More than DNA methylation: does pleiotropy drive the complex pattern of evolution of Dnmt1?

DNA methylation is an important chromatin modification that can stably
alter gene expression in cells and maintain genome integrity in plants and
vertebrates. The function of DNA methylation outside of these well-studied
systems, however, is unclear. Insects, in particular, represent an
understudied group. Variation in the level of DNA methylation and gains
and losses in the maintenance methyltransferase, DNMT1, across the insect
tree of life suggests that there is much we don’t understand about DMNT1
function and evolution. One constant across the studies examining patterns
of Dnmt1 expression in insects is that expression is consistently high in
reproductive tissues compared to somatic tissue. The explanation for this
has been that DNMT1 is required in tissues that have high levels of cell
division. Our previous study found that downregulation of Dnmt1 expression
in the milkweed bug Oncopeltus fasciatus results in the expected reduction
of DNA methylation, no global changes in gene expression reflecting
changes in DNA methylation, and the loss of the ability to produce viable
oocytes. Here, we show that females treated with ds-Dnmt1 RNA during
larval development have a more extreme phenotype; they lack oocytes
entirely but develop a normal somatic ovary. Our results indicate a
specific role for DNMT1 in the formation of gametes and are consistent
with data from other systems, including Tribolium castaneum, a species
does not have DNA methylation. We propose that DNMT1 has multiple
functional roles in addition to methylating DNA, which explains its
complex patterns of evolution.