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Molecular Mechanisms of Gamete Formation in Plants

Gametogenesis, in most sexual flowering plants, is initiated from a single surviving gametic cell, known as the functional megaspore, which is formed after meiosis of the somatically derived megaspore mother cell. Certain wild type sexual species and also mutants present more than 1 megaspore mother cell, however only 1 of these undergoes gametogenesis, as twin female gametophytes are never observed. In addition, many species are known to be able to form gametes without meiosis through a process named apomixis. These observations have lead to the hypothesis that somatic cells in the ovule are competent to respond to a local signal that determines whether meiotic gametogenesis will take place. Olmedo-Monfil et al have recently reported in the journal Nature (Nature., 464, 628-632) the identification of such a signal able to control female gamete formation in Arabidopsis. The authors demonstrated that the Arabidopsis protein ARGONAUTE 9 (AGO9) restricts the specification of gametophyte precursors in a dosage-dependent, noncell autonomous manner. Mutations in AGO9 lead to abnormal somatic cells that were able to differentiate into gametic cells and initiate gametogenesis without undergoing meiosis. AGO9 was preferentially expressed in cytoplasmic foci of reproductive somatic companion cells but neither in the associated male or female gametes nor in their precursors. In addition, mutations in the putative RNA binding protein supressor of gene silencing 3 (SGS3) and in the RNA-dependent RNA polymerase 6, which are essential for trans-acting siRNAs to move as signal molecules and cause gene silencing beyond their cellular sites of initiation, also lead to Arabidopsis defects identical to those of AGO9 mutants. Finally, the authors showed that AGO9 preferentially interacts with a 24-nucleotide small RNA derived from transposable elements, silencing their activity in female gametophyte. In sum, the work presented by Olmedo-Monfil et al demonstrates that the function of AGO9 is reminiscent of the PIWI subclass of ARGONAUTE proteins that are known to be necessary to maintain transposon silencing in the germ line of invertebrates and mammals. Moreover, their results show that the AGO9 expressed in the reproductive companion cells is critical to specify cell fate in the Arabidopsis ovule through small RNA silencing.