Abstract
The highly conserved Group 1 late embryogenesis abundant (Lea) genes are present in the genome of most plants as a gene family. Family members are conserved along the entire coding region, especially within the extremely hydrophilic internal 20 amino acid motif, which may be repeated. Cloning of Lea Group 1 genes from barley resulted in the characterization of four family members named B19.1, B19.1b, B19.3 and B19.4 after the presence of this motif 1, 1, 3 and 4 times in each gene, respectively. We present here the results of comparative and evolutionary analyses of the barley Group 1 Lea gene family (B19). The most important findings resulting from this work are (1) the tandem clustering of B19.3 and B19.4, (2) the spatial conservation of putative regulatory elements between the four B19 gene promoters, (3) the determination of the relative ‘age’ of the gene family members and (4) the ‘chimeric’ nature of B19.3 and B19.4, reflecting a cross-over or gene-conversion event in their common ancestor. We also show evidence for the presence of one or two additional expressed B19 genes in the barley genome. Based on our results, we present a model for the evolution of the family in barley, including the 20 amino acid motif. Comparisons of the relatedness between the barley family and all other known Group 1 Lea genes using maximum parsimony (PAUP) analysis provide evidence for the time of divergence between the barley genes containing the internal motif as a single copy and as a repeat. The PAUP analyses also provide evidence for independent duplications of Group 1 genes containing the internal motif as a repeat in both monocots and dicots.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Almoguera C, Jordano J: Developmental and environmental concurrent expression of sunflower dry-seed-stored low-molecular-weight heat-shock protein and Lea mRNAs. Plant Mol Biol 19: 781–792 (1992).
Baker J, Steele C, DureIII L: Sequence and characterization of 6 Lea proteins and their genes from cotton. Plant Mol Biol 11: 277–291 (1988).
Blin N, Stafford DF: A general method for isolation of high molecular weight DNA from eucaryotes. Nucl Acids Res 3: 2303–2308 (1976).
Crouch M: Regulation of gene expression during seed development in flowering plants. In: Browder LW (ed), Developmental Biology: A Comprehensive Synthesis, vol. 5, pp. 367–404. Plenum Press, New York (1988).
Calvo ES, Rodermel SR, Shoemaker RC: A third highly conserved group 1 Lea gene from Arabidopsis thaliana L. Plant Physiol 106: 787–788 (1994).
Cuming AC, Lane BG: Protein synthesis in imbibing wheat embryos. Eur J Biochem 99: 217–224 (1979).
Dickenson CD, Evans RP, Nielsen NC: RY repeats are conserved in the 5′-flanking regions of legume seed-protein genes. Nucl Acids Res 16: 371 (1988).
Espelund M, Jakobsen KS: Cloning and direct sequencing of plant promoters using primer-adapter mediated PCR on DNA coupled to a magnetic solid phase. Biotechniques 13: 74–81 (1992).
Espelund M, Sæbøe-Larssen S, Hughes DW, Galau GA, Larsen F, Jakobsen KS: Late embryogenesis-abundant genes encoding proteins with different numbers of hydrophilic repeats are regulated differentially by abscisic acid and osmotic stress. Plant J 2: 241–252 (1992).
Espelund M, Prentice Stacy RA, Jakobsen KS: A simple method for generating single-stranded DNA probes labeled to high activities. Nucl Acids Res 18: 6157–6158 (1990).
Finkelstein RR: Abscisic acid-insensitive mutations provide evidence for stage-specific signal pathways regulating expression of an Arabidopsis late embryogenesis-abundant (lea) gene. Mol Gen Genet 238: 401–408 (1993).
Futers TS, Onde S, Turet M, Cuming AC: Sequence analysis of two tandemly linked Em genes from wheat. Plant Mol Biol 23: 1067–1072 (1993).
