Pautot V, Granier F, Giraudat J, Parcy F (2002) The homologous ABI5 and EEL transcription factors function antagonistically to fine-tune gene expression during late embryogenesis. Plant Cell 14:1391–1403

    PubMed  Article  CAS  Google Scholar 

  • Bies N, Aspart L, Carles C, Gallois P, Delseny M (1998). Accumulation and degradation of Em proteins in Arabidopsis thaliana: evidence for post-translational controls. J Exp Bot 329:1925–1933

    Article  Google Scholar 

  • Blanc G, Wolfe KH (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16:1679–1691

    PubMed  Article  CAS  Google Scholar 

  • Blanc G, Hokamp K, Wolfe KH (2003) A recent polyploïdy superimposed on older large scale duplications in the Arabidopsis genome. Genome Res 13:137–144

    PubMed  Article  CAS  Google Scholar 

  • Borrell A, Cutanda MC, Lumbreras V, Pujal J, Goday A, Culianez-Macia FA, Pages M (2002) Arabidopsis thaliana Atrab28: a nuclear targeted protein related to germination and toxic cation tolerance. Plant Mol Biol 50:249–259

    PubMed  Article  CAS  Google Scholar 

  • Bray EA (1993) Molecular responses to water deficit. Plant Physiol 103:1035–1040

    PubMed  CAS  Google Scholar 

  • Campos F, Zamudio F, Covarrubias AA (2006) Two different late embryogenesis abundant proteins from Arabidopsis thaliana contain specific domains that inhibit Escherichia coli growth. Biochem Biophys Res Commun 342:406–413

    PubMed  Article  CAS  Google Scholar 

  • Carles C, Bies-Ethève N, Aspart L, Leon-Kloosterziel KM, Koornneef M, Echeverria M, Delseny M (2002) Regulation of Arabidopsis thaliana Em genes: role of ABI5. Plant J 30:373–383

    PubMed  Article  CAS  Google Scholar 

  • Close TJ (1996) Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiol Plant 97:795–803

    Article  CAS  Google Scholar 

  • Colmenero-Flores JM, Moreno LP, Smith CE, Covarrubias AA (1999) Pvlea-18, a member of a new Late-Embryogenesis-Abundant protein family that accumulates during water stress and in the growing regions of well-irrigated bean seedlings. Plant Physiol 120:93–104

    PubMed  Article  CAS  Google Scholar 

  • Cooke R, Raynal M, Laudié M, Grellet F, Delseny M (1996) Further progress towards a catalogue of all Arabidopsis genes: analysis of a set of 5000 non-redundant ESTs. Plant J 9:101–124

    PubMed  Article  CAS  Google Scholar 

  • Cuming A (1999) LEA proteins. In: Shewry P, Casey R (eds) Seed proteins. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 753–780

    Google Scholar 

  • Delseny M, Gaubier P, Hull G, Saez-Vasquez J, Gallois P, Raynal M, Cooke R, Grellet F (1993) Nuclear gene expressed during seed desiccation: relationship with responses to stress. In: Basra AS (ed) Stress induced gene expression. Harwood Academic Publishers, Reading, UK, pp 25–59

    Google Scholar 

  • Delseny M, Bies-Ethève N, Carles C, Hull G, Vicient C, Raynal M, Grellet F, Aspart L (2001) Late Embryogenesis abundant (LEA) protein gene regulation during Arabidopsis seed maturation. J Plant Physiol 158:419–427

    Article  CAS  Google Scholar 

  • Dure L (1993) Structural motifs in lea proteins. In: Close T, Bray EA (eds) Plant responses to cellular dehydration during environmental stress. Curr Topics Plant Physiol. American Assoc Plant Physiol, Rockville, MD, USA, pp 91–103

    Google Scholar 

  • Dure L (2001) Occurrence of a repeating 11-mer amino acid sequence motif in diverse organisms. Protein Pept Lett 8:115–122

    Article  CAS  Google Scholar 

  • Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–610

    PubMed  Article  CAS  Google Scholar 

  • Finkelstein RR, Rock C (2002) Abscisic acid biosynthesis and response. In Meyerowitz EM, Somerville CR (eds) The Arabidopsis book. http://www.aspb.org/publications/arabidopsis

