Spatially and temporally regulated expression of the MADS-box gene AGL2 in wild-type and mutant arabidopsis flowers

Abstract

AGL2 is one of several Arabidopsis floral MADS-box genes that were isolated based on sequence similarity to the homeotic gene AGAMOUS. To investigate its possible role in flower development, we have characterized in detail the expression pattern of AGL2 in both wild-type and mutant flowers using RNA in situ hybridization. We find that AGL2 is floral-specific; it is not expressed in the inflorescence meristem. Within the floral meristem, AGL2 is first expressed very early in development, after the floral meristem has emerged from the inflorescence meristem but before any of the organ primordia emerge. The AGL2 transcript is very abundant and uniform throughout the floral meristem and in the primordia of all four floral organs: sepals, petals, stamens and carpels. Thus, AGL2 represents a new class of MADS-box genes which is expressed in all four whorls of the flower. The AGL2 transcript remains abundant in each organ during morphological differentiation, but diminishes as each organ undergoes the final maturation phase of development. AGL2 expression is high in developing ovules and, after fertilization, in developing embryos and seed coats, abating as seeds mature. In the floral organ identity mutants ag-1, ap3-3 and ap2-2, the AGL2 expression pattern is organ- and stage-dependent. These results indicate that AGL2 may play a fundamental role in the development of all floral organs, and of seeds and embryos, and that AGL2 ultimately depends upon the organ identity genes for proper expression.

This is a preview of subscription content, access via your institution.

References

  1. 1.

    Angenent GC, Busscher M, Franken J, Mol JNM, van Tunen AJ: Differential expression of two MADS box genes in wild-type and mutant petunia flowers. Plant Cell 4: 983–993 (1992).

    Article  PubMed  Google Scholar 

  2. 2.

    Angenent GC, Franken J, Busscher M, Weiss D, van Tunen AJ: Co-suppression of the petunia homeotic gene fbp2 affects the identity of the generative meristem. Plant J 5: 33–44 (1994).

    Article  PubMed  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 (1991).

    Article  PubMed  Google Scholar 

  4. 4.

    Bowman JL, Smyth DR, Meyerowitz EM: Genes directing flower development in Arabidopsis. Plant Cell 1: 37–52 (1989).

    Article  PubMed  Google Scholar 

  5. 5.

    Bowman JL, Smyth DR, Meyerowitz EM: Genetic interactions among floral homeotic genes of Arabidopsis. Development 112: 1–20 (1991).

    PubMed  Google Scholar 

  6. 6.

    Bradley D, Carpenter R, Sommer H, Hartley N, Coen E: Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell 72: 85–95 (1993).

    Article  PubMed  Google Scholar 

  7. 7.

    Christ C, Tye B-K: Functional domains of the yeast transcription/replication factor MCM1. Genes Devel 5: 751–763 (1991).

    PubMed  Google Scholar 

  8. 8.

    Coen ES: The role of homeotic genes in flower development and evolution. Annu Rev Plant Physiol Plant Mol Biol 42: 241–279 (1991).

    Article  Google Scholar 

  9. 9.

    Coen ES, Carpenter R: The metamorphosis of flowers. Plant Cell 5: 1175–1181 (1993).

    Article  PubMed  Google Scholar 

  10. 10.

    Coen ES, Meyerowitz EM: The war of the whorls: genetic interactions controlling flower development. Nature 353: 31–37 (1991).

    Article  PubMed  Google Scholar 

  11. 11.

    Dolan JW, Fields S: Cell-type-specific transcription in yeast. Biochim Biophys Acta 1088: 155–169 (1991).

    PubMed  Google Scholar 

  12. 12.

    Drews GN, Bowman JL, Meyerowitz EM: Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65: 991–1002 (1991).

    Article  PubMed  Google Scholar 

  13. 13.

    Green PB: A theory for inflorescence development and flower formation based on morphological and biophysical analysis in Echeveria. Planta 175: 153–169 (1988).

    Google Scholar 

  14. 14.

    Gustafson-Brown C, Savidge B, Yanofsky MF: Regulation of the Arabidopsis floral homeotic gene APETALA1. Cell 76: 131–143 (1994).

    Article  PubMed  Google Scholar 

  15. 15.

    Hansen G, Estruch JJ, Sommer H, Spena A: NTGLO: a tobacco homologue of the GLOBOSA floral homeotic gene of Antirrhinum majus: cDNA sequence and expression pattern. Mol Gen Genet 239: 310–312 (1993).

    PubMed  Google Scholar 

  16. 16.

    Haughn GW, Somerville CR: Genetic control of morphogenesis in Arabidopsis. Devel Genet 9: 73–89 (1988).

    Google Scholar 

  17. 17.

    Huijser P, Klein J, Lönnig W-E, Meijer H, Saedler H, Sommer H: Bracteomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box gene squamosa in Antirrhinum majus. EMBO J 11: 1239–1249 (1992).

    PubMed  Google Scholar 

  18. 18.

    Jack T, Brockman LL, Meyerowitz EM: The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68: 683–697 (1992).

    Article  PubMed  Google Scholar 

  19. 19.

    Kempin SA, Mandel MA, Yanofsky MF: Conversion of perianth into reproductive organs by ectopic expression of the tobacco floral homeotic gene NAG1. Plant Physiol 103: 1041–1046 (1993).

    Article  PubMed  Google Scholar 

  20. 20.

    Kush A, Brunelle A, Shevell D, Chua N-H: The cDNA sequence of two MADS box proteins in Petunia. Plant Physiol 102: 1051–1052 (1993).

    Article  PubMed  Google Scholar 

  21. 21.

    Lu Z-X, Wu M, Loh C-S, Yeong C-Y, Goh C-J: Nucleotide sequence of a flower-specific MADS box cDNA clone from orchid. Plant Mol Biol 23: 901–904 (1993).

    PubMed  Google Scholar 

  22. 22.

    Ma H: The unfolding drama of flower development: recent results from genetic and molecular analyses. Genes Devel 8: 745–756 (1994).

    PubMed  Google Scholar 

  23. 23.

    Ma H, Yanofsky MF, Meyerowitz EM: AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Devel 5: 484–495 (1991).

    PubMed  Google Scholar 

  24. 24.

    Mandel MA, Bowman JL, Kempin SA, Ma H, Meyerowitz H, Yanofsky ME: Manipulation of flower structure in transgenic tobacco. Cell 71: 133–143 (1992).

    Article  PubMed  Google Scholar 

  25. 25.

    Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF: Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360: 273–277 (1992).

    Article  PubMed  Google Scholar 

  26. 26.

    Mueller CGF, Nordheim A: A protein domain conserved between yeast MCM1 and human SRF directs ternary complex formation. EMBO J 10: 4219–4229 (1991).

    PubMed  Google Scholar 

  27. 27.

    Norman C, Runswick M, Pollock R, Treisman R: Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element. Cell 55: 989–1003 (1988).

    Article  PubMed  Google Scholar 

  28. 28.

    Okamuro JK, den Boer BGW, Jofuku KD: Regulation of Arabidopsis flower development. Plant Cell 5: 1183–1193 (1993).

    Article  PubMed  Google Scholar 

  29. 29.

    Passmore S, Maine GT, Elble R, Christ C, Tye B-K: Saccharomyces cerevisiae protein involved in plasmid maintenance is necessary for mating of MATα cells. J Mol Biol 204: 593–606 (1988).

    Article  PubMed  Google Scholar 

  30. 30.

    Pneuli L, Abu-Abeid M, Zamir D, Nacken W, Schwarz-Sommer Z, Lifschitz E: The MADS box gene family in tomato: temporal expression during floral development, conserved secondary structures and homology with homeotic genes from Antirrhinum and Arabidopsis. Plant J 1: 255–266 (1991).

    PubMed  Google Scholar 

  31. 31.

    Pnueli L, Hareven D, Broday L, Hurwitz C, Lifschitz E: The TM5 MADS box gene mediates organ differentiation in the three inner whorls of tomato flowers. Plant Cell 6: 175–186 (1994).

    Article  PubMed  Google Scholar 

  32. 32.

    Pnueli L, Hareven D, Rounsley SD, Yanofsky MF, Lifschitz E: Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell 6: 163–173 (1994).

    Article  PubMed  Google Scholar 

  33. 33.

    Robinson-Beers K, Pruitt RE, Gasser CS: Ovule development in wild-type Arabidopsis and two female-sterile mutants. Plant Cell 4: 1237–1249 (1992).

    Article  PubMed  Google Scholar 

  34. 34.

    Schmidt RJ, Veit B, Mandel MA, Mena M, Hake S, Yanofsky MF: Identification and molecular characterization of ZAG1, the maize homolog of the Arabidopsis floral homeotic gene AGAMOUS. Plant Cell 5: 729–737 (1993).

    Article  PubMed  Google Scholar 

  35. 35.

    Schröter H, Mueller CGF, Meese K, Nordheim A: Synergism in ternary complex formation between the dimeric glycoprotein p67SRF, polypeptide p62TCFand the c-fos serum response element. EMBO J 9: 1123–1130 (1990).

    PubMed  Google Scholar 

  36. 36.

    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 

  37. 37.

    Smyth DR, Bowman JL, Meyerowitz EM: Early flower development in Arabidopsis. Plant Cell 2: 755–767 (1990).

    Article  PubMed  Google Scholar 

  38. 38.

    Sommer H, Beltrán J-P, Huijser P, Pape H, Lönnig W-E, Saedler H, Schwarz-Sommer Z: Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. EMBO J 9: 605–613 (1990).

    PubMed  Google Scholar 

  39. 39.

    Tröbner W, Ramirez L, Motte P, Hue I, Huijser P, Lönnig W-E, Saedler H, Sommer H, Schwarz-Sommer Z: GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. EMBO J 11: 4693–4704 (1992).

    PubMed  Google Scholar 

  40. 40.

    Tsuchimoto S, van der Krol AR, Chua N-H: Ectopic expression of pMADS3 in transgenic petunia phenocopies the petunia blind mutant. Plant Cell 5: 843–853 (1993).

    Google Scholar 

  41. 41.

    van der Krol AR, Chua N-H: Flower development in petunia. Plant Cell 5: 1195–1203 (1993).

    Article  PubMed  Google Scholar 

  42. 42.

    Veit B, Schmidt RJ, Hake S, Yanofsky MF: Maize floral development: new genes and old mutants. Plant Cell 5: 1205–1215 (1993).

    Article  PubMed  Google Scholar 

  43. 43.

    Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM: LEAFY controls floral meristem identity in Arabidopsis. Cell 69: 843–859 (1992).

    Article  PubMed  Google Scholar 

  44. 44.

    Weigel D, Meyerowitz EM: Activation of floral homeotic genes in Arabidopsis. Science 261: 1723–1726 (1993).

    Google Scholar 

  45. 45.

    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).

    Article  PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Flanagan, C.A., Ma, H. Spatially and temporally regulated expression of the MADS-box gene AGL2 in wild-type and mutant arabidopsis flowers. Plant Mol Biol 26, 581–595 (1994). https://doi.org/10.1007/BF00013745

Download citation

Key words

  • arabidopsis thaliana
  • embryo
  • flower development
  • in situ hybridization
  • MADS-box
  • ovule