Futcrs TS, Vaughan TJ, Sharp PJ, Cuming AC: Molecular cloning and chromosomal location of genes encoding the ‘Early-methionine-labelled’ (Em) polypeptide of Triticum aestivum L var. Chinese Spring. Theor Appl Genet 80: 43–48 (1990).
Galau GA, Hughes DW, DureIII L: Abscisic acid induction of cloned cotton late embryogenesis-abundant (Lea) mRNAs. Plant Mol Biol 7: 155–170 (1986).
Galau GA, Legocki AB, Greenway SC, DureIII L: Cotton messenger RNA sequences exist in both polyadenylated and nonpolyadenylated forms. J Biol Chem 256: 2551–2560 (1981).
Galau GA, Wang HYC, Hughes DW: Cotton Lea4 (D19) and LeaA2 (D132) group 1 Lea genes encoding water stress-related proteins containing a 20-amino acid motif. Plant Physiol 99: 783–788 (1992).
Gaubier P, Raynal M, Hull G, Huestis GM, Grellet F, Arenas C, Pages M, Delseny M: Two different Em-like genes are expressed in Arabidopsis thaliana seeds during maturation. Mol Gen Genet 238: 409–418 (1993).
Giuliano G, Pichersky E, Malik VS, Timko MP, Sednik PA, Cashmore AR: An evolutionary conserved protein binding sequence upstream of a plant light-regulated gene. Proc Natl Acad Sci USA 85: 7089–7093 (1988).
Guiltinan MJ, MarcotteJr WR, Quatrano RS: A plant leucine zipper protein that recognizes an abscisic acid response element. Science 250: 267–271 (1990).
Guthrie C, Abelson J: Organization and expression of tRNA genes in Saccharomyces cerevisae. In: Strathern JN, Jones EW, Broach JR (eds) The Molecular Biology of the Yeast Saccharomyces: Metabolism and Gene Expression, pp. 487–528. Cold Spring Harbor Press, Cold Spring Harbor, NY (1982).
Hanley BA, Schuler MA: Plant intron sequences: evidence for distinct groups of introns. Nucl Acids Res 16: 7159–7176 (1988).
Hattori T, Vasil V, Rosenkrans L, Hannah LC, McCarty DR, Vasil IK: The Viviparous-1 gene and abscisic acid activate the C1 regulatory gene for anthocyanin biosynthesis during seed maturation in maize. Genes Devel 6: 609–618 (1992).
Hollung K, Espelund M, Jakobsen KS: Another Lea B19 gene (Group 1 Lea) from barley containing a single 20 amino acid hydrophilic motif. Plant Mol Biol 25: 559–564 (1994).
Hughes DW, Galau GA: Temporally modular gene expression during cotyledon development. Genes Devel 3: 358–369 (1989).
Hughes DW, Galau GA: Developmental and environmental induction of Lea and LeaA mRNAs and the post-abscission program during embryo culture. Plant Cell 3: 605–618 (1991).
Hultman T, Ståhl S, Hornes E, Uhlèn M: Direct solid phase sequencing of genomic and plasmid DNA using magnetic beads as solid support. Nucl Acids Res 17: 4937–4946 (1989).
Jakobsen KS, Breivold E, Hornes E: Purification of mRNA directly from crude plant tissues in 15 minutes using magnetic oligo dT microspheres. Nucl Acids Res 18: 3669 (1990).
Jakobsen K, Klemsdal SS, Aalen RB, Bosnes M, Alexander D, Olsen O-A: Barley aleurone cell development: molecular cloning of aleurone-specific cDNAs from immature grains. Plant Mol Biol 12: 285–293 (1989).
Joshi CP: An inspection of the domain between putative TATA box and translation start site in 79 plant genes. Nucl Acids Res 15: 6643–6653 (1987).
Klemsdal SS, Kvaale A, Olsen O-A: Effects of the barley mutants Risø 1508 and 527 high lysine genes on the cellular development of the endosperm. Physiol Plant 67: 453–459 (1986).
