Epigenetic Control of Animal Development - Building the Most Complex Structure on Earth - page 133

divisions are exclusively controlled and regulated by epigenetic factors parentally
(there is evidence that the paternal cytoplasmic factors are also involved in early
embryonic development along the maternal factors) provided to gametes.
Depending on the species, zygotic genome activation (ZGA) occurs some-
time between the two-cell stage and the gastrulation. It is interesting to note that in
Drosophila , ZGA starts with the expression of intronless genes ( De Renzis et al.,
2007 ), which is likely unavoidable given the fact that the mechanisms for eliminat-
ing introns through gene splicing are not established yet. Some maternal products are
supplied in insufficient quantities, and this is the reason for starting the expression of
relevant zygotic genes ( Wieschaus, 1996 ).
Live-bearing, viviparous animals also deposit cytoplasmic factors in their gametes, but
their role in development is less important and lasts for shorter periods than oviparous
animals. This is evolutionarily plausible: the mother can, and does, control the devel-
opment by transplacentally supplying epigenetic factors to the embryo for the whole in
utero life (embryonic and fetal). In mice, for example, 90% of maternal transcripts are
degraded by the two-cell stage. A weak, “minor,” ZGA may occur before the cleavage,
primarily in the sperm pronucleus ( Aoki et al., 1997 ), but the relatively small number
of transcripts are translated only in the two-cell stage ( Hamatani et al., 2004 ) when the
“major” ZGA begins ( Latham et al., 1991 ). Although the embryonic genome in a mam-
mal like the mouse is activated as early as the first cleavage, the maternally provided
mRNAs and proteins persist until the eight-cell stage ( Hamatani et al., 2004 ), suggesting
that they may play some role in early development until that point in time (and possibly
even later). Recall that even the activation of the zygotic genome and initial patterns of
gene expression are determined by maternal transcriptional factors.
In Drosophila , the almost exclusive epigenetic control of development via cyto-
plasmic factors persists until the 13th division cycle (i.e., with formation of the syn-
citial blastoderm and the end of cleavage divisions). Repression of zygotic genes
is associated with condensed zygotic chromatin, as well as hypoacetylation and
methylation of the histone H3 ( Meehan et al., 2005 ). Zygotic genes are generally
repressed until the 13th cell cycle, and are associated with condensed, hypoacety-
lated, and H3-methylated chromatin (Meehan et al., 2005).
At the blastoderm stage, the Drosophila embryo has 8192 cells. It is estimated
that the majority of the approximately 20,000 transcriptional units in Drosophila
must be provided maternally (Wieschaus, 1996). However, by the 14th division cycle
in Drosophila , 33% of maternal factors go down significantly, and part of the zygotic
transcription is intended to compensate for the loss of maternal mRNAs/proteins
( De Renzis et al., 2007 ). Such facts led biologists to the conclusion that “[g]enes
that must be supplied zygotically represent only a small fraction of the Drosophila
genome” (Wieschaus, 1996).
The Mid-Blastula or Maternal-Embryonic Transition
In many oviparous animals, after formation of morula, which occurs sometime
during the blastula stage, the embryo begins a large-scale expression of zygotic