Skip to main content
Log in

Seed-specific expression patterns and regulation by ABI3 of an unusual late embryogenesis-abundant gene in sunflower

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

We cloned the genomic sequences that correspond to a previously described group 1 late embryogenesis-abundant (Lea) cDNA from sunflower: Ha ds10. The Ha ds10 G1 gene had structural and gene-expression features that depart from those of other group 1 Lea genes. An intron was present at a conserved position but showed a much larger size (1024 bp). Transcription from the Ha ds10 G1 promoter was strictly seed-specific and it originated from at least two close initiation sites. The mRNAs accumulated from stages of embryogenesis that preceded seed desiccation. Ha ds10 G1 mRNA accumulation was moderately induced, by exogenous abscisic acid treatments, in immature seeds but not induced in seedlings. We observed unprecedented changes in Lea mRNA localization associated with seed desiccation: the homogeneous tissue distribution of Ha ds10 G1 mRNAs, which was characteristic of immature embryos, evolved later in embryogenesis to an asymmetric distribution within the cotyledons, with preferential mRNA accumulation in the cells of the palisade parenchyma and provascular bundles. We also showed that, in sunflower embryos, the Ha ds10 G1 promoter could be transiently activated by the Arabidopsis ABI3 transcription factor. We discuss the significance of these results regarding hypotheses of regulation and function of plant genes from the same family.

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.

Similar content being viewed by others

References

  1. Almoguera C, Jordano J: Developmental and environmental concurrent expresion of sunflower dry-seed-stored lowmolecular-weight heat-shock protein and Lea mRNAs. Plant Mol Biol 19: 781–792(1992).

    Google Scholar 

  2. Bäumlein H, Nagy I, Villarroel R, Inzé D, Wobus U: Cisanalysis of a seed protein gene promoter: the conservative RY repeat CATGCATG within the legumin box is esential for tissue-specific expression of a legumin gene. Plant J 2: 233–239(1992).

    Article  PubMed  Google Scholar 

  3. Bobb AJ, Eiben HG, Bustos MM: PvAlf, an embryo-specific acidic transcriptional activator enhances gene expression from phaseolin and phytohemagglutinin promoters. Plant J 8: 331–343 (1995).

    Article  PubMed  Google Scholar 

  4. Bustos MM, Begum D, Kalkan FA, Battraw MJ, Hall TC: Positive and negative cis-acting DNA domains are required for spatial and temporal regulation of gene expression by a seed storage protein promoter. EMBO J 10: 1469–1479(1991).

    PubMed  Google Scholar 

  5. Chern MS, Bobb AJ, Bustos MM: The regulator of MAT2 (ROM2) protein binds to early maturation promoters and represses PvALF-activated transcription. Plant Cell 8: 305–321 (1996).

    Article  PubMed  Google Scholar 

  6. Coca MA, Almoguera C, Thomas TL, Jordano J: Differential regulation of small heat-shock genes in plants: analysis of a water-stress-inducible and developmentally activated sunflower promoter. Plant Mol Biol 31: 863–876(1996).

    PubMed  Google Scholar 

  7. Conceição AD, Krebbers E: A cotyledon regulatory region is responsible for the different spatial expression patterns of Arabidopsis 2S albumin genes. Plant J 5: 493–505(1994).

    Article  PubMed  Google Scholar 

  8. Delcasso-Tremousaygue D, Grellet F, Panabieres F, Ananiev ED, Delseny M: Structural and transcriptional characterization of the external spacer of a ribosomal mRNA nuclear gene from a higher plant. Eur J Biochem 172: 767–776(1988).

    PubMed  Google Scholar 

  9. Delseny M, Gaibier P, Hull G, Saez-Vasquez J, Gallois P, Raynal M, Cooke R, Grellet F: Nuclear Genes expressed during seed desiccation: relationship with responses to stress. In: Basra AS (ed) Stress-Induced Gene Expression in Plants, pp. 25–59. Harwood Academic Publishers, Reading, UK (1994).

    Google Scholar 

  10. Domon C, Evrard JL, Pillay DTN, Steinmetz A: A 2.6 kb intron separates the signal peptide coding sequence of an anther-specific protein from the rest of the gene in sunflower. Mol Gen Genet 229: 238–244(1991).

    PubMed  Google Scholar 

  11. Dure III L: The Lea proteins of higher plants. In: Verma DPS (ed) Control of Plant Gene Expression, pp. 325–336. CRC Press, Boca Raton, FL (1993).

    Google Scholar 

  12. Dure III L: Structural motifs in Lea proteins. In: Close TJ, Bray EA (eds) Plant Responses to Plant Dehydration During Environmental Stress, pp. 91–103. Current Topics in Plant Physiology, vol. 10, American Society of Plant Physiologists (1993).

  13. Franz G, Hatzopoulos P, Jones TJ, Kraiss M, Sung ZR: Molecular and genetic analysis of an embryonic gene, DC8, from Daicus carota L. Mol Gen Genet 218: 134–151(1989).

    Google Scholar 

  14. Gaibier P, Raynal M, Hull G, Huestis GM, Grellet F, Arenas C, Pages M, Delseny M: 2 different Em-like genes are expressed in Arabidopsis thaliana seeds during maturation. Mol Gen Genet 238: 409–418(1993).

