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Engineering sulfur storage in maize seed proteins without apparent yield loss.

ABSTRACT: Sulfur assimilation may limit the pool of methionine and cysteine available for incorporation into zeins, the major seed storage proteins in maize. This hypothesis was tested by producing transgenic maize with deregulated sulfate reduction capacity achieved through leaf-specific expression of the Escherichia coli enzyme 3'-phosphoadenosine-5'-phosphosulfate reductase (EcPAPR) that resulted in higher methionine accumulation in seeds. The transgenic kernels have higher expression of the methionine-rich 10-kDa ?-zein and total protein sulfur without reduction of other zeins. This overall increase in the expression of the S-rich zeins describes a facet of regulation of these proteins under enhanced sulfur assimilation. Transgenic line PE5 accumulates 57.6% more kernel methionine than the high-methionine inbred line B101. In feeding trials with chicks, PE5 maize promotes significant weight gain compared with nontransgenic kernels. Therefore, increased source strength can improve the nutritional value of maize without apparent yield loss and may significantly reduce the cost of feed supplementation.

SUBMITTER: Planta J

PROVIDER: S-EPMC5664557 | biostudies-literature | 2017 Oct

REPOSITORIES: biostudies-literature

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Engineering sulfur storage in maize seed proteins without apparent yield loss.

Planta Jose J Xiang Xiaoli X Leustek Thomas T Messing Joachim J

Proceedings of the National Academy of Sciences of the United States of America 20171009 43

Sulfur assimilation may limit the pool of methionine and cysteine available for incorporation into zeins, the major seed storage proteins in maize. This hypothesis was tested by producing transgenic maize with deregulated sulfate reduction capacity achieved through leaf-specific expression of the <i>Escherichia coli</i> enzyme 3'-phosphoadenosine-5'-phosphosulfate reductase (<i>Ec</i>PAPR) that resulted in higher methionine accumulation in seeds. The transgenic kernels have higher expression of ...[more]

PMID: 29073061

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Project description:BACKGROUND: A balanced composition of amino acids in seed flour is critical because of the demand on essential amino acids for nutrition. However, seed proteins in cereals like maize, the crop with the highest yield, are low in lysine, tryptophan, and methionine. Although supplementation with legumes like soybean can compensate lysine deficiency, both crops are also relatively low in methionine. Therefore, understanding the mechanism of methionine accumulation in the seed could be a basis for breeding cultivars with superior nutritional quality. RESULTS: In maize (Zea mays), the 22- and 19-kDa ?-zeins are the most prominent storage proteins, nearly devoid of lysine and methionine. Although silencing synthesis of these proteins through RNA interference (RNAi) raises lysine levels in the seed, it fails to do so for methionine. Computational analysis of annotated gene models suggests that about 57% of all proteins exhibit a lysine content of more than 4%, whereas the percentage of proteins with methionine above 4% is only around 8%. To compensate for this low representation, maize seeds produce specialized storage proteins, the 15-kDa ?-, 18-kDa and 10-kDa ?-zeins, rich in methionine. However, they are expressed at variant levels in different inbred lines. A654, an inbred with null ?-zein alleles, methionine levels are significantly lower than when the two intact ?-zein alleles are introgressed. Further silencing of ?-zein results in dramatic reduction in methionine levels, indicating that ?- and ?-zeins are the main sink of methionine in maize seed. Overexpression of the 10-kDa ?-zein can increase the methionine level, but protein analysis by SDS-PAGE shows that the increased methionine levels occur at least in part at the expense of cysteines present in ?- and ?-zeins. The reverse is true when ?- and ?-zein expression is silenced through RNAi, then 10-kDa ?-zein accumulates to higher levels. CONCLUSIONS: Because methionine receives the sulfur moiety from cysteine, it appears that when seed protein synthesis of cysteine-rich proteins is blocked, the synthesis of methionine-rich seed proteins is induced, probably at the translational level. The same is true, when methionine-rich proteins are overexpressed, synthesis of cysteine-rich proteins is reduced, probably also at the translational level. Although we only hypothesize a translational control of protein synthesis at this time, there are well known paradigms of how amino acid concentration can play a role in differential gene expression. The latter we think is largely controlled by