Skip to main content
Log in

Genome-wide identification and analysis of late embryogenesis abundant (LEA) genes in Prunus mume

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Late embryogenesis abundant (LEA) proteins play important roles in plant desiccation tolerance. In this study, 30 LEA genes were identified from Chinese plum (Prunus mume) through genome-wide analysis. The PmLEA genes are distributed on all Chinese plum chromosomes except chromosome 3. Twelve (40 %) and five PmLEA genes are arranged in tandem and segmental duplications, respectively. The PmLEA genes could be divided into eight groups (LEA_1, LEA_2, LEA_3, LEA_4, LEA_5, PvLEA18, dehydrin and seed maturation protein). Ten gene conversion events were observed and most of them (70 %) were identified in dehydrin group. Most PmLEA genes were highly expressed in flower (22/30) and up-regulated by ABA treatment (19/30).

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

Similar content being viewed by others

References

  1. Dure LI, Galau GA (1981) Developmental biochemistry of cottonseed embryogenesis and germination XIII. Regulation of biosynthesis of principal storage proteins. Plant Physiol 68(1):187–194

    Article  PubMed  CAS  Google Scholar 

  2. Monteiro Costa CdN, Santa Brigida AB, BdN Borges, de Menezes Neto MA, Castelo Branco Carvalho LJ, Batista de Souza CR (2011) Levels of MeLEA3, a cDNA sequence coding for an atypical late embryogenesis abundant protein in Cassava, increase under in vitro salt stress treatment. Plant Mol Biol Rep 29(4):997–1005. doi:10.1007/s11105-011-0292-7

    Article  Google Scholar 

  3. Olvera-Carrillo Y, Campos F, Luis Reyes J, 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(1):373–390. doi:10.1104/pp.110.158964

    Article  PubMed  CAS  Google Scholar 

  4. George S, Usha B, Parida A (2009) Isolation and characterization of an atypical LEA protein coding cDNA and its promoter from drought-tolerant plant Prosopis juliflora. Appl Biochem Biotechnol 157(2):244–253. doi:10.1007/s12010-008-8398-6

    Article  PubMed  CAS  Google Scholar 

  5. 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):137–145. doi:10.1016/j.jbiotec.2008.09.014

    Article  PubMed  CAS  Google Scholar 

  6. Borovskii GB, Stupnikova IV, Antipina AI, Vladimirova SV, Voinikov VK (2002) Accumulation of dehydrin-like proteins in the mitochondria of cereals in response to cold, freezing, drought and ABA treatment. BMC Plant Biol 2:5. doi:10.1186/1471-2229-2-5

    Article  PubMed  Google Scholar 

  7. Oztur ZN, Talame V, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N, Tuberosa R, Bohnert HJ (2002) Monitoring large-scale changes in transcript abundance in drought- and salt-stressed barley. Plant Mol Biol 48(5–6):551–573. doi:10.1023/a:1014875215580

    Article  PubMed  Google Scholar 

  8. Stacy RA, 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(3):476–478. doi:10.1007/s004250050424

    Article  PubMed  CAS  Google Scholar 

  9. Denekamp NY, Reinhardt R, Kube M, Lubzens E (2010) Late Embryogenesis Abundant (LEA) proteins in nondesiccated, encysted, and diapausing embryos of rotifers. Biol Reprod 82(4):714–724. doi:10.1095/biolreprod.109.081091

    Article  PubMed  CAS  Google Scholar 

  10. Warner AH, Miroshnychenko O, Kozarova A, Vacratsis PO, MacRae TH, Kim J, Clegg JS (2010) Evidence for multiple group 1 late embryogenesis abundant proteins in encysted embryos of Artemia and their organelles. J Biochem 148(5):581–592. doi:10.1093/jb/mvq091

    Article  PubMed  CAS  Google Scholar 

  11. Wu G, Zhang H, Sun J, Liu F, Ge X, Chen W-H, Yu J, Wang W (2011) Diverse LEA (late embryogenesis abundant) and LEA-like genes and their responses to hypersaline stress in post-diapause embryonic development of Artemia franciscana. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology 160(1):32–39. doi:10.1016/j.cbpb.2011.05.005

    Article  CAS  Google Scholar 

  12. Boswell LC, Menze MA, Hand SC (2009) Multiple isoforms of late embryogenesis abundant proteins in Artemia franciscana embryos. Integr Comp Biol 49:E203

