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An Integrated "Multi-Omics" Comparison of Embryo and Endosperm Tissue-Specific Features and Their Impact on Rice Seed Quality.

ABSTRACT: Although rice is a key crop species, few studies have addressed both rice seed physiological and nutritional quality, especially at the tissue level. In this study, an exhaustive "multi-omics" dataset on the mature rice seed was obtained by combining transcriptomics, label-free shotgun proteomics and metabolomics from embryo and endosperm, independently. These high-throughput analyses provide a new insight on the tissue-specificity related to rice seed quality. Foremost, we pinpointed that extensive post-transcriptional regulations occur at the end of rice seed development such that the embryo proteome becomes much more diversified than the endosperm proteome. Secondly, we observed that survival in the dry state in each seed compartment depends on contrasted metabolic and enzymatic apparatus in the embryo and the endosperm, respectively. Thirdly, it was remarkable to identify two different sets of starch biosynthesis enzymes as well as seed storage proteins (glutelins) in both embryo and endosperm consistently with the supernumerary embryo hypothesis origin of the endosperm. The presence of a putative new glutelin with a possible embryonic favored abundance is described here for the first time. Finally, we quantified the rate of mRNA translation into proteins. Consistently, the embryonic panel of protein translation initiation factors is much more diverse than that of the endosperm. This work emphasizes the value of tissue-specificity-centered "multi-omics" study in the seed to highlight new features even from well-characterized pathways. It paves the way for future studies of critical genetic determinants of rice seed physiological and nutritional quality.

SUBMITTER: Galland M

PROVIDER: S-EPMC5702907 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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An Integrated "Multi-Omics" Comparison of Embryo and Endosperm Tissue-Specific Features and Their Impact on Rice Seed Quality.

Galland Marc M He Dongli D Lounifi Imen I Arc Erwann E Clément Gilles G Balzergue Sandrine S Huguet Stéphanie S Cueff Gwendal G Godin Béatrice B Collet Boris B Granier Fabienne F Morin Halima H Tran Joseph J Valot Benoit B Rajjou Loïc L

Frontiers in plant science 20171122

Although rice is a key crop species, few studies have addressed both rice seed physiological and nutritional quality, especially at the tissue level. In this study, an exhaustive "multi-omics" dataset on the mature rice seed was obtained by combining transcriptomics, label-free shotgun proteomics and metabolomics from embryo and endosperm, independently. These high-throughput analyses provide a new insight on the tissue-specificity related to rice seed quality. Foremost, we pinpointed that exten ...[more]

PMID: 29213276

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Project description: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.

Project description:BackgroundRice is not only an essential food but also a source of high quality protein. Polyploidy is an evolutionary trajectory in plants, and enhancing glutelin by polyploidization is an attractive strategy for improving the nutritional value of rice seeds and presents a great potential for enhancing the commercial value of rice. Elucidating the mechanisms underlying glutelin synthesis and accumulation in tetraploid rice is of great significance.ResultsTo enhance the nutritional value of rice, we developed tetraploid rice and evaluated the contents of various nutrient elements in mature seeds. The results revealed a significant increase in protein contents, including the total seed storage proteins, glutelins, and amino acids in tetraploid rice when compared with those in diploid rice. Tandem mass tag-based quantitative proteomic analyses of seeds revealed that glutelins regulated by several glutelin genes in 9311-4x were significantly up-regulated (≥1.5-fold), which was further verified by immunoblot analyses. In addition, temporal expression patterns of various glutelin subunits in different rice lines were investigated. The results revealed significant differences in the expression patterns between diploid and tetraploid rice seeds. Cytohistological analyses results revealed that the thickness of aleurone cell layers increased significantly by 32% in tetraploid rice, the structures of protein storage vacuoles (PSVs) in sub-aleurone cells were more diverse and abundant than those of diploid rice. Temporal expression and proteomic analyses results revealed that protein disulfide isomerase-like 1-1 expression levels were higher in tetraploid rice than in diploid rice, and that the gene responded to oxidative folding with increased levels of proglutelin and appropriate distribution of seed glutelins in tetraploid rice.ConclusionThe results of the present study revealed that polyploidization increased glutelin content by influencing glutelin biosynthesis, transport, and deposition, while variations in glutelin accumulation between tetraploid and diploid rice were largely manifested in the initial time, duration, and relative levels of various glutelin gene expressions during seed filling stages. These findings provide novel insights into improving the protein quality and nutritional value of rice seeds by polyploid breeding.

Dataset Information

An Integrated "Multi-Omics" Comparison of Embryo and Endosperm Tissue-Specific Features and Their Impact on Rice Seed Quality.

Publications

An Integrated "Multi-Omics" Comparison of Embryo and Endosperm Tissue-Specific Features and Their Impact on Rice Seed Quality.

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