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Metabolomics reveals significant variations in metabolites and correlations regarding the maturation of walnuts (Juglans regia L.).

Rao G, Sui J, Zhang J - Biol Open (2016)

Bottom Line: PCA scores revealed that the metabolic compositions of the embryo are different at each stage, while the metabolic composition of the endotesta could not be significantly separated into distinct groups.Additionally, 7225 metabolite-metabolite correlations were detected in walnut kernel by a Pearson correlation coefficient approach; during screening of the calculated correlations, 463 and 1047 were determined to be significant with r(2)≥0.49 and had a false discovery rate (FDR) ≤0.05 in endotesta and embryo, respectively.This work provides the first comprehensive metabolomic study of walnut kernels and reveals that most of the carbohydrate and protein-derived carbon was transferred into other compounds, such as fatty acids, during the maturation of walnuts, which may potentially provide the basis for further studies on walnut kernel metabolism.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Tree Genetics and Breeding, Research Institute of Forestry, Chinese Academy of Forestry, Beijing 100091, Republic of China Collaborative Innovation Center of Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing 210037, Republic of China Key Laboratory of Tree Breeding and Cultivation, State Forestry Administration, Research Institute of Forestry, Chinese Academy of Forestry, Beijing 100091, Republic of China.

No MeSH data available.


Boxplot-visualizations of amino acid relative abundances in endotesta and embryo of walnut kernels. The relative abundance of endotesta amino acids at different time points (1-5) are show in green, and the relative abundance of embryo amino acids at different time points (P1-P5; R1-R5) are show in red.
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BIO017863F4: Boxplot-visualizations of amino acid relative abundances in endotesta and embryo of walnut kernels. The relative abundance of endotesta amino acids at different time points (1-5) are show in green, and the relative abundance of embryo amino acids at different time points (P1-P5; R1-R5) are show in red.

Mentions: Levels of most amino acids were stable, however, not for asparagine, proline, and leucine in endotesta, which decreased during kernel ripening (Fig. 4). Asparagine is a nitrogen transport compound found in many plants, it accounts for 50-70% of the nitrogen carried in translocatory channels serving fruit and seed of white lupin (Lupinus albus L.) (Atkins et al., 1975). In soybean, asparagine was proven to have a positive correlation with protein concentration in developing seeds, and the level of asparagine synthesis was high initially and progressively declined in the seed coat (Pandurangan et al., 2012). In the present study the level of asparagine was over tenfold higher in the early stage (stage 1), suggesting that the development of kernels requires a large amount of nitrogen which can be used for protein synthesis at the early stage. Many studies have shown that proline plays a regulatory role in response to biotic and abiotic stress by increasing its content. A functional link between elevated proline and the ability of tolerance stress of seeds has been demonstrated in Arabidopsis thaliana (Hare et al., 2003). In sorghum seeds, proline also has the ability to increase the antioxidant compounds and oil antioxidant activity under normal and drought stress conditions in maize seed (Zea mays L.) (Ali et al., 2013). The level of proline is much higher at the early stage compared to other stages and progressively declines from stage 1 to stage 5, suggesting high levels of proline are required at the beginning of kernel development for preventing stress-induced damage. Observations have shown that leucine-derived carbon is incorporated into sugars and organic acids and is an alternate source of acetyl-CoA to sustain respiration and metabolic processes (Anderson et al., 1998). In the present study, leucine is present only at the early stage (stage 1), and barely detected at the later stages (stages 2-5), suggesting that leucine at stage 1 provides leucine-derived carbon for the subsequent synthesis of other compounds (sugars or organic acids) at the following stages. Endotesta are the barrier between the embryo and outer environment, and proteins in this tissue are mainly comprised of structural proteins, regulatory proteins, and transport proteins. The levels of these proteins are stable during the kernel ripening, which complies with the stability of amino acid levels noted in comparison with the embryo. The embryo is the main part of seed, consisting of precursor tissues for leaves, stem and root. Proteins in the embryo mainly comprise of storage proteins which provide the energy for kernel germination. High levels of amino acids were detected at the early stage and the level of most amino acids decreased during the development of kernel in embryo until only low levels were detected at stage 5 (Fig. 5), suggesting that most of the protein-derived carbon was transferred into other compounds during kernel development. A targeted global metabolomics platform with GC-MS was used to verify the accurate content of amino acids of kernels, which showed the same variation of trends of amino acids contents detected by an untargeted method. A total of 20 amino acids with a decreasing pattern across five development stages were identified, the total content of amino acids decreased from 3282.65 µg/g at T1 to 369.80 µg/g at T5 (Table 1).Fig. 4.