    Google Scholar 

  13. Dure L, Crouch M, Harada J, Ho T-HD, Mundy J, Quatrano R, Thomas T, Sung ZR (1989) Common amino acid sequence domains among the LEA proteins of higher plants. Plant Mol Biol 12(5):475–486

    Article  CAS  Google Scholar 

  14. Hunault G, Jaspard E (2010) LEAPdb: a database for the late embryogenesis abundant proteins. Bmc Genomics 11. doi:10.1186/1471-2164-11-221

  15. He S, Tan L, Hu Z, Chen G, Wang G, Hu T (2011) Molecular characterization and functional analysis by heterologous expression in E. coli under diverse abiotic stresses for OsLEA5, the atypical hydrophobic LEA protein from Oryza sativa L. Mol Genet Genomics 287(1):39–54. doi:10.1007/s00438-011-0660-x

    Article  PubMed  Google Scholar 

  16. Park S-C, Kim Y-H, Jeong JC, Kim CY, Lee H-S, Bang J-W, Kwak S–S (2011) Sweetpotato late embryogenesis abundant 14 (IbLEA14) gene influences lignification and increases osmotic- and salt stress-tolerance of transgenic calli. Planta 233(3):621–634. doi:10.1007/s00425-010-1326-3

    Article  PubMed  CAS  Google Scholar 

  17. Wang L, Li X, Chen S, Liu G (2009) Enhanced drought tolerance in transgenic Leymus chinensis plants with constitutively expressed wheat TaLEA (3). Biotechnol Lett 31(2):313–319. doi:10.1007/s10529-008-9864-5

    Article  PubMed  CAS  Google Scholar 

  18. Angel Jimenez J, Alonso-Ramirez A, Nicolas C (2008) Two cDNA clones (FsDhn1 and FsClo1) up-regulated by ABA are involved in drought responses in Fasus sylvatica L seeds. J Plant Physiol 165(17):1798–1807. doi:10.1016/j.jplph.2007.11.013

    Article  Google Scholar 

  19. Zhao P, Liu F, Ma M, Gong J, Wang Q, Jia P, Zheng G, Liu H (2011) Overexpression of AtLEA3-3 confers resistance to cold stress in Escherichia coli and provides enhanced osmotic stress tolerance and ABA sensitivity in Arabidopsis thaliana. Mol Biol 45(5):785–796. doi:10.1134/s0026893311050165

    Article  CAS  Google Scholar 

  20. Hundertmark M, Popova AV, Rausch S, Seckler R, Hincha DK (2011) Influence of drying on the secondary structure of intrinsically disordered and globular proteins. Biochem Biophys Res Commun 417(1):122–128. doi:10.1016/j.bbrc.2011.11.067

    Article  PubMed  Google Scholar 

  21. Furuki T, Shimizu T, Kikawada T, Okuda T, Sakurai M (2011) Salt effects on the structural and thermodynamic properties of a group 3 lea protein model peptide. Biochemistry 50(33):7093–7103. doi:10.1021/bi200719s

    Article  PubMed  CAS  Google Scholar 

  22. Hand SC, Menze MA, Toner M, Boswell L, Moore D (2011) LEA proteins during water stress: not just for plants anymore. In: Annual review of physiology, vol 73, pp 115–134. doi:10.1146/annurev-physiol-012110-142203

  23. Hundertmark M, Dimova R, Lengefeld J, Seckler R, Hincha DK (2011) The intrinsically disordered late embryogenesis abundant protein LEA18 from Arabidopsis thaliana modulates membrane stability through binding and folding. Biochim Et Biophys Acta Biomembr 1:446–453. doi:10.1016/j.bbamem.2010.09.010

    Article  Google Scholar 

  24. 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(4):586–589

    Article  PubMed  CAS  Google Scholar 

  25. Bassett CL, Wisniewski ME, Artlip TS, Richart G, Norelli JL, Farrell RE Jr (2009) Comparative expression and transcript initiation of three peach dehydrin genes. Planta 230(1):107–118. doi:10.1007/s00425-009-0927-1

    Article  PubMed  CAS  Google Scholar 

  26. Wisniewski M, Bassett C, Artlip T, Renaut J, Farrell R (2005) Differential patterns of expression and regulation of two dehydrin genes from peach (Prunus persica) bark tissues. HortScience 40(4):1036

