Molecular Biology Reports

, Volume 43, Issue 4, pp 221–228 | Cite as

A LEA 4 protein up-regulated by ABA is involved in drought response in maize roots

  • Jesús Alejandro Zamora-Briseño
  • Estela Sánchez de Jiménez
Rapid Communication


Late embryogenesis abundant (LEA) proteins are hydrophilic proteins that accumulate to high concentrations during the late stages of seeds development, which are integral to desiccation tolerance. LEA proteins also play a protective role under other abiotic stresses. We analyzed in silico a maize protein predicted to be highly hydrophilic and intrinsically disordered. This prediction was experimentally corroborated by solubility assays under denaturing conditions. Based on its amino acid sequence, we propose that this protein belongs to group four of the LEA proteins. The accumulation pattern of this protein was similar to that of dehydrins during the desiccation process that takes place during seed development. This protein was induced by exogenous abscisic acid in immature embryos, but during imbibition was down-regulated by gibberellins. It was also induced in maize roots under osmotic stress. So far, this is the first member of the LEA proteins belonging to group four to be characterized in maize, and it plays a role in the response to osmotic stress.


LEA 4 proteins Desiccation Disordered protein 



J.-A. Zamora was the recipient of a Conacyt fellowship (no. 512028419). We thank Dr. Rosario Muñoz-Clares for her invaluable comments. This research was supported partially by Conacyt Grant 213872 and PAIP Grant FQ747, UNAM.

Author contribution statement

ZB and SQ conceived and designed research. ZB conducted experiments. ZB and SQ wrote the manuscript. All authors read and approved the manuscript.

Supplementary material (248 kb)
Supplementary material 1 (PS 247 kb)


