Heterochromatin, small RNA and post-fertilization dysgenesis in allopolyploid and interploid hybrids of Arabidopsis

Abstract

In many plants, including Arabidopsis, hybrids between species and subspecies encounter postfertilization barriers in which hybrid seed fail to develop, or else give rise to infertile progeny. In Arabidopsis, some of these barriers are sensitive to ploidy and to the epigenetic status of donor and recipient genomes. Recently, a role has been proposed for heterochromatin in reprogramming events that occur in reproductive cells, as well as in the embryo and endosperm after fertilization. 21 nt small interfering RNA (siRNA) from activated transposable elements accumulate in pollen, and are translocated from companion vegetative cells into the sperm, while in the maturing seed 24 nt siRNA are primarily maternal in origin. Thus maternal and paternal genomes likely contribute differing small RNA to the zygote and to the endosperm. As heterochromatic sequences also differ radically between, and within, species, small RNA sequences will diverge in hybrids. If transposable elements in the seed are not targeted by small RNA from the pollen, or vice versa, this could lead to hybrid seed failure, in a mechanism reminiscent of hybrid dysgenesis in Drosophila. Heterochromatin also plays a role in apomixis and nucleolar dominance, and may utilize a similar mechanism.

Fig. 1

A model for postfertilization transposon activation in interspecific and interploid hybrids of Arabidopsis. The dosage of Arabidopsis thaliana (T) and bidopsis arenosa (A) genomes derived from diploid and tetraploid parents is indicated in pollen, egg and central cells. According to the model, the pollen grain (circle) has active transposable elements (TE) that give rise to siRNA (black hammerheads) which can inhibit complementary TE in the sperm. If 24 nt siRNA are also produced from TEs in the central cell (octagon), or from maternal somatic tissues (not shown), they may also contribute to silencing in the egg cell (dotted lines). According to this model, TEs require both 21 nt siRNA from the sperm, and 24 nt siRNA from the maternal side for silencing in the endosperm and embryo after fertilization (TE and siRNA activity is indicated by font and point size). In interspecific allotetraploid hybrids (a), sequence differences between siRNA from the A genome and TE from the T genome (and vice versa) result in TE activation in the endosperm. This effect is enhanced when diploid TT seed parents are used (b), because A. arenosa transposons are in even greater excess. In interploid A. thaliana crosses with a tetraploid seed parent (c), TE are also activated in the endosperm because of maternal TE excess relative to sperm cell siRNA. Conversely, in interploid crosses with a tetraploid pollen parent (d) TEs are activated because of paternal excess relative to maternal siRNA.