Involvement of sulfur assimilation in the low β subunit content of soybean seed storage protein revealed by comparative transcriptome analysis

Xi, Zhiyong; Xu, Ruixin; Hu, Wei; Wang, Wan; Han, Dejun; Zhang, Fan; Gu, Ying; Guo, Yong; Wang, Jun; Qiu, Lijuan

doi:10.1016/j.cj.2019.01.001

Cited by 8 publications

(6 citation statements)

References 51 publications

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“…To date, efforts to alter sulfur amino acid content in various plants, including maize, rice, and soybean, have resulted in increased cysteine and/or methionine levels, but also a range of other effects on plant metabolism, seed composition, and plant growth 8 , 9 , 13 , 14 , 31 – 33 , 35 , 50 – 53 . As shown here and in previous work 46 , increased expression of either sulfur assimilation (ATP sulfurylase) or cysteine biosynthesis (OASS) enzymes in soybean enhance sulfur-containing amino acid content but with rebalanced distribution of sulfur-rich seed proteins. Similar approaches that enhancement of sulfur metabolism in maize led to increases of methionine-rich zein seed proteins without negative effects on plant growth 13 , 14 , which highlights differences in nutrient metabolism and seed development in different crop plants.…”

Section: Discussionsupporting

confidence: 83%

“…The increase in the methionine availability in transgenic seeds may be a contributing factor for the suppression of the β-subunit of β-conglycinin accumulation observed in our study. A recent study reported a 31.5% increase in the sulfur amino acid content in soybean lines that tend to accumulate low level of the β-subunit of β-conglycinin 46 . Transcriptome analysis of this soybean line revealed up regulation of genes involved in anabolism of cysteine, methionine and glutathione indicating a close relationship between sulfur amino acid content and the β-subunit of β-conglycinin accumulation 46 .…”

Section: Discussionmentioning

confidence: 98%

“…A recent study reported a 31.5% increase in the sulfur amino acid content in soybean lines that tend to accumulate low level of the β-subunit of β-conglycinin 46 . Transcriptome analysis of this soybean line revealed up regulation of genes involved in anabolism of cysteine, methionine and glutathione indicating a close relationship between sulfur amino acid content and the β-subunit of β-conglycinin accumulation 46 . Previously, we reported transgenic soybean plants overexpressing a cytosolic OASS contained higher amounts of BBI 9 .…”

Section: Discussionmentioning

confidence: 98%

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Overexpression of ATP sulfurylase improves the sulfur amino acid content, enhances the accumulation of Bowman–Birk protease inhibitor and suppresses the accumulation of the β-subunit of β-conglycinin in soybean seeds

Kim

Sun-Hyung

Oehrle

et al. 2020

Sci Rep

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ATP sulfurylase, an enzyme which catalyzes the conversion of sulfate to adenosine 5′-phosphosulfate (APS), plays a significant role in controlling sulfur metabolism in plants. In this study, we have expressed soybean plastid ATP sulfurylase isoform 1 in transgenic soybean without its transit peptide under the control of the 35S CaMV promoter. Subcellular fractionation and immunoblot analysis revealed that ATP sulfurylase isoform 1 was predominantly expressed in the cell cytoplasm. Compared with that of untransformed plants, the ATP sulfurylase activity was about 2.5-fold higher in developing seeds. High-resolution 2-D gel electrophoresis and immunoblot analyses revealed that transgenic soybean seeds overexpressing ATP sulfurylase accumulated very low levels of the β-subunit of β-conglycinin. In contrast, the accumulation of the cysteine-rich Bowman–Birk protease inhibitor was several fold higher in transgenic soybean plants when compared to the non-transgenic wild-type seeds. The overall protein content of the transgenic seeds was lowered by about 3% when compared to the wild-type seeds. Metabolite profiling by LC–MS and GC–MS quantified 124 seed metabolites out of which 84 were present in higher amounts and 40 were present in lower amounts in ATP sulfurylase overexpressing seeds compared to the wild-type seeds. Sulfate, cysteine, and some sulfur-containing secondary metabolites accumulated in higher amounts in ATP sulfurylase transgenic seeds. Additionally, ATP sulfurylase overexpressing seeds contained significantly higher amounts of phospholipids, lysophospholipids, diacylglycerols, sterols, and sulfolipids. Importantly, over expression of ATP sulfurylase resulted in 37–52% and 15–19% increases in the protein-bound cysteine and methionine content of transgenic seeds, respectively. Our results demonstrate that manipulating the expression levels of key sulfur assimilatory enzymes could be exploited to improve the nutritive value of soybean seeds.

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Section: Discussionsupporting

confidence: 83%

Section: Discussionmentioning

confidence: 98%

Section: Discussionmentioning

confidence: 98%

See 1 more Smart Citation

Overexpression of ATP sulfurylase improves the sulfur amino acid content, enhances the accumulation of Bowman–Birk protease inhibitor and suppresses the accumulation of the β-subunit of β-conglycinin in soybean seeds

Kim

Sun-Hyung

Oehrle

et al. 2020

Sci Rep

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“…Zhang observed that proteins at the oil‐water interface tend to unfold and rearrange, thus making it easier to oxidize free sulfhydryl groups or freeing sulfhydryl groups at the interface to form disulfide bonds, improving dilational modulus (Zheng et al, 2015). Previous studies have demonstrated dramatic changes in physicochemical properties of proteins induced by sulfhydryl group‐disulfide bond exchange reactions (He et al.,2014) or β‐elimination reactions (Sun et al., 2020; Zhang, Xu, et al., 2019; Zhang, Xiong, et al., 2019). In this study, it was found that throughout LOX‐catalyzed oxidation of arachin and conarachin, total sulfhydryl content and number of disulfide bonds was greater for conarachin when compared with arachin, while there were less active sulfhydryl groups in conarachin (Shen et al., 2015).…”

Section: Resultsmentioning

confidence: 99%

Effect of lipoxygenase‐induced oxidation on molecular structure and digestive properties of arachin and conarachin

Zhang

et al. 2021

Food Processing Preservation

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Lipid oxidation products can affect the molecular structure and digestibility of peanut protein isolates. Lipid-oxidizing systems (LOS) is a simulation system which uses oxygen-free radicals generated by the reaction of linoleic acid and lipoxygenase as oxidants.The simulation system was established to mediate oxidation of arachin or conarachin. Degree of oxidation (DOX) of peanut protein isolates (PPIs) was measured as quantity of LA to generate LOS. This study analyzed the effect of lipid oxidation-derived free radicals on the molecular structure and digestive properties of arachin and conarachin and observed substantial changes in carbonyl content, total sulfhydryl content, and number of disulfide bonds as quantities of LA increased, thus indicating significant oxidation of two proteins. Further, it was found that arachin was more stable than conarachin in a LOX-catalyzed oxidizing system. When the amount of LA was 3 and 5 ml, the maximum surface hydrophobic characteristic values of arachin and conarachin reached the maximum, which were 235 ± 10 and 349 ± 13, respectively. This study laid a theoretical foundation for the application of peanut protein in food products.

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“…To performed qRT-PCR, seeds germinated at 0HAG, 18HAG, and 36HAG were stored in liquid nitrogen immediately after germination. qRT-PCR were performed basically according to Zhang et al 64 with modifications. Total RNA was isolated by TRNzol (cat.…”

Section: Methodsmentioning

confidence: 99%

Nutritional evaluation and transcriptome analyses of short-time germinated seeds in soybean (Glycine max L. Merri.)

Liu

Xiong

et al. 2021

Sci Rep

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Germination is a common practice for nutrition improvement in many crops. In soybean, the nutrient value and genome-wide gene expression pattern of whole seeds germinated for short-time has not been fully investigated. In this study, protein content (PC), water soluble protein content (WSPC), isoflavone compositions were evaluated at 0 and 36 h after germination (HAG), respectively. The results showed that at 36HAG, PC was slightly decreased (P > 0.05) in ZD41, J58 and JHD, WSPC and free isoflavone (aglycones: daidzein, genistein, and glycitein) were significantly increased (P < 0.05), while total isoflavone content was unchanged. Transcriptomic analysis identified 5240, 6840 and 15,766 DEGs in different time point comparisons, respectively. GO and KEGG analysis showed that photosynthesis process was significantly activated from 18HAG, and alternative splicing might play an important role during germination in a complex manner. Response to hydrogen peroxide (H2O2) was found to be down regulated significantly from 18 to 36HAG, suggesting that H2O2 might play an important role in germination. Expression pattern analysis showed the synthesis of storage proteins was slowing down, while the genes coding for protein degradation (peptidase and protease) were up regulated as time went by during germination. For genes involved in isoflavone metabolism pathway, UGT (7-O-glucosyltransferase) coding genes were significantly up regulated (40 up-DEGs vs 27 down-DEGs), while MAT (7-O-glucoside-6′′-O-malonyltransferase) coding genes were down regulated, which might explain the increase of aglycones after germination. This study provided a universal transcriptomic atlas for whole soybean seeds germination in terms of nutrition and gene regulation mechanism.

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Involvement of sulfur assimilation in the low β subunit content of soybean seed storage protein revealed by comparative transcriptome analysis

Cited by 8 publications

References 51 publications

Overexpression of ATP sulfurylase improves the sulfur amino acid content, enhances the accumulation of Bowman–Birk protease inhibitor and suppresses the accumulation of the β-subunit of β-conglycinin in soybean seeds

Overexpression of ATP sulfurylase improves the sulfur amino acid content, enhances the accumulation of Bowman–Birk protease inhibitor and suppresses the accumulation of the β-subunit of β-conglycinin in soybean seeds

Effect of lipoxygenase‐induced oxidation on molecular structure and digestive properties of arachin and conarachin

Nutritional evaluation and transcriptome analyses of short-time germinated seeds in soybean (Glycine max L. Merri.)

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