  • Finkelstein R, Gampala SS, Lynch TJ, Thomas TL, Rock CD (2005) Redundant and distinct functions of the ABA response loci ABA-insensitive (ABI)5 and ABRE-binding factor (ABF)3. Plant Mol Biol 59:253–267

    PubMed  Article  CAS  Google Scholar 

  • Florea L, Hartzell G, Zhang Z, Rubin GM, Miller W (1998) A computer program for aligning a cDNA sequence with a genomic DNA sequence. Genome Res 8:967–974

    PubMed  CAS  Google Scholar 

  • Gal TZ, Glazer I, Koltai H (2004) An LEA group 3 family member is involved in survival of C. elegans during exposure to stress. FEBS Lett 577:21–26

    PubMed  Article  CAS  Google Scholar 

  • Galau GA, Hughes DW, Dure L (1986) Abscisic acid induction of cloned cotton late embryogenesis-abundant (Lea) mRNAs. Plant Mol Biol 7:155–170

    Article  CAS  Google Scholar 

  • Gaubier P, Raynal M, Hull G, Huestis GM, Grellet F, Arenas C, Pagès M, Delseny M (1993) Two different Em-like genes are expressed in Arabidopsis thaliana seeds during maturation. Mol Gen Genet 238:409–418

    PubMed  Article  CAS  Google Scholar 

  • Gilmour SJ, Artus NN, Tomashow MF (1992) cDNA sequence analysis and expression of two cold-regulated genes of Arabidopsis thaliana. Plant Mol Biol 18:13–21

    PubMed  Article  CAS  Google Scholar 

  • Gosti F, Bertauche N, Vartanian N, Giraudat J (1995) Abscisic acid-dependent and -independent regulation of gene expression by progressive drought in Arabidopsis thaliana. Mol Gen Genet 246:10–18

    PubMed  Article  CAS  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

    PubMed  Article  CAS  Google Scholar 

  • Goyal K, Pinelli C, Maslen SL, Rastogi RK, Stephens E, Tunnacliffe A (2005a) Dehydration-regulated processing of late embryogenesis abundant protein in a desiccation-tolerant nematode. FEBS Lett 579:4093–4098

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Grelet J, Benamar A, Teyssier E, Velange-Macherel MH, 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

    PubMed  Article  CAS  Google Scholar 

  • Heyen BJ, Alsheikh MK, Smith EA, Torvik CF, Seals DF, Randall SK (2002) The calcium-binding activity of a vacuole-associated, dehydrin-like protein is regulated by phosphorylation. Plant Physiol 130:675–687

    PubMed  Article  CAS  Google Scholar 

  • Hsing YI, Tsou CH, Hsu TF, Chen ZY, Hsieh KL, Hsieh JS, Chow TY (1998) Tissue and stage specific expression of a soybean (Glycine max L.) seed maturation, biotinylated protein . Plant Mol Biol 38:481–490

    PubMed  Article  CAS  Google Scholar 

  • Hughes DW, Galau GA (1991). Developmental and environmental induction of Lea and LeaA mRNAs and the postabscission program during embryo culture. Plant Cell 3:605–618

    PubMed  Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Irar SEO, Pagès M, Goday A (2006) Towards the identification of late-embryogenic-abundant phosphoproteome in Arabidopsis by 2-DE and MS. Proteomics 6:S175–S185

    PubMed  Article  Google Scholar 

  • Kamisugi YC, Cuming A (2005) The evolution of the abscisic acid-response in land plants: comparative analysis of group 1 LEA gene expression in moss and cereals. Plant Mol Biol 59:723–737

    PubMed  Article  CAS  Google Scholar 

  • Keith K, Kraml M, Dengler NG, McCourt P (1994) fusca3: a heterochronic mutation affecting late embryo development in Arabidopsis. Plant Cell 6:589–600

    PubMed  Article  CAS  Google Scholar 

  • Kim J, Shiu S-H, Thoma S, Li W-H, Patterson SE (2006) Pattern of expansion and expression divergence in the plant polygalacturonase gene family. Genome Biol 7(9):R87

    PubMed  Article  Google Scholar 

  • Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K (1994) Characterization of two cDNAs (ERD10 and ERD14) corresponding to genes that respond rapidly to dehydration stress in Arabidopsis thaliana. Plant Cell Physiol 35:225–231

    PubMed  CAS  Google Scholar 

  • Koag M-C, Fenton RD, Wilkens S, Close TJ (2003) The binding of maize DHN1 to lipid vesicles gain of structure and lipid specificity. Plant Physiol 131:309–316

