Multi-Omics Approaches Unravel Specific Features of Embryo and Endosperm in Rice Seed Germination

Abstract

Seed germination and subsequent seedling growth affect the final yield and quality of the crop. Seed germination is defined as a series of processes that begins with water uptake by a quiescent dry seed and ends with the elongation of embryonic axis. Rice is an important cereal crop species, and during seed germination, two tissues function in a different manner; the embryo grows into a seedling as the next generation and the endosperm is responsible for nutritional supply. Toward understanding the integrated roles of each tissue at the transcriptional, translational, and metabolic production levels during germination, an exhaustive "multi-omics" analysis was performed by combining transcriptomics, label-free shotgun proteomics, and metabolomics on rice germinating embryo and endosperm, independently. Time-course analyses of the transcriptome and metabolome in germinating seeds revealed a major turning point in the early phase of germination in both embryo and endosperm, suggesting that dramatic changes begin immediately after water imbibition in the rice germination program at least at the mRNA and metabolite levels. In endosperm, protein profiles mostly showed abundant decreases corresponding to 90% of the differentially accumulated proteins. An ontological classification revealed the shift from the maturation to the germination process where over-represented classes belonged to embryonic development and cellular amino acid biosynthetic processes. In the embryo, 19% of the detected proteins are differentially accumulated during germination. Stress response, carbohydrate, fatty acid metabolism, and transport are the main functional classes representing embryo proteome change. Moreover, proteins specific to the germinated state were detected by both transcriptomic and proteomic approaches and a major change in the network operating during rice germination was uncovered. In particular, concomitant changes of hormonal metabolism-related proteins (GID1L2 and CNX1) implicated in GAs and ABA metabolism, signaling proteins, and protein turnover events emphasized the importance of such biological networks in rice seeds. Using metabolomics, we highlighted the importance of an energetic supply in rice seeds during germination. In both embryo and endosperm, starch degradation, glycolysis, and subsequent pathways related to these cascades, such as the aspartate-family pathway, are activated during germination. A relevant number of accumulated proteins and metabolites, especially in embryos, testifies the pivotal role of energetic supply in the preparation of plant growth. This article summarizes the key genetic pathways in embryo and endosperm during rice seed germination at the transcriptional, translational, and metabolite levels and thereby, emphasizes the value of combined multi-omics approaches to uncover the specific feature of tissues during germination.

Keywords: embryo; endosperm; germination; multi-omics; seed.