Litts JC, Colwell GW, Chakerian RL, Quatrano RS: The nucleotide sequence of a cDNA clone encoding the wheat Em protein. Nucl Acids Res 15: 3607–3618 (1987).
Litts JC, Colwell GW, Chakerian RL, Quatrano RS: Sequence analysis of a functional member of the Em gene family from wheat. J DNA Sequencing Mapping 1: 263–274 (1991).
Litts JC, Erdman MB, Huang N, Karrer EE, Noueiry A, Quatrano RS, Rodrigues RL: Nucleotide sequence of the rice (Oryza sativa) Em protein gene (Empl). Plant Mol Biol 19: 335–337 (1992).
Maas C, Schaal S, Wolfgan W: A feedback control element near the transcription start site of the maize Shrunken gene determines promoter activity. EMBO J 9: 3447–3452 (1990).
McCarty DR, Hattori T, Carson CB, Vasil V, Lazar M, Vasil IK: The Viviparous-1 developmental gene of maize encodes a novel transcriptional activator. Cell 66: 395–905 (1991).
Mitchell PJ, Tjian R: Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science 245: 371–378 (1989).
Nei M: Molecular Evolutionary Genetics, pp. 293–298. Columbia University Press, NY (1987).
Nelson D, Salamini F, Bartels D: Abscisic acid promotes novel DNA-binding activity to a desiccation-related promoter of Craterostigma plantagineum. Plant J 5: 451–458 (1994).
Pichersky E: Nomad DNA: a model for movement and duplication of DNA sequences in plant genomes. Plant Mol Biol 15: 437–448 (1990).
Raynal M, Depigny D, Cooke R, Delseny M: Characterization of a radish nuclear gene expressed during late seed maturation. Plant Physiol 91: 829–836 (1989).
Ranjhan S, Litts JC, Foolad MR, Rodriguez RL: Chromosomal localization and genomic organization of α-amylase genes in rice (Oryza sativa L.). Theor Appl Genet 82: 481–488 (1991).
Rychlik W, Rhoads RE: A computer program for choosing optimal oligonucleotides for filter hybridization, sequencing and in vitro amplification of cDNA. Nucl Acids Res 17: 8543–8551 (1989).
Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).
Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).
Sutliff TD, Huang N, Litts JC, Rodriguez RL: Characterization of an α-amylase multigene cluster in rice. Plant Mol Biol 16: 579–591 (1991).
Swofford DL: Phylogenetic analysis using parsimony: program and documentation. Illinois Natural History Survey, Champaign, Urbana (1990).
Thomas TL: Gene expression during plant embryogenesis and germination: an overview. Plant Cell 5: 1401–1410 (1993).
Ulrich TU, Wurtele ES, Nikolau BJ: Sequence of EMB-1, an mRNA accumulating specifically in embryos of carrot. Nucl Acids Res 18: 2826 (1990).
Williams B, Tsang A: A maize gene expressed during embryogenesis is abscisic acid-inducible and highly conserved. Plant Mol Biol 16: 919–923 (1991).
Williams BA, Tsang A: Nucleotide sequence of an abscisic acid-responsive, embryo-specific maize gene. Plant Physiol 100: 1067–1068 (1992).
Williams ME, Foster R, Chua NH: Sequences flanking the hexameric G-box core CACGTG affect the specificity of protein binding. Plant Cell 4: 485–496 (1992).
Yamaguchi-Shinozaki K, Shinosaki K: A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low temperature, or high-salt stress. Plant Cell 6: 251–264 (1994).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Stacy, R.A.P., Espelund, M., Sæbøe-Larssen, S. et al. Evolution of the Group 1 late embryogenesis abundant (Lea) genes: analysis of the Lea B19 gene family in barley. Plant Mol Biol 28, 1039–1054 (1995). https://doi.org/10.1007/BF00032665
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00032665