503
are unusually stable during the growth phase, which takes about 2.5 weeks, with an
average half-life of ~10–14 days as compared to hours or minutes in somatic cells
(Bachvarova et al. 1985 ; Bachvarova and De Leon 1980 ; Brower et al. 1981 ). It is
after the resumption of meiosis, when a globally destabilizing environment forms,
in which many maternal mRNAs are extensively degraded (Bachvarova and De
Leon 1980 ; Su et al. 2007 ). While the bulk of maternal mRNA is eliminated by the
time the mammalian zygotic genome is fully activated (2-cell mouse embryos or
8-cell bovine embryos (Graf et al. 2014 ; Zeng and Schultz 2005 )), maternal
mRNAs are not degraded uniformly. The observed global elimination of maternal
RNA during OET is a result differential stabilization/destabilization of populations
of maternal mRNAs (Fig. 10.7).
The scale and complexity of differential control of maternal RNA stability in
vertebrates have been revealed during the last decade by high-throughput tran-
scriptome analyses using microarrays and next-generation sequencing in fish
(Mathavan et al. 2005 ; Vesterlund et al. 2011 ; Harvey et al. 2013 ; Kleppe et al.
2012 ), frog (Paranjpe et al. 2013 ; Tan et al. 2013 ), and mammals (Su et al. 2007 ;
Zeng and Schultz 2005 ; Wang et al. 2004 ; Hamatani et al. 2004 ; Zeng et al.
2004 ; Abe et al. 2015 ; Park et al. 2013 ; Xue et al. 2013 ; Yan et al. 2013 ; Deng
et al. 2014 ; Xie et al. 2010 ).
It must be stressed that poly(A)-based mRNA estimations made for OET are an
indirect measure of mRNA degradation or transcription because reversible deade-
nylation may cause false data interpretation. For example, although a slight increase
in the total amount of poly(A) RNA was observed during fertilization in mice (Piko
and Clegg 1982 ) (Fig. 10.5, left graph), it should be attributed to cytoplasmic RNA
polyadenylation as there is no transcription at that time. Thus, a conserved core of
the initial ZGA identified by single-cell poly(A) RNA sequencing (Xue et al. 2013 )
rather reflects changes in the cytoplasmic polyadenylation than true zygotic tran-
scription detected by total RNA sequencing (Abe et al. 2015 ).
10.2.2.2 “Passive” Maternal mRNA Elimination Before Meiotic
Maturation
Maternal mRNA degradation before resumption of meiosis (Phase 0) has not
received much attention in the literature. However, the mouse transcriptome
remodeling during Phase 0 has several interesting features, which justify its
specific recognition. Phase 0 occurs in an mRNA-stabilizing environment where
an average mRNA half-life is ~10–14 days (Bachvarova et al. 1985 ; Bachvarova
and De Leon 1980 ; Brower et al. 1981 ). Thus, mRNA degradation during Phase
0 involves maternal mRNAs with naturally high turnover. Such high-turnover
RNAs in fully grown oocytes might be even seen as a countdown clock turned
on when transcription ceases.
Genome-wide analysis of transcript stability in mouse fully grown oocytes identi-
fied approximately 1000 mRNAs with a half-life of <48 h (Puschendorf et al. 2006 ).
Only tens of mRNAs appeared to have a half-life of <12 h (i.e., were reduced greater
10 Clearance of Parental Products