Plant Molecular Biology

, Volume 38, Issue 6, pp 1147–1160 | Cite as

CaMADS1, a MADS box gene expressed in the carpel of hazelnut

  • D. Rigola
  • M.E. Pè
  • C. Fabrizio
  • G. Mè
  • M. Sari-Gorla
Article

Abstract

Hazelnut (Corylus avellana L.) is a species of economic interest that shows a peculiar floral biology. Unlike most of the angiosperms, which produce ovules during floral development such that they are ready for pollen at anthesis, hazelnut ovary development is delayed and triggered by compatible pollination. In order to elucidate the mechanisms regulating this unusual process and the role of the MADS box genes in ovary development, a cDNA library from pollinated styles of hazelnut was screened with a mixture of MADS box genes from different plant species. CaMADS1 (Corylus avellana MADS box), a floral-specific MADS box gene, was isolated, and characterized as belonging to the sub-family of the AGAMOUS genes. Northern blot, RT-PCR analyses and in situ hybridization experiments show a precise correlation between ovary development and CaMADS1 expression, indicating a role of this MADS box gene in the processes of floral organogenesis.

hazelnut Corylus avellana MADS box genes flower development ovule AGAMOUS 

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References

  1. 1.
    Angenent GC, Franken J, Busscher M, van Dijken A, van Went JL, van Tunen AJ: A novel class of MADS box genes is involved in ovule development in Petunia. Plant Cell 7: 1569–1582 (1995).Google Scholar
  2. 2.
    Bahloul M, Burkard G: An improved method for the isolation of total RNA from spruce tissues. Plant Mol Biol Rep 11: 212–215 (1993).Google Scholar
  3. 3.
    Bowman JL, Drews GN. Meyerowitz EM: Expression of the Arabidopsis floral homeotic gene AGAMOUS is restricted to specific cell types late in flower development. Plant Cell 3: 749–758 (1993).Google Scholar
  4. 4.
    Cañas LA, Busscher M, Angenent GC, Beltran JP, van Tunen AJ: Nuclear localization of the petunia MADS box protein FBP11. Plant J 6: 597–604 (1994).Google Scholar
  5. 5.
    Chung YY, Kim SR, Finkel D, Yanofsky MF, An G: Early flowering and reduced apical dominance result from ectopic expression of a rice MADS-box gene. Plant Mol Biol 26: 657–665 (1994).Google Scholar
  6. 6.
    Chung YY, Kim SR, Kang HG, Noh YS, Park MC, Finkel D, An G: Characterization of two rice MADS-box genes homologous to GLOBOSA. Plant Sci 109: 45–56 (1995).Google Scholar
  7. 7.
    Coen ES, Meyerowitz EM: The war of the whorls: genetic interaction controlling flower development. Nature 353: 31–37 (1991).Google Scholar
  8. 8.
    Colombo L, Franken J, Koetje E, van Went J, Dons HJM, Angenent GC, van Tunen AJ: The Petunia MADS box gene FBP11 determines ovule identity. Plant Cell 7: 1859–1868 (1995).Google Scholar
  9. 9.
    Dayhoff MO: Atlas of Protein Sequences and Structure, vol 5 Supplement 3. National Biomedical Research Foundation, Washington, DC (1979).Google Scholar
  10. 10.
    Drews GN, Bowman JL, Meyerowitz EM: Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65: 991–1002 (1991).Google Scholar
  11. 11.
    Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQJ, Gerentes D, Perez P, Smyth DR: AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8: 155–168 (1996).Google Scholar
  12. 12.
    Evans PT, Malmberg RL: Alternative pathways of tobacco placental development: time and commitment and analysis of a mutant. Devel Biol 136: 273–283 (1989).Google Scholar
  13. 13.
    Fischer A, Baum N, Saedler H, Theissen G: Chromosomal mapping of the MADS-box multigene family in Zea mays reveals dispersed distribution of allelic genes as well as transposed copies. Nucl Acids Res 23: 1901–1911 (1995).Google Scholar
  14. 14.
    Flanagan CA, Hu Y, Ma H: Specific expression of the AGL1 MADS box gene suggests regulatory function in Arabidopsis gynoecium and ovule development. Plant J 10: 343–353 (1996).Google Scholar
  15. 15.
    Germain E: The reproduction of hazelnut (Corylus avellana L.): a review. Acta Hort 351: 195–203 (1994).Google Scholar
  16. 16.
    Greco R, Stagi L, Colombo L, Angenent GC, Sari-Gorla M, Pé ME: MADS box genes expressed in developing inflorescences of rice and sorghum. Mol Gen Genet 253: 615–623 (1997).Google Scholar
  17. 17.
    Irish VF, Yamamoto YT: Conservation of floral homeotic gene function between Arabidopsis and Antirrhinum. Plant Cell 7: 1635–1644 (1995).Google Scholar
  18. 18.
    Johansen DA: Plant Microtechnique. McGraw-Hill, New York, pp. 80–82 (1940).Google Scholar
  19. 19.
    Klucher KM, Chow H, Reiser L, Fischer RL: The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8: 137–153 (1996).Google Scholar
  20. 20.
