Bypassing genomic imprinting allows seed development

Abstract

In developing progeny of mammals the two parental genomes are differentially expressed according to imprinting marks, and embryos with only a uniparental genetic contribution die [1][2][3] . Gene expression that is dependent on the parent of origin has also been observed in the offspring of flowering plants, and mutations in the imprinting machinery lead to embryonic lethality, primarily affecting the development of the endosperm-a structure in the seed that nourishes the embryo, analogous to the function of the mammalian placenta 4 . Here we have generated Arabidopsis thaliana seeds in which the endosperm is of uniparental, that is, maternal, origin. We demonstrate that imprinting in developing seeds can be bypassed and viable albeit smaller seedlings can develop from seeds lacking a paternal contribution to the endosperm. Bypassing is only possible if the mother is mutant for any of the FIS-class genes, which encode Polycomb group chromatinmodifying factors. Thus, these data provide functional evidence that the action of the FIS complex balances the contribution of the paternal genome. As flowering plants have evolved a special reproduction system with a parallel fusion of two female with two male gametes, our findings support the hypothesis that only with the evolution of double fertilization did the action of the FIS genes become a requirement for seed development. Furthermore, our data argue for a gametophytic origin of endosperm in flowering plants, thereby supporting a hypothesis raised in 1900 by Eduard Strasburger.Flowering plants (angiosperms) have evolved to be one of the predominant life forms on earth with more than 250,000 extant species. An important feature, and probably one of the main reasons for this evolutionary success, is the development of an embryo along with a second fertilization product, the endosperm. The endosperm is usually triploid because a homo-diploid female central cell fuses with one of the male gametes. The exact genome dosage of typically two maternal and one paternal genomes seems to be crucial for endosperm development. Raising the maternal contribution in the endosperm has been found to result in smaller seeds comprising fewer endosperm cells and smaller embryos. In contrast, increasing the paternal input results in larger seeds [5][6][7] . These results have been interpreted in light of the parental conflict theory (kinship theory) according to which mothers and fathers have a different interest in allocation of resources to their offspring 8,9 . Hence, it has been proposed that paternal genes promote seed growth, whereas maternal genes rather reduce growth; or, conversely, that in the maternal genome growth promoting factors are inactivated.Indeed, flowering plants have been found to imprint certain genes during endosperm development, which is similar to the situation observed for the placenta of mammals [10][11][12][13][14] . Interestingly, the imprinting machinery seems to regulate itself [15][16][17] . Imprinting involves the recognition of methylated DNA and histone...

Mechanisms and evolution of genomic imprinting in plants

“…Developmental defects are associated with increased expression of PHE1 and many other genes in the endosperm (Kang et al, 2008;Kö hler et al, 2003b;Erilova et al, 2009), suggesting that the main function of the FIS PcG complex is to suppress dosage sensitive genes in the endosperm. Support for this idea stems from experiments showing that fis mutants can form viable seeds if a sexually derived fis embryo is supported by an autonomously developing diploid endosperm (Nowack et al, 2007). This can be achieved by fertilizing fis mutants with single sperm cell containing pollen of the cdka;1 mutant that preferentially fertilizes the egg cell (Nowack et al, 2006).…”

“…Lack of FIS function causes autonomous endosperm development and the formation of seed-like structures without viable embryos (Chaudhury et al, 1997). However, sexually derived embryos surrounded by a diploid autonomous fis endosperm develop into viable seeds (Nowack et al, 2007), suggesting that developmental aberrations in fis mutant endosperm are caused by increased expression of dosage sensitive genes and reducing genome dose by bypassing fertilization can restore viable seed formation.…”

“…After this logic, many imprinted genes are likely to have an endosperm-constrained function, or, alternatively, they have no functional role in the endosperm and are on the trajectory to convert to pseudogenes (Figure 2). Although there are exceptions (for example, PHE1 and HDG3 (Kö hler et al, 2005;Gehring et al, 2009)), the majority of imprinted genes is likely to be maternally active and paternally silenced, imposing a strong maternal control over endosperm development, as it could be predicted based on the hypothesis that the endosperm is an extension of the maternal gametophytic life phase (Nowack et al, 2007). To conclude, both hypotheses, the 'defense hypothesis' as well as 'kinship theory' together can explain the origin of genomic imprinting in the endosperm; whereas the first hypothesis explains how imprinting originates, the latter explains how imprinting will be manifested and maintained.…”

Networks controlling seed size in Arabidopsis

“…The failure of 111 karyogamy in the central cell has been shown to impair 112 endosperm development causing seed abortion (Aw et al 113 2010). Interestingly, viable seeds can also be produced in 114 the presence of homoparental diploid, as opposed to trip-115 loid, endosperm (Nowack et al 2006(Nowack et al , 2007. In cdka;1 116 mutants, pollen fertilizes only the egg cell, not the central 117 cell due to karyogamy failure (Aw et al 2010).…”

Cell wall invertase as a regulator in determining sequential development of endosperm and embryo through glucose signaling early in seed development

“…8,9 Such a developmental sequence is of great importance for proper seed development. There is compelling evidence that the endosperm drives seed and embryo growth, 10,11 and controls seed size in a range of species.…”