    Google Scholar 

  27. Wisniewski ME, Bassett CL, Renaut J, Farrell R, Tworkoskii T, Artlip TS (2006) Differential regulation of two dehydrin genes from peach (Prunus persica) by photoperiod, low temperature and water deficit. Tree Physiol 26(5):575–584

    Article  PubMed  CAS  Google Scholar 

  28. Swarbreck D, Wilks C, Lamesch P, Berardini TZ, Garcia-Hernandez M, Foerster H, Li D, Meyer T, Muller R, Ploetz L, Radenbaugh A, Singh S, Swing V, Tissier C, Zhang P, Huala E (2008) The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Res 36:D1009–D1014. doi:10.1093/nar/gkm965

    Article  PubMed  CAS  Google Scholar 

  29. Altschul SF, Madden TL, Schaffer 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(17):3389–3402. doi:10.1093/nar/25.17.3389

    Article  PubMed  CAS  Google Scholar 

  30. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer ELL, Eddy SR, Bateman A (2010) The Pfam protein families database. Nucleic Acids Res 38:D211–D222. doi:10.1093/nar/gkp985

    Article  PubMed  CAS  Google Scholar 

  31. McDowall J, Hunter S (2011) InterPro protein classification. Methods Mol Biol (Clifton) 694:37–47

    Article  CAS  Google Scholar 

  32. Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31(13):3784–3788. doi:10.1093/nar/gkg563

    Article  PubMed  CAS  Google Scholar 

  33. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP SignalP and related tools. Nat Protoc 2(4):953–971. doi:10.1038/nprot.2007.131

    Article  PubMed  CAS  Google Scholar 

  34. Guo A-Y, Zhu Q-H, Chen X, Luo J-C (2007) GSDS: a gene structure display server. Yi chuan 29(8):1023–1026

    Article  PubMed  CAS  Google Scholar 

  35. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 20. Bioinformatics 23(21):2947–2948. doi:10.1093/bioinformatics/btm404

    Article  PubMed  CAS  Google Scholar 

  36. Huson DH, Richter DC, Rausch C, Dezulian T, Franz M, Rupp R (2007) Dendroscope: an interactive viewer for large phylogenetic trees. Bmc Bioinformatics 8. doi:10.1186/1471-2105-8-460

  37. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208. doi:10.1093/nar/gkp335

    Article  PubMed  CAS  Google Scholar 

  38. Maher C, Stein L, Ware D (2006) Evolution of Arabidopsis microRNA families through duplication events. Genome Res 16(4):510–519. doi:10.1101/gr.4680506

    Article  PubMed  CAS  Google Scholar 

  39. Tang H, Wang X, Bowers JE, Ming R, Alam M, Paterson AH (2008) Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Res 18(12):1944–1954. doi:10.1101/gr.080978.108

    Article  PubMed  CAS  Google Scholar 

  40. Tang H, Bowers JE, Wang X, Ming R, Alam M, Paterson AH (2008) Synteny and collinearity in plant genomes. Science 320(5875):486–488. doi:10.1126/science.1153917

    Article  PubMed  CAS  Google Scholar 

  41. Sawyer S (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6(5):526–538

    PubMed  CAS  Google Scholar 

  42. Liu JH, Ban Y, Wen X-P, Nakajima I, Moriguchi T (2009) Molecular cloning and expression analysis of an arginine decarboxylase gene from peach (Prunus persica). Gene 429:10–17

    Article  PubMed  CAS  Google Scholar 

  43. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3(6):1101–1108

    Article  PubMed  CAS  Google Scholar 

  44. Higo K, Ugawa Y, Iwamoto M, Higo H (1998) PLACE: a database of plant cis-acting regulatory DNA elements. Nucleic Acids Res 26(1):358–359. doi:10.1093/nar/26.1.358

    Article  PubMed  CAS  Google Scholar 

  45. Prestridge DS (1991) SIGNAL SCAN: a computer program that scans DNA sequences for eukaryotic transcriptional elements. Comput Appl Biosci 7(2):203–206

    PubMed  CAS  Google Scholar 

  46. Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias AA (2008) The enigmatic LEA proteins and other hydrophilins. Plant Physiol 148(1):6–24. doi:10.1104/pp.108.120725

    Article  PubMed  CAS  Google Scholar 

  47. Shih M-D, Hoekstra FA, Hsing YIC (2008) Late embryogenesis abundant proteins. Advances in botanical research. Academic Press, London, pp 21–225. doi:10.1016/s0065-2296(08)00404-7