Metabolomics reveals significant variations in metabolites and correlations regarding the maturation of walnuts (Juglans regia L.).

Rao G, Sui J, Zhang J - Biol Open (2016)

Boxplot-visualizations of amino acid relative abundances in endotesta and embryo of walnut kernels. The relative abundance of endotesta amino acids at different time points (1-5) are show in green, and the relative abundance of embryo amino acids at different time points (P1-P5; R1-R5) are show in red.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4920193&req=5

BIO017863F4: Boxplot-visualizations of amino acid relative abundances in endotesta and embryo of walnut kernels. The relative abundance of endotesta amino acids at different time points (1-5) are show in green, and the relative abundance of embryo amino acids at different time points (P1-P5; R1-R5) are show in red.
Mentions: Levels of most amino acids were stable, however, not for asparagine, proline, and leucine in endotesta, which decreased during kernel ripening (Fig. 4). Asparagine is a nitrogen transport compound found in many plants, it accounts for 50-70% of the nitrogen carried in translocatory channels serving fruit and seed of white lupin (Lupinus albus L.) (Atkins et al., 1975). In soybean, asparagine was proven to have a positive correlation with protein concentration in developing seeds, and the level of asparagine synthesis was high initially and progressively declined in the seed coat (Pandurangan et al., 2012). In the present study the level of asparagine was over tenfold higher in the early stage (stage 1), suggesting that the development of kernels requires a large amount of nitrogen which can be used for protein synthesis at the early stage. Many studies have shown that proline plays a regulatory role in response to biotic and abiotic stress by increasing its content. A functional link between elevated proline and the ability of tolerance stress of seeds has been demonstrated in Arabidopsis thaliana (Hare et al., 2003). In sorghum seeds, proline also has the ability to increase the antioxidant compounds and oil antioxidant activity under normal and drought stress conditions in maize seed (Zea mays L.) (Ali et al., 2013). The level of proline is much higher at the early stage compared to other stages and progressively declines from stage 1 to stage 5, suggesting high levels of proline are required at the beginning of kernel development for preventing stress-induced damage. Observations have shown that leucine-derived carbon is incorporated into sugars and organic acids and is an alternate source of acetyl-CoA to sustain respiration and metabolic processes (Anderson et al., 1998). In the present study, leucine is present only at the early stage (stage 1), and barely detected at the later stages (stages 2-5), suggesting that leucine at stage 1 provides leucine-derived carbon for the subsequent synthesis of other compounds (sugars or organic acids) at the following stages. Endotesta are the barrier between the embryo and outer environment, and proteins in this tissue are mainly comprised of structural proteins, regulatory proteins, and transport proteins. The levels of these proteins are stable during the kernel ripening, which complies with the stability of amino acid levels noted in comparison with the embryo. The embryo is the main part of seed, consisting of precursor tissues for leaves, stem and root. Proteins in the embryo mainly comprise of storage proteins which provide the energy for kernel germination. High levels of amino acids were detected at the early stage and the level of most amino acids decreased during the development of kernel in embryo until only low levels were detected at stage 5 (Fig. 5), suggesting that most of the protein-derived carbon was transferred into other compounds during kernel development. A targeted global metabolomics platform with GC-MS was used to verify the accurate content of amino acids of kernels, which showed the same variation of trends of amino acids contents detected by an untargeted method. A total of 20 amino acids with a decreasing pattern across five development stages were identified, the total content of amino acids decreased from 3282.65 µg/g at T1 to 369.80 µg/g at T5 (Table 1).Fig. 4.

Bottom Line: PCA scores revealed that the metabolic compositions of the embryo are different at each stage, while the metabolic composition of the endotesta could not be significantly separated into distinct groups.Additionally, 7225 metabolite-metabolite correlations were detected in walnut kernel by a Pearson correlation coefficient approach; during screening of the calculated correlations, 463 and 1047 were determined to be significant with r(2)≥0.49 and had a false discovery rate (FDR) ≤0.05 in endotesta and embryo, respectively.This work provides the first comprehensive metabolomic study of walnut kernels and reveals that most of the carbohydrate and protein-derived carbon was transferred into other compounds, such as fatty acids, during the maturation of walnuts, which may potentially provide the basis for further studies on walnut kernel metabolism.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Tree Genetics and Breeding, Research Institute of Forestry, Chinese Academy of Forestry, Beijing 100091, Republic of China Collaborative Innovation Center of Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing 210037, Republic of China Key Laboratory of Tree Breeding and Cultivation, State Forestry Administration, Research Institute of Forestry, Chinese Academy of Forestry, Beijing 100091, Republic of China.

No MeSH data available.