Sex-biased lethality or transmission of defective transcription machinery in Arabidopsis.

Unlike animals, whose gametes are direct products of meiosis, plant meiotic products undergo additional rounds of mitosis, developing into multicellular haploid gametophytes that produce egg or sperm cells. The complex development of gametophytes requires extensive expression of the genome, with DNA-dependent RNA polymerases I, II, and III being the key enzymes for nuclear gene expression. We show that loss-of-function mutations in genes encoding key subunits of RNA polymerases I, II, or III are not transmitted maternally due to the failure of female megaspores to complete the three rounds of mitosis required for the development of mature gametophytes. However, male microspores bearing defective polymerase alleles develop into mature gametophytes (pollen) that germinate, grow pollen tubes, fertilize wild-type female gametophytes, and transmit the mutant genes to the next generation at moderate frequency. These results indicate that female gametophytes are autonomous with regard to gene expression, relying on transcription machinery encoded by their haploid nuclei. By contrast, male gametophytes make extensive use of transcription machinery that is synthesized by the diploid parent plant (sporophyte) and persists in mature pollen. As a result, the expected stringent selection against nonfunctional essential genes in the haploid state occurs in the female lineage but is relaxed in the male lineage.

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