    Google Scholar 

  48. Zhao P, Liu F, Zheng G, Liu H (2011) Group 3 late embryogenesis abundant protein in Arabidopsis: structure, regulation, and function. Acta Physiologiae Plantarum 33(4):1063–1073. doi:10.1007/s11738-010-0678-4

    Article  CAS  Google Scholar 

  49. Roychoudhury A, Sengupta DN (2009) The promoter-elements of some abiotic stress-inducible genes from cereals interact with a nuclear protein from tobacco. Biol Plant 53(3):583–587. doi:10.1007/s10535-009-0106-z

    Article  CAS  Google Scholar 

  50. Kim J-S, Mizoi J, Yoshida T, Fujita Y, Nakajima J, Ohori T, Todaka D, Nakashima K, Hirayama T, Shinozaki K, Yamaguchi-Shinozaki K (2011) An ABRE promoter sequence is involved in osmotic stress-responsive expression of the DREB2A Gene, which encodes a transcription factor regulating drought-inducible genes in Arabidopsis. Plant Cell Physiol 52(12):2136–2146. doi:10.1093/pcp/pcr143

    Article  PubMed  CAS  Google Scholar 

  51. Wang XS, Zhu HB, Jin GL, Liu HL, Wu WR, Zhu J (2007) Genome-scale identification and analysis of LEA genes in rice (Oryza sativa L.). Plant Sci 172(2):414–420. doi:10.1016/j.plantsci.2006.10.004

    Article  CAS  Google Scholar 

  52. Hundertmark M, Hincha DK (2008) LEA (Late Embryogenesis Abundant) proteins and their encoding genes in Arabidopsis thaliana. Bmc Genomics 9. doi:10.1186/1471-2164-9-118

  53. Bies-Etheve 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):107–124. doi:10.1007/s11103-008-9304-x

    Article  PubMed  CAS  Google Scholar 

  54. Bassett CL, Dardick C, Gasic K, Wisniewski ME, Fisher K (2010) The peach dehydrin family is small relative to all other sequenced plant genomes. HortScience 45(8):S120–S121

    Google Scholar 

  55. Yamane H, Kashiwa Y, Kakehi E, Yonemori K, Mori H, Hayashi K, Iwamoto K, Tao R, Kataoka I (2006) Differential expression of dehydrin in flower buds of two Japanese apricot cultivars requiring different chilling requirements for bud break. Tree Physiol 26(12):1559–1563

    Article  PubMed  CAS  Google Scholar 

  56. Duarte JM, Cui LY, Wall PK, Zhang Q, Zhang XH, Leebens-Mack J, Ma H, Altman N, dePamphilis CW (2006) Expression pattern shifts following duplication indicative of subfunctionalization and neofunctionalization in regulatory genes of Arabidopsis. Mol Biol Evol 23(2):469–478. doi:10.1093/molbev/msj051

    Article  PubMed  CAS  Google Scholar 

  57. Li Z, Zhang H, Ge S, Gu X, Gao G, Luo J (2009) Expression pattern divergence of duplicated genes in rice. Bmc Bioinformatics 10. doi:10.1186/1471-2105-10-s6-s8

  58. Osada N, Innan H (2008) Duplication and gene conversion in the Drosophila melanogaster genome. Plos Genet 4(12). doi:10.1371/journal.pgen.1000305

  59. Stacy RA, Espelund M, Saeboe-Larssen S, Hollung K, Helliesen E, Jakobsen KS (1995) Evolution of the group 1 late embryogenesis abundant (Lea) genes: analysis of the Lea B19 gene family in barley. Plant Mol Biol 28(6):1039–1054. doi:10.1007/bf00032665

    Article  PubMed  CAS  Google Scholar 

  60. Jun J, Si-hai Y, Da-cheng T (2007) Patterns of positive selection and gene conversion in the complete disease resistance genes of rice. Scientia Agricultura Sinica 40(9):1856–1863

    CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by Ministry of Science and Technology (Grant No. 2011AA100207) and the State Forestry Administration of China (Grant No. 201004012).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Qixiang Zhang.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Du, D., Zhang, Q., Cheng, T. et al. Genome-wide identification and analysis of late embryogenesis abundant (LEA) genes in Prunus mume . Mol Biol Rep 40, 1937–1946 (2013). https://doi.org/10.1007/s11033-012-2250-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-012-2250-3

Keywords

Navigation