Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte

Abstract

Haploid spores of plants divide mitotically to form multicellular gametophytes. The female spore (megaspore) of most flowering plants develops by means of a well-defined programme into the mature megagametophyte consisting of the egg apparatus and a central cell1,2. We investigated the role of the Arabidopsis retinoblastoma3,4 protein homologue and its function as a negative regulator of cell proliferation during megagametophyte development. Here we show that three mutant alleles of the gene for the Arabidopsis retinoblastoma-related protein, RBR1 (ref. 4), are gametophytic lethal. In heterozygous plants 50% of the ovules are aborted when the mutant allele is maternally inherited. The mature unfertilized mutant megagametophyte fails to arrest mitosis and undergoes excessive nuclear proliferation in the embryo sac. Supernumerary nuclei are present at the micropylar end of the megagametophyte, which develops into the egg apparatus and central cell. The central cell nucleus, which gives rise to the endosperm after fertilization, initiates autonomous endosperm development reminiscent of fertilization-independent seed (fis) mutants5. Thus, RBR1 has a novel and previously unrecognized function in cell cycle control during gametogenesis and in the repression of autonomous endosperm development.

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Figure 1: Arabidopsis rbr1 mutant alleles induce ovule abortion and proliferation of nuclei in the egg apparatus.
Figure 2: The rbr1-1 mutant initiates a fertilization-independent endosperm and affects embryo and pollen development.
Figure 3: RBR1 is expressed in the female gametophyte and at different stages of flower development.

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Acknowledgements

We are grateful to M. Collinge, J. Fütterer, U. Grossniklaus, M. Hanin and L. Hennig for discussions and critical reading of the manuscript. We thank J. Wyrzykowska and A. Johnston for help with in situ hybridization and ovule clearings. We also thank the Salk Institute Genomic Analysis Laboratory for providing the sequence-indexed Arabidopsis T-DNA insertion mutants and ABRC for providing us with seeds. This work was supported by funding from the Swiss National Science Foundation to W.G.

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Correspondence to Wilhelm Gruissem.

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Ebel, C., Mariconti, L. & Gruissem, W. Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte. Nature 429, 776–780 (2004). https://doi.org/10.1038/nature02637

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