    PubMed  Google Scholar 

  15. Giraidat J, Haige BM, Valon C, Smalle J, Parcy F, Goodman HM: Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4: 1251–1261(1992).

    Article  PubMed  Google Scholar 

  16. Giraidat J, Parcy F, Bertaiche N, Gosti F, Leung J, Morris PC, Bouvierdurand M, Vartanian N: Current advances in abscisic acid action and signalling. Plant Mol Biol 26: 1557–1577 (1995).

    Google Scholar 

  17. Guiltinan MJ, Marcotte, WR, Quatrano RS: A plant leucine zipper protein that recognizes an abscisic acid response element. Science 250: 267–271(1990).

    PubMed  Google Scholar 

  18. Hattori T, Terada T, Hamasuna S: Regulation of the Osem gene by abscisic acid and the transcriptional activator VP1: analysis of cis-acting promoter elements required for regulation by abscisic acid and VP1. Plant J 7: 913–925(1995).

    Article  PubMed  Google Scholar 

  19. Hughes DW, Galai GA: Temporally modular gene expression during cotyledon development. Genes Dev 3: 358–369(1989).

    PubMed  Google Scholar 

  20. Imai R, Chang L, Ohta A, Bray EA, Takagi M: A lea-class gene of tomato confers salt and freezing tolerance when expressed in Saccharomyces cerevisiae. Gene 170: 243–248 (1996).

    PubMed  Google Scholar 

  21. Jefferson RA, Kavanagh TA, and Bevan MW: GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901–3907(1987).

    PubMed  Google Scholar 

  22. Kosugi S, Ohashi Y, Nakajima K, Arai Y: An improved assay for β-glucuronidase in transformed cells: methanol almost completely suppressed a putative endogenous β-glucuronidase activity. Plant Sci 70: 133–140(1990).

    Article  Google Scholar 

  23. 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: 895–905(1991).

    Article  PubMed  Google Scholar 

  24. Molinier J: Expression spatio-temporelle de l'hélianthinine dans l'embryon zygotique de tournesol (Helianthus anuus L.). Diplome d'Etude Approfondies de Biologie Céllulaire et Moléculaire, Université Louis Pasteur, Strasbourg (1995).

  25. Ow DW, Wood KV, DeLuca M, de Wet JR, Helinski DR, Howell SH: Transient and stable expression of the firefly luciferase gene in plant cells and transgenic plants. Science 234: 856–859(1986).

    Google Scholar 

  26. Parcy F, Valon C, Raynal M, Gaibier-Comella P, Delseny M, Giraidat J: Regulation of gene expression programs during arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6: 1567–1582(1995).

    Google Scholar 

  27. Phillips J, Artsaenko O, Fiedler U, Horstmann C, Mock HP, Muntz K, Conrad U: Seed-specific immunomodulation of abscisic acid activity induces a developmental switch. EMBO J 16: 4489–4496(1997).

    PubMed  Google Scholar 

  28. Roberts JK, DeSimone NA, Lingle WL, Dure L III: Cellular concentrations and uniformity of cell-type accumulation of two Lea proteins in cotton embryos. Plant Cell 5: 769–780 (1993).

    PubMed  Google Scholar 

  29. Sambrook J, Fritsch FF, Maniatis T: Molecular Cloning A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1989).

    Google Scholar 

  30. Simpson GG, Filipowicz W: Splicing of precursors to mRNA in higher plants: mechanism, regulation and sub-nuclear organisation of the spliceosomal machinery. Plant Mol Biol 32: 1–41(1996).

    PubMed  Google Scholar 

  31. Stacy RAP, Espelund M, Larsen SS, Hollung K, Helliesen E, Jakobsen KS: Evolution of the group 1 late embryogenesis abundant (lea) genes: analyses of the lea B19 gene family in barley. Plant Mol Biol 28: 1039–1054(1995).

    PubMed  Google Scholar 

  32. Thomas TL, Chung HJ, Nunberg AN: ABA signaling in plant development and growth. In: Aducci P (ed) Signal Transduction in Plants, pp. 23–43. Birkhäuser Verlag, Basel (1997).

    Google Scholar 

  33. Williams B, Tsang A: A maize gene expressed during embryogenesis is abscisic acid-inducible and highly conserved. Plant Mol Biol 16: 919–923(1991).

    PubMed  Google Scholar 

  34. Wurtele ES, Wang HQ, Durgerian S, Nikolai BJ, Ulrich TH: Characterization of a gene that is expressed early in somatic embryogenesis of Daicus carota. Plant Physiol 102: 303–312 (1993).

    PubMed  Google Scholar 

  35. Xu DP, Duan XL, Wang BY, Hong BM, Ho THD, Wu R: 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(1996).

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Prieto-Dapena, P., Almoguera, C., Rojas, A. et al. Seed-specific expression patterns and regulation by ABI3 of an unusual late embryogenesis-abundant gene in sunflower. Plant Mol Biol 39, 615–627 (1999). https://doi.org/10.1023/A:1006178220289

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006178220289

Navigation