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.