Carbohydrate flow during grain filling: Phytohormonal regulation and genetic control in rice (Oryza sativa)

Abstract

Both the filling and development of grain are key processes determining agriculture production and reproductive growth in rice. The processes of grain filling and endosperm development are crucial for the accumulation of major storage compounds in rice grains. This requires extensive remobilization of carbon reserves from source to sink and the precise regulation of sucrose-to-starch conversion. Both the developmental sequence of the panicle and environmental signals influence the carbon flow between the leaves, leaf sheath, stem, and spikelets during grain filling. This, in turn, affects endosperm development and the production of storage compounds. In this review, we synthesize recent insight into grain development in rice, focusing on the dynamic changes in phytohormones and how their homeostasis integrates developmental and environmental cues to control grain filling in the developing panicle. We also highlight recent advances in the genetic control of carbohydrate remobilization and the transcriptional regulatory networks governing carbohydrate metabolism and grain development in rice. The asynchronous initiation and imbalance in grain filling limit the full yield potential of cereal crops. The "superior/inferior spikelets" serve as a model system for understanding the regulatory mechanisms underlying grain filling and development. Systematic research on carbohydrate flow and phytohormone crosstalk could enhance our understanding of optimizing yield production in cereal crops. Additionally, a thorough analysis of key genetic regulatory mechanisms can offer a genetic foundation and targets for precisely adjusting grain filling traits, ultimately aiding in the development of high-yield crop varieties.

Keywords: carbohydrate; environmental response; genetic control; grain development; grain filling; phytohormonal regulation; rice.

Figure 1

Schematic overview of grain development in rice (A) The relative volume of caryopsis within the grain and morphological event is presented throughout the developmental process of rice grain. Total starch and protein content in grain (relative to maximum volume) is shown in parallel with the time course (days after pollination (DAP)). (B) Timeline diagram of developmental differences and hormone level changes between superior and inferior grains. The solid lines represent superior spikelet grains (SS), and the dashed lines represent inferior spikelet grains (IS), illustrating the developmental differences and changes in hormone levels over time.

Figure 2

Schematic model of carbohydrate transportation and metabolism during grain filling and development (A) Possible transport routes of carbohydrates during rice grain filling. The model is made based on previous studies. In source tissues, sucrose may move from the mesophyll cell (MSC) to bundle sheath cell (BSC) and parenchyma cells (PC) in the leaf vascular bundle. The companion cell (CC) takes up sucrose and transfers sugar into the sieve elements (SE) in the phloem. In sink tissues, sucrose may unload from the phloem to PC in a vascular bundle and then transfer to nucellar cells (NC) through symplasmic transportation, then sucrose is exported into the apoplasmic space between nucellar cells and storage cells (SC). Clade III OsSWEET genes (OsSWEET11/15) involved in sucrose export into the apoplasmic space, and CIN/CWI gene (GIF1)‐mediated hydrolysis of sucrose are also important to the starch quality and grain filling rate. OsSWEET4‐mediated hexose transportation also plays an essential role in rice grain filling. (B) Schematic of carbohydrate transformation during grain filling and development. The dotted red lines indicate sucrose transportation routes, and the dotted gray lines represent the metabolic flow of carbohydrates. The major gene families involved in these bio‐processes are marked in the corresponding plots.

Figure 3

Schematic presentation of the regulatory network regulating grain filling, grain development and carbohydrate partitioning in rice Transcription factors and their downstream pathways are involved in starch degradation, carbohydrate transportation, storage synthesis and grain development in rice. Green rounded squares and yellow rounded squares represent positive regulators and negative regulators, respectively. Red blocking arrows and green arrows indicate inhibition and promotion, respectively.