Embryo-Endosperm Interaction and Its Agronomic Relevance to Rice Quality

Abstract

Embryo-endosperm interaction is the dominant process controlling grain filling, thus being crucial for yield and quality formation of the three most important cereals worldwide, rice, wheat, and maize. Fundamental science of functional genomics has uncovered several key genetic programs for embryo and endosperm development, but the interaction or communication between the two tissues is largely elusive. Further, the significance of this interaction for grain filling remains open. This review starts with the morphological and developmental aspects of rice grain, providing a spatial and temporal context. Then, it offers a comprehensive and integrative view of this intercompartmental interaction, focusing on (i) apoplastic nutrient flow from endosperm to the developing embryo, (ii) dependence of embryo development on endosperm, (iii) regulation of endosperm development by embryo, and (iv) bidirectional dialogues between embryo and endosperm. From perspective of embryo-endosperm interaction, the mechanisms underlying the complex quality traits are explored, with grain chalkiness as an example. The review ends with three open questions with scientific and agronomic importance that should be addressed in the future. Notably, current knowledge and future prospects of this hot research topic are reviewed from a viewpoint of crop physiology, which should be helpful for bridging the knowledge gap between the fundamental plant sciences and the practical technologies.

Keywords: embryo; endosperm; grain quality; interaction; rice; seed development.

Figure 1

The structure of mature rice grain (caryopsis). The maternal tissues are composed of pericarp (light green), testa (green), and nucellus (yellow), and are located at the outer layer. The endosperm consists of aleurone (white) and starchy endosperm (pink) that are packed with starch granules and protein bodies, respectively. Generally, the aleurone has two or three layers at the dorsal, whereas one at the ventral side of rice grain. Opaque tissues (light blue), called chalkiness, generally occurs at the ventral (white-belly) and central (white-core) parts of endosperm. The embryo (light yellow) is composed of two structures: scutellum and embryonic axis (plumule, mesocotyl, and radicle).

Figure 2

Schematic illustration of morphological changes of embryo (longitudinal section, I), endosperm (transversal, II), and the dynamics of dry matter accumulation (III) during rice grain filling. The three phases proposed are indicated. Changed colors of the pericarp and testa show the process of degradation of maternal tissues (Wu et al., 2016a,b), and that of the starchy endosperm indicates the grain-filling process. The curve of grain weight and water content are depicted by data synthesized from Zhu et al. (2011), Fu et al. (2013), and Wu et al. (2016b). Stage 1 (embryo morphogenesis): At 2 days after fertilization (DAF), embryo is at globular stage (A), and endosperm at the coenocyte stage (A'). At 5 DAF, embryo has the first leaf primordium and recognizable scutellum (B), endosperm cellularization is completed (B'). At 10 DAF, embryo morphogenesis is basically completed (C); endosperm differentiation is finished, with two structures of the aleurone and starchy endosperm (C'). Stage 2 (endosperm filling): During 10–30 DAF, embryo becomes dormant (D,E); endosperm accumulates storage compounds and attains its maximum weight (D',E'). Stage 3 (seed maturation): embryo (F) and endosperm (F') continue to dehydrate until maturity.

Figure 3

Schematic illustration of embryo-endosperm interactions during rice grain filling. Concomitant development of embryo and endosperm within the limited space of seed coat requires bidirectional dialogues between the two compartments. This interaction can be summarized by the following four aspects. (A) Nutrient flow from endosperm to the developing embryo via apoplastic transportation. Nutrients and their transporters are indicated. ① Sucrose transporters, SWEET11, SWEET15 (Chen et al., 2015), and SUC5 (Baud et al., 2005). ② Amino acids transporters, UMAMIT25 (Besnard et al., 2018), and AAP1 (Sanders et al., 2009). ③ Lipids transporter, OsLTPL36 (Wang et al., 2015). ④ Fe transporter, OsYSL9 (Senoura et al., 2017). (B) Dependence of embryo development on endosperm. Genes exclusively expressed in or signaling released from endosperm that regulate embryo development are shown. ① FIS-PRC2 and AGL62 (Hehenberger et al., 2012). ② EDE1 (Pignocchi et al., 2009). ③ RGH3 (Fouquet et al., 2011). ④ Zou (Yang et al., 2008). ⑤ OS1 (Song et al., 2019). ⑥ Auxin (Chen et al., 2014). ⑦ Polypeptides (Widiez et al., 2017). ⑧ PHS8 (Du et al., 2018). ⑨ Small-interfering RNA (siRNA; Lafon-Placette and Köhler et al., 2014). (C) Regulation of endosperm development by embryo. Genes elusively expressed in or signaling released from embryo that modulate endosperm development are demonstrated. ① GA/ABA (Zeeman, 2015). ② CDC2A (Nowack et al., 2006). ③ VP1 (Zheng et al., 2019). (D) Developmental coordination between embryo and endosperm. Bidirectional dialogues are presented by signaling pathways mediated by ① GE (Nagasawa et al., 2013) and ② TWS1 (Doll et al., 2020a). Dotted line indicates putative or unproven signaling pathway.

Figure 4

Starch degradation in the endosperm cells facing the scutellum of the embryo. Micro-pores or pits (white arrow) on the surface of starch granule indicate the hydrolysis of starch reserve by α-amylase. The location of (A) is nearer to embryo (scutellum) than that of (B). Note that starch granules are smaller at location (A) than those at (B). The immature starch granules at location (A) might be the result of nutrient deprivation by the developing embryo.