    PubMed  Article  CAS  Google Scholar 

  • Kurkela S, Franck M (1990) Cloning and characterization of a cold- and ABA-inducible Arabidopsis gene. Plant Mol Biol 15(1):137

    PubMed  Article  CAS  Google Scholar 

  • Lang V, Palva ET (1993) The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 21:581–582

    PubMed  CAS  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

    PubMed  Article  CAS  Google Scholar 

  • Lopez-Molina L, Mongrand S, McLachlin DT, Chait B, Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32:317–328

    PubMed  Article  CAS  Google Scholar 

  • Luerssen H, Kirik V, Herrmann P, Misera S (1998) FUSCA3 encodes a protein with a conserved VP1/ABI3-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. Plant J 15:755–764

    PubMed  Article  CAS  Google Scholar 

  • Manfre AJ, Lanni AJ, Marcotte WR (2006) The Arabidopsis group 1 late embryogenesis abundant protein ATEM6 is required for normal seed development. Plant Physiol 140:140–149

    PubMed  Article  CAS  Google Scholar 

  • Miller JD, Arteca RN, Pell E J (1999) Senescence-associated gene expression during ozone-induced leaf senescence in Arabidopsis. Plant Physiol 120:1015–1024

    PubMed  Article  CAS  Google Scholar 

  • Mouillon JM, Gustafsson P, Harryson P (2006) Structural investigation of disordered stress proteins. Comparison of full-length dehydrins with isolated peptides of their conserved segments. Plant Physiol 141:638–650

    PubMed  Article  CAS  Google Scholar 

  • Nakamura S, Lynch TJ, Finkelstein RR (2001) Physical interactions between ABA response loci of Arabidopsis. Plant J 26:627–635

    PubMed  Article  CAS  Google Scholar 

  • Nambara E, Keith K, McCourt P, Naito S (1994) Isolation of an internal deletion mutant of the Arabidopsis thaliana ABI3 gene. Plant Cell Physiol 35:506–513

    Google Scholar 

  • Oliver M, Dowd S, Zaragoza J, Mauget S, Payton P (2004) The rehydration transcriptome of the desiccation-tolerant bryophyte Tortula ruralis: transcript classification and analysis. BMC Genomics 5:89

    PubMed  Article  Google Scholar 

  • Parcy F, Valon C, Raynal M, Gaubier-Comella P, Delseny M, Giraudat J. (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6:1567–1582

    PubMed  Article  CAS  Google Scholar 

  • Puhakainen T, Hess MW, Makela 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

    PubMed  Article  CAS  Google Scholar 

  • Quatrano RS, Bartels D, Ho THD, Pages M (1997) New insights into ABA mediated processes. Plant Cell 9:470–475

    Article  CAS  Google Scholar 

  • Raynal M, Guilleminot J, Gueguen C, Cooke R, Delseny M, Gruber V (1999) Structure, organization and expression of two closely related novel Lea (late-embryogenesis-abundant) genes in Arabidopsis thaliana. Plant Mol Biol 40:153–165

    PubMed  Article  CAS  Google Scholar 

  • Reyes JL, Rodrigo M-J, Colmenero-Flores JM, Gil J-V, Garay-Arroyo A, Campos F, Salamini F, Bartels D, Covarrubias AA (2005) Hydrophilins from distant organisms can protect enzymatic activities from water limitation effects in vitro. Plant Cell Environ 28:709–718

    Article  CAS  Google Scholar 

  • Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B (2000) Artemis: sequence visualization and annotation. Bioinformatics 16(10):944–945

    PubMed  Article  CAS  Google Scholar 

  • Soulages JL, Kim K, Arrese EL, Walters C, Cushman JC (2003) Conformation of a group 2 late embryogenesis abundant protein from soybean. Evidence of poly (l-proline)-type II structure. Plant Physiol 131:963–975

    PubMed  Article  CAS  Google Scholar 

  • Stacy RAP, Aalen RB (1998) Identification of sequence homology between the internal hydrophilic repeated motifs of Group 1 late-embryogenesis-abundant proteins in plants and hydrophilic repeats of the general stress protein GsiB of Bacillus subtilis. Planta 206:476–478

    PubMed  Article  CAS  Google Scholar 

  • Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fisscher RL, Goldberg RB, Harada JJ (2001) Leafy Cotyledon2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci USA 98:11806–11811