  1. 1.
    Agrawal GK, Thelen JJ (2009) A high-resolution two dimensional Gel and Pro-Q DPS-based proteomic workflow for phosphoprotein identification and quantitative profiling. Methods Mol Biol 527(9):3–10CrossRefPubMedGoogle Scholar
  2. 2.
    Amara I, Odena A, Oliveira E, Moreno A, Masmoudi K, Pagès M, Goday A (2012) Insights into maize LEA proteins: from proteomics to functional approaches. Plant Cell Physiol 53(2):312–329CrossRefPubMedGoogle Scholar
  3. 3.
    Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428Google Scholar
  4. 4.
    Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias AA (2008) The Enigmatic LEA Proteins and Other Hydrophilins. Plant Physiol 148(1):6–24CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Bies N, Aspart L, Carles C, Gallois P, Delseny M (1998) Accumulation and degradation of Em proteins in Arabidopsis thaliana: evidence for post-transcriptional controls. J Exp Bot 49(329):1925–1933Google Scholar
  6. 6.
    Bies-Ethève N, Gaubier-Comella P, Debures A, Lasserre E, Jobet E, Raynal M, Cooke R, Delseny M (2008) Inventory, evolution and expression profiling diversity of the Lea (late embryogenesis abundant) protein gene family in Arabidopsis thaliana. Plant Mol Biol 67(1–2):107–124CrossRefPubMedGoogle Scholar
  7. 7.
    Boudet J, Buitink J, Hoekstra FA, Rogniaux H, Larré C, Satour P, Leprince O (2006) Comparative analysis of the heat stable proteome of radicles of Medicago truncatula seeds during germination identifies late embryogenesis abundant proteins associated with desiccation tolerance. Plant Physiol 140(4):1418–1436CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Campos F, Guillén G, Reyes JL, Covarrubias AA (2011) A general method of protein purification for recombinant unstructured non-acidic proteins. Protein Expr Purif 80(1):47–51CrossRefPubMedGoogle Scholar
  9. 9.
    Chakrabortee S, Meersman F, Kaminski Schierle GS, Bertoncini CW, McGee B, Kaminski CF, Tunnacliffe A (2010) Catalytic and chaperone-like functions in an intrinsically disordered protein associated with desiccation tolerance. Proc Natl Acad Sci USA 107(37):16084–16089CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Costantini S, Colonna G, Facchiano AM (2006) Amino acid propensities for secondary structures are influenced by the protein structural class. Biochem Biophys Res Commun 342:441–445CrossRefPubMedGoogle Scholar
  11. 11.
    Dalal M, Tayal D, Chinnusamy V, Bansal KC (2009) Abiotic stress and ABA-inducible group 4 LEA from Brassica napus plays a key role in salt and drought tolerance. J Biotechnol 139(2):137–145CrossRefPubMedGoogle Scholar
  12. 12.
    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(9):e45117CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Dure L III, Crouch M, Harada J, Ho THD, Mundy J, Quatrano RS, Thomas T, Sung ZR (1989) Common amino acid sequence domains among the LEA proteins of higher plants. Plant Mol Biol 12(5):475–486CrossRefPubMedGoogle Scholar
  14. 14.
    Dure L (1993) Structural motifs in LEA proteins. In: Close TJ, Bray EA (eds) Plant responses to cellular dehydration during environmental stress. American Society of Plant Physiologists, Rockville, pp 91–103Google Scholar
  15. 15.
    Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer ELL, Tate J, Punta M (2014) The Pfam protein families database. Nucleic Acids Res 42:222–230CrossRefGoogle Scholar
  16. 16.
    Galau GA, Bijaisoradat N, Huges DW (1987) Accumulation kinetics of cotton late embryogenesis abundant mRNAs and storage protein mRNAs: coordinate regulation during embryogenesis and the role of abscisic acid. Dev Biol 123(1):198–212CrossRefPubMedGoogle Scholar
  17. 17.
    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(8):5668–5674CrossRefPubMedGoogle Scholar
  18. 18.
    Grelet J, Benamar A, Teyssier E, Avelange-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(1):157–167CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Gu H, Jia Y, Wang X, Chen Q, Shi S, Ma L, Zhang J, Zhang H, Ma H (2012) Identification and characterization of a LEA family gene CarLEA4 from chickpea (Cicer arietinum L.). Mol Biol Rep 39(4):3565–3572CrossRefPubMedGoogle Scholar
  20. 20.
    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(1):115–134CrossRefPubMedGoogle Scholar
  21. 21.
    Hu T, Zeng H, He S, Wu Y, Wang G, Huang X (2012) Molecular analysis of OsLEA 4 and its contributions to improve E. coli viability. Appl Biochem Biotechnol 166:222–233CrossRefPubMedGoogle Scholar
  22. 22.
    Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157(1):105–132CrossRefPubMedGoogle Scholar
  23. 23.
    Manfre AJ, LaHatte GA, Climer CR, Marcotte WR (2009) Seed dehydration and the establishment of desiccation tolerance during seed maturation is altered in the Arabidopsis thaliana mutant atem6-1. Plant Cell Physiol 50(2):243–253CrossRefPubMedGoogle Scholar
  24. 24.
    Nylander M., Svensson J, Palva ET, Welin BV (2001) Stress-induced accumulation and tissue-specific localization of dehydrins in Arabidopsis thaliana. Plant Mol Biol 45:263–279CrossRefPubMedGoogle Scholar
  25. 25.
    Oliveira E, Amara I, Bellido D, Odena MA, Dominguez E, Pages M, Goday A (2007) LCMSMS Identification of Arabidopsis thaliana heat-stable seed proteins: enriching for LEA-type proteins by acid treatment. J Mass Spectrom 42:1485–1495CrossRefPubMedGoogle Scholar
  26. 26.
    Olvera-Carrillo Y, Campos F, Reyes J, Garciarrubio A, Covarrubias A (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(1):373–390CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Park S, Kim Y, Jeong JC et al (2011) Sweetpotato late embryogenesis abundant 14 (IbLEA14) gene influences lignification and increases osmotic- and salt stress-tolerance of transgenic calli. Planta 233(3):621–634CrossRefPubMedGoogle Scholar
  28. 28.
    Ritchie, SW, Hanway JJ, Benson, Go (1992) How a corn plant develops. Special Report No. 48 Iowa State University, Cooperative Extension Service, Ames, IA,
  29. 29.
    Roberts JK, DeSimone NA, Lingle WL, Dure L III (1993) Cellular concentrations and uniformity of cell-type accumulation of two LEA proteins in cotton embryos. Plant Cell 5:769–780CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Simossis VA1, Heringa J (2005) PRALINE: a multiple sequence alignment toolbox that integrates homology-extended and secondary structure information. Nucleic Acids Res. 33:W289–94Google Scholar
  31. 31.
    Shih MD, Lin SC, Hsieh JS, Tsou Ch, Chow TY, Lin T, Hsing YI (2004) Gene cloning and characterization of a soybean (Glycine max L.) LEA protein, GmPM16. Plant Mol Biol 56(5):689–703CrossRefPubMedGoogle Scholar
  32. 32.
    Shih MD, Hsieh TY, Lin TP, Hsing YI, Hoekstra FA (2010) Characterization of two soybean (Glycine max L.) LEA IV proteins by circular dichroism and Fourier transform infrared spectrometry. Plant Cell Physiol 51(3):395–407CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Sun X, Rikkerink EHA, Jones WT, Uversky VN (2013) Multifarious roles of intrinsic disorder in proteins illustrate its broad impact on plant biology. Plant Cell 25(1):38–55CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Thomann EB, Sollinger J, White C, Rivin CJ (1992) Accumulation of group 3 late embryogenesis abundant proteins in Zea mays embryos. Roles of abscisic acid and the viviparous-1 gene product. Plant Physiol 99(2):607–614CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Tompa P (2002) Intrinsically unstructured proteins. Trends Biochem Sci 27(10):527–533CrossRefPubMedGoogle Scholar
  36. 36.
    Wang M, Li P, Li C, Pan Y, Jiang X, Zhu D, Zhao Q, Yu J (2014) SiLEA14, a novel atypical LEA protein, confers abiotic stress resistance in foxtail millet. BMC Plant Biol 14(1):290CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Wise MJ, Tunnaclife A (2004) POPP The question: what do LEA proteins do. Naturwissenschaften 9(1):13–17Google Scholar
  38. 38.
    Wise MJ (2003) LEAping to conlusions: a computational reanalysis of late embryogenesis abundant proteins and their possible roles. BMC Bioinform 4(1):52CrossRefGoogle Scholar
  39. 39.
    Xue B, DunBrack RL, Wiliams RW, Dunker AJ, Uversky VN (2010) PONDR-Fit: a meta-predictor of intrinsically disordered amino acids. Biochim Biophys Acta 4:996–1101CrossRefGoogle Scholar
  40. 40.
    Zegzouti H, Jones B, Marty C, Lelievre JM, Latche A, Pech JC, Bouzayen M (1997) ER5, a tomato cDNA encoding an ethylene-responsive LEA-like protein: characterization and expression in response to drought, ABA and wounding. Plant Mol Biol 35(1):847–885CrossRefPubMedGoogle Scholar
  41. 41.
    Zhang Y, Li Y, Lai J, Zhang H, Liu Y, Liang L, Xie Q (2012) Ectopic expression of a LEA protein gene TsLEA1 from Thellungiella salsuginea confers salt-tolerance in yeast and Arabidopsis. Mol Biol Rep 39(4):4627–4633CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Laboratorio 103, Departamento de Bioquímica, Facultad de QuímicaUniversidad Nacional Autónoma de MéxicoMéxicoMexico

Personalised recommendations