    Lu ZX, Wu M, Loh CS, Yeong CY, Goh CJ: Nucleotide sequence of a flower-specific MADS-box cDNA clone from orchid. Plant Mol Biol 23: 901–904 (1993).Google Scholar
  21. 21.
    Ma H: The unfolding drama of flower development: recent results from genetic and molecular analyses. Genes Devel 8: 745–756 (1994).Google Scholar
  22. 22.
    Ma H, Yanofsky MF, Meyerowitz M: AGL1–AGL6, an Arabidopsis gene family with similarity to flower homeotic and transcription factors genes. Genes Devel 5: 484–495 (1991).Google Scholar
  23. 23.
    Mandel MA, Bowman JL, Kempin SA, Ma H, Meyerowitz EM, Yanofsky M: Manipulation of flower structure in transgenic tobacco. Cell 71: 133–143 (1992).Google Scholar
  24. 24.
    Modrusan Z, Reiser L, Feldmann KA, Fisher RL, Haughn GW: Homeotic transformation of ovules into carpel-like structures in Arabidopsis. Plant Cell 6: 333–349 (1994).Google Scholar
  25. 25.
    Munster T, Pahnke J, Di Rosa A, Kim JT, Martin W, Saedler H, Theissen G: Floral homeotic genes were recruited from homologous MADS-box genes pre-existing in the common ancestor of fern and seed plants. Proc Natl Acad Sci USA 94: 2415–2420 (1997).Google Scholar
  26. 26.
    Nadeau JA, Sheng Zhangs S, Li J, O'Neill SD: Ovule development: Identification of stage-specific and tissue-specific cDNAs. Plant Cell 8: 213–239 (1996).Google Scholar
  27. 27.
    Reiser L, Modrusan Z, Margossian L, Samach A, Ohad N, Haughn GW, Fischer RL: The BELL1 gene encodes a homeodomain protein involved in pattern formation in the Arabidopsis ovule primordium. Cell 83: 735–742 (1995).Google Scholar
  28. 28.
    Rigola D, Pè ME, Sari-Gorla M: A cDNA clone from hazelnut (Corylus avellana L.) encoding a low molecular weight heat shock protein expressed in the reproductive structures. Sex Plant Reprod 11: 29–30 (1998).Google Scholar
  29. 29.
    Robinson-Beers K, Pruitt RE, Gasser CS: Ovule development in wild-type Arabidopsis and two female-sterile mutants. Plant Cell 4: 1237–1249 (1992).Google Scholar
  30. 30.
    Sadvige B, Rounsley D, Yanofsky MF: Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. Plant Cell 7: 721–733 (1995).Google Scholar
  31. 31.
    Saitou N, Nei M: The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425 (1987).Google Scholar
  32. 32.
    Schmidt RJ, Veit B, Mandel MA, Mena m, Hake S, Yanofsky MF: Identification and molecular characterization of ZAG1, the maize homologue of the Arabidopsis floral homeotic gene AGAMOUS. Plant Cell 5: 729–737 (1993).Google Scholar
  33. 33.
    Schwarz-Sommer Z, Huijser P, Nacken W, Saedler H, Sommer H: Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 250: 931–936 (1990).Google Scholar
  34. 34.
    Shore P, Sharrocks AD: The MADS-box family of transcription factor. Eur J Biochem 229: 1–13 (1995).Google Scholar
  35. 35.
    Sieburth LE, Meyerowitz ME: Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically. Plant Cell 9: 355–365 (1997).Google Scholar
  36. 36.
    Tandre K, Albert VA, Sundas A, Engstrom P: Conifer homologues to gene that control flower development in angiosperm. Plant Mol Biol 27: 69–78 (1995).Google Scholar
  37. 37.
    Theissen G, Kim JT, Saedler H: Classification and phylogeny of the MADS box multigene family suggest defined roles of the MADS box gene subfamilies in the morphological evolution of eukariotes. J Mol Evol 43: 484–516 (1996).Google Scholar
  38. 38.
    Theissen G, Saedler H: MADS-box genes in plant ontogeny and phylogeny: Haeckel's ‘biogenetic low’ revisited. Curr Opin Genet Devel 5: 628–639 (1995).Google Scholar
  39. 39.
    Thompson MM: Growth and development of the pistillate flower and nut in ‘Barcellona’ filbert. J Am Soc Hort Sci 104: 427–432 (1979).Google Scholar
  40. 40.
    van Tunen AJ, Koes RE, Spelt CE, van der Krol AR, Mol JNM: Cloning of the two chalcone flavonone isomerase genes from Petunia hybrida co-ordinate light regulated and differential expression of flavonoid genes. EMBO J 7: 1257–1263 (1988).Google Scholar
  41. 41.
    Weigel D, Meyerowitz EM: The ABCs of floral homeotic genes. Cell 78: 203–209 (1994).Google Scholar
  42. 42.
    Weigel D: The genetic of flower development: from floral induction to ovule morphogenesis. Annu Rev Genet 29: 19–39 (1995).Google Scholar
  43. 43.
    Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM: The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346: 35–39 (1990).Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • D. Rigola
    • 1
  • M.E. Pè
    • 1
  • C. Fabrizio
    • 1
  • G. Mè
    • 2
  • M. Sari-Gorla
    • 1
  1. 1.Department of Genetics and MicrobiologyUniversity of MilanoMilanoItaly
  2. 2.Departmento di Colture ArboreeUniversity of TorinoTorinoItaly

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