    PubMed  Article  CAS  Google Scholar 

  • Suzuki M, Wang HH, McCarty DR (2007) Repression of the leafy cotyledon 1/B3 regulatory network in plant embryo development by VP1/abscisic acid insensitive 3-like B3 genes. Plant Physiol 143(2):902–911

    PubMed  Article  CAS  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

    PubMed  Article  CAS  Google Scholar 

  • Thareau V, Dehais P, Serizet C, Hilson P, Rouze P, Aubourg S (2003) Automatic design of gene-specific sequence tags for genome-wide functional studies. Bioinformatics 19:2191–2198

    PubMed  Article  CAS  Google Scholar 

  • To A, Valon C, Savino G, Guilleminot J, Devic M, Giraudat J, Parcy F (2006) A network of local and redundant gene regulation governs. Plant Cell 18:1642–1651

    PubMed  Article  CAS  Google Scholar 

  • Tunnacliffe A, Wise M (2007) The continuing conundrum of the LEA proteins. Naturwissenschaften. doi 10.1007/s00114-007-0254-y

  • Tsuchiya Y, Nambara E, Naito S, McCourt P (2004) The FUS3 transcription factor functions through the epidermal regulator TTG1 during embryogenesis in Arabidopsis. Plant J 37:73–81

    PubMed  Article  CAS  Google Scholar 

  • Vicient CM, Bies-Ethève N, Delseny M (2000a) Changes in gene expression in the leafy cotyledon 1 (lec1 and fusca 3 (fus3) mutants of Arabidopsis thaliana L. J Exp Bot 51:995–1003

    PubMed  Article  CAS  Google Scholar 

  • Vicient CM, Hull G, Guilleminot J, Devic M, Delseny M (2000b) Differential expression of the Arabidopsis genes coding for Em like proteins. J Exp Bot 51:1211–1220

    PubMed  Article  CAS  Google Scholar 

  • Welin BV, Olson A, Nylander M, Palva ET (1994). Characterization and differential expression of dhn/lea/rab-like genes during cold acclimation and drought stress in Arabidopsis thaliana. Plant Mol Biol 26:131–144

    PubMed  Article  CAS  Google Scholar 

  • Wise MJ (2003). LEAping to conclusions: a computational reanalysis of late embryogenesis abundant proteins and their possible roles. BMC Bioinformatics 4:52

    PubMed  Article  Google Scholar 

  • Wise MJ, Tunnacliffe A (2004) POPP the question: what do LEA proteins do? Trends Plant Sci 9:13–17

    PubMed  Article  CAS  Google Scholar 

  • Xu D, Duan X, Wang B, Hong B, Ho T, Wu R. (1996). Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 110:249–257

    PubMed  CAS  Google Scholar 

  • Yang H, Saitou T, Komeda Y, Harada H, Kamada H (1997) Arabidopsis thaliana ECP63 encoding a LEA protein is located in chromosome 4. Gene 184:83–88

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank François Parcy for providing mutant seeds. This work was supported by the Génoplante programme and by the CNRS.

Author information

Affiliations

  1. Laboratoire Génome et Développement des Plantes, Unité Mixte de Recherche 5096 CNRS-IRD-UP, Centre National de la Recherche Scientifique, Université de Perpignan, 52, Avenue Paul Alduy, 66860, Perpignan, France

    Natacha Bies-Ethève, Pascale Gaubier-Comella, Anne Debures, Eric Lasserre, Edouard Jobet, Monique Raynal, Richard Cooke & Michel Delseny

Authors
  1. Natacha Bies-Ethève
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pascale Gaubier-Comella
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anne Debures
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eric Lasserre
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Edouard Jobet
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Monique Raynal
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Richard Cooke
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Michel Delseny
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Natacha Bies-Ethève.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Bies-Ethève, N., Gaubier-Comella, P., Debures, A. et al. Inventory, evolution and expression profiling diversity of the LEA (late embryogenesis abundant) protein gene family in Arabidopsis thaliana . Plant Mol Biol 67, 107–124 (2008). https://doi.org/10.1007/s11103-008-9304-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-008-9304-x

Keywords

  • Abiotic stresses
  • Abscisic acid
  • Arabidopsis thaliana
  • Gene expression
  • LEA
  • Seed maturation