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The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS

Abstract

The Arabidopsis homeotic gene AGAMOUS (AG) is necessary for the specification of reproductive organs (stamens and carpels) during the early steps of flower development1,2,3. AG encodes a transcription factor of the MADS-box family that is expressed in stamen and carpel primordia. At later stages of development, AG is expressed in distinct regions of the reproductive organs2,3,4,5. This suggests that AG might function during the maturation of stamens and carpels, as well as in their early development. However, the developmental processes that AG might control during organogenesis and the genes that are regulated by this factor are largely unknown. Here we show that microsporogenesis, the process leading to pollen formation, is induced by AG through activation of the SPOROCYTELESS gene (SPL, also known as NOZZLE,NZZ), a regulator of sporogenesis6,7. Furthermore, we demonstrate that SPL can induce microsporogenesis in the absence of AG function, suggesting that AG controls a specific process during organogenesis by activating another regulator that performs a subset of its functions.

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Figure 1: Activation of AG–GR rescues the ag-1 mutant phenotype.
Figure 2: AG-mediated induction of SPL through a binding site in the 3′ region of the gene.
Figure 3: Expression of SPL and AG in wild-type flowers, and expression of SPL in flowers of ag mutants and in the lines with inducible AG activity.
Figure 4: SPL is sufficient to induce microsporogenesis in the inner organs of ag-1 mutant flowers.

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Acknowledgements

We thank J. Chow for experimental help; M. Hasebe; former Meyerowitz laboratory members, J. A. Long, K. Goto, M. Frohlich and P. Kumar; and current laboratory members, especially P. Sieber, I. Negrutiu, A. Dubois, C. Ohno, C. Baker, E. Haswell, M. Heisler, V. R. Gonehal and Y. X. Zhao for comments on the manuscript. M.A-F. is indebted to IPBO and M. Van Montagu for a fellowship sponsored by Aventis CropSciences. This work was supported by a grant from the National Institutes of Health to E.M.M.

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Correspondence to Elliot M. Meyerowitz.

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Supplementary information

Supplementary Figure S1

Results of microarray analyses for selected genes. (JPG 83 kb)

Supplementary Figure S2

Real-time PCR quantitation of SPL/NZZ mRNA accumulation in response to AG-GR activation. (JPG 48 kb)

Supplementary Figure S3

The CArG box-like sequence in the 3’ region of SPL/NZZ is required for its normal expression in the integuments and the funiculus of developing ovules. (JPG 280 kb)

Supplementary Table 1

Primer and oligonucleotide sequences. (DOC 21 kb)

Supplementary Figure legends

Legends to supplementary Figs S1–S3 and Table 1 (DOC 27 kb)

Supplementary Methods

This includes a detailed description of the microarray data and additional references. (DOC 31 kb)

Supplementary Data

This includes an HTML Contents Table linking to the microarray time course, processed data and raw data files. (HTM 9 kb)

Files to Supplementary Data (ZIP 20 mb)

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Ito, T., Wellmer, F., Yu, H. et al. The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 430, 356–360 (2004). https://doi.org/10.1038/nature02733

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