3. The integrative landscape of rice seed development
One of the major goals of crop production is to produce more grains with
less time, thus improving resource use efficiency. The duration of each
stage of seed development and the timing of transition between them is
of agronomical significance. As reviewed by Olsen (2020), mechanism
regulating the timing of endosperm cellularization has attracted
attention due to its positive correlation with endosperm and seed size.
Consequently, a precise and integrative landscape of seed development is
necessary and useful for both fundamental and applied studies on the
mechanisms underpinning crop yield and quality. Previously, from
viewpoint of crop physiology, we proposed a practical staging system
with three phases: embryo morphogenesis, endosperm filling, and seed
maturation (An et al., 2020). Here,
we update this staging system by
integrating of molecular, physiological, and anatomical evidence in the
current study as well as from the literature. In particular, considering
the dragging effect of embryo on endosperm development at the former
second stage (endosperm filling), we highlight the importance of this
stage as critical for grain filling and quality formation, and thus
subdivide it into two stages: embryo enlargement and endosperm filling.
Accordingly, we paint a holistic and dynamic picture of rice seed
development (Figure 8), and provide a brief description of each stage
and its agronomical relevance as follows.
Stage I : Morphogenesis (0-10 DAF): After double fertilization,
patterning and differentiation occurs simultaneously in the embryo and
endosperm. At the end of this stage, most of morphogenetic events in
embryo have already occurred. Endosperm has finished differentiation,
forming two subregions, the aleurone and starchy endosperm, and starts
storing starch and proteins.
Stage II : Embryo enlargement (10-20 DAF): Embryo greatly grows
to its maximum volume at 20 DAF (Itoh et al., 2005). Starchy endosperm
attains its highest rate of storage accumulation (Fu et al., 2013; Zhu,
Ye, Yang, Peng, & Zhang, 2011), while the aleurone cells is filled with
aleurone particles and spherosomes at the end of this stage (Yu, Zhou,
Xiong, & Wang, 2014). This stage witnesses strong interactions between
embryo and endosperm, hence being critical for rice grain filling and
quality.
Stage III : Endosperm filling (20-30 DAF): Embryo becomes
dormant and endosperm continues to accumulate starch and proteins,
reaching its maximum weight at 30 DAF. By the end of this stage, most of
the starchy endosperm and maternal tissues have undergone PCD, losing
their biological activity, while the aleurone and embryo is still alive
(Wu, Liu, Li, & Liu, 2016b; Wu, Liu, Li, & Liu, 2016c).
Stage IV : Maturation (30 DAF-maturity): After completion of
reserve accumulation, the embryo becomes tolerant of desiccation, and
undergoes a developmentally programmed dehydration event leading to
dormancy and a quiescent state (Angelovici, Galili, Fernie, & Fait,
2010; Manfre, LaHatte, Climer, & Marcotte, 2009). The starchy endosperm
cells die completely upon seed maturation and desiccation. At this
stage, seeds are susceptible to germination under hot and humid
conditions, thus being vulnerable to preharvest sprouting (Du et al.,
2018).
The integrative landscape from Figure 8 has important implications in
crop science and management. It draws distinctive patterns of embryo and
endosperm development, with endosperm ceasing storage accumulation at 30
DAF, ten days after the corresponding timepoint of embryo (20 DAF).
Figure S11 shows that the capacity of embryo to germinate starts at 15
DAF and peaks at 20 DAF for both genotypes of WT and NB. It is thus
inferred that the embryo has the priority of nutrient allocation over
endosperm during seed development. Moreover, it appears that this
asynchrony of embryo and endosperm
development is conserved across modern cultivars. They share a common
chronological time, with embryo developmentally maturing at 20 DAF
(Armenta-Medina et al., 2021; Itoh et al., 2016), while endosperm
matures at 30 DAF (Chen et al., 2013; Morita et al., 2005; Wang et al.,
2008; Wei et al., 2017; Wu et al., 2016c; Xu et al., 2021; Yang, Zhang,
Wang, Liu, & Wang, 2006). Therefore, the essential period of rice yield
and quality formation is the Stages I-III (Figure 8), from anthesis to
30 DAF. After that, rice seed enters the stage of desiccation and
maturation, lasting for 20 to 40 days with no marked increase in grain
weight. By dividing the 60-day period of grain filling into two separate
months, our previous report showed that only 10 % of the grain yield
was formed after 30 DAF (Xu et al., 2021). Under the intensive
rice-wheat and rice-oilseed rape cropping systems in the lower reaches
of Yangtze River, China, late maturity of the rice crop causes the late
sowing of wheat and oilseed rape, adversely affecting the seedling
growth and subsequently the grain or seed yield (Bai & Tao, 2017; Zhang
et al., 2020b). Accordingly, we suggest an agronomical intervention to
shorten the duration of the late maturation stage of rice in order to
adapt to the double cropping systems. In addition, future work should
exploit more genotypes to verify if this asynchrony of embryo and
endosperm development in chronological time is conserved in rice as well
as other cereal crops like maize and wheat.