...response: Parental conflict and infanticide during embryogenesis

Hatred and revenge as rendered in Euripides'[1xSee all References[1]classic tragedy are deeply rooted in past events. As outlined by Animesh Ray[2xNew paradigms in plant embryogenesis: maternal control comes in different flavors. Ray, A. Trends Plant Sci. 1998; 3: 325–327Abstract | Full Text | Full Text PDF | Scopus (8)See all References[2], the ability to `remember' events in the past is of great importance to cellular processes during animal and plant development. Our studies indicate that `remembering' cellular states may play an important role both in the regulation and function of the Arabidopsis gene MEDEA. Expression analysis by in situ hybridization indicates that MEDEA is expressed both before and after fertilization (J-P. Vielle-Calzada, M. Hoeppner, U. Grossniklaus, unpublished). Interestingly, post-fertilization transcription appears to be restricted to the maternally inherited MEDEA alleles, suggesting that MEDEA is regulated by genomic imprinting. Thus, the MEDEA locus `remembers' whether it was transmitted through the male or female gametophyte and this prior exposure to a specific cellular environment determines its transcriptional state during the seed's subsequent development. MEDEA encodes a SET domain protein and is similar to proteins which belong to the Polycomb and trithorax group. These do not control gene expression directly, but ensure that an active or repressed transcriptional state is remembered over many cell divisions[3xPropagating memory of transcriptional states. Paro, R. Trends Genet. 1995; 11: 295–297Abstract | Full Text PDF | PubMed | Scopus (80)See all References[3]. MEDEA may regulate cell proliferation by controlling putative target genes through the establishment of a `chromatin imprint' ensuring that the correct transcriptional state is maintained during development. Also, because MEDEA itself appears to be regulated by genomic imprinting the transcriptional state of its target genes are likely to be subject to similar maternal control.The gametophytic maternal effect of medea could be caused by a dosage effect in the endosperm. A single wild-type copy of MEDEA may be insufficient to support normal endosperm development and may ultimately result in seed abortion. This hypothesis was tested by introducing two wild-type MEDEA alleles using a tetraploid pollen donor. Seed abortion was not rescued by an additional wild-type allele in embryo and endosperm[4xMaternal control of embryogenesis by MEDEA, a Polycomb group gene in Arabidopsis. Grossniklaus, U. et al. Science. 1998; 280: 446–450Crossref | PubMed | Scopus (550)See all References[4]. However, endosperm derived from such a cross carries an equal number of mutant and wild-type alleles. It is possible that the ratio of wild-type to mutant copies is crucial and that an excess of the wild-type product is required for normal development. We have tested this hypothesis by analyzing seed abortion in tetraploid plants carrying two mutant medea alleles (U. Grossniklaus and J-P. Vielle-Calzada, unpublished). Upon self-fertilization such duplex tetraploids produce some seeds that carry endosperms with four mutant and two wild-type copies; this ratio is identical to the one obtained in a diploid out-cross using medea as the female parent. Our data suggest that these seeds develop normally if the wild-type alleles are inherited from the female parent. Thus, a distinct ratio of mutant to wild-type alleles is not required for MEDEA function because seeds with a 2:1 ratio of mutant to wild-type alleles in the endosperm develop normally in duplex tetraploids but abort in an out-cross.Several other mutants display a gametophytic maternal effect on seed development[5xThe molecular and genetic basis of ovule and megagametophyte development. Grossniklaus, U. and Schneitz, K. Semin. Cell Dev. Biol. 1998; 9: 227–238Crossref | PubMedSee all References[5], and the relationship between medea and mutants of the fie/fis class, which allow autonomous endosperm development in the absence of fertilization, is currently unknown. Genes of this class may also be regulated by genomic imprinting or they may encode components of the MEDEA pathway. Indeed, medea mutants show endosperm development after emasculation (Fig. 1Fig. 1), but the penetrance of this trait is poor and only approximately 15% of the gametophytes carrying a mutant medea allele show autonomous endosperm development. It is possible that FIE/FIS genes act in parallel with MEDEA and encode other components of the large multimeric protein complexes that are thought to be formed by proteins of the Polycomb and trithorax group. Other SET domain proteins (of which there are a multitude in the Arabidopsis genome) may also partially substitute for MEDEA; so explaining the low penetrance of this aspect of the medea phenotype. Alternatively, mutants of the fie/fis class may act upstream of MEDEA or represent target genes, some of which are expected to show parent-of-origin-specific effects.Fig. 1An ovule from an emasculated silique of a medea heterozygote. Free nuclear endosperm is produced in the absence of fertilization. Abbreviations: Ch, chalaza; Mi, micropyle; Fu, funiculus.View Large Image | Download PowerPoint SlideThe behavior of the medea mutation is consistent with the parental conflict theory on the evolution of imprinting[6xGenomic imprinting in mammalian development: a parental tug-of-war. Moore, T. and Haig, D. Trends Genet. 1991; 7: 45–49Abstract | Full Text PDF | PubMed | Scopus (693)See all References[6]. Although parental conflicts at the gene level are just coming to light in plants, it is likely that counter-acting genes that are only transcribed if inherited from the father will be discovered before too long. At that juncture it might be appropriate to remember the tragedy of Agamemnon who kills his daughter Iphigenia at Aulis[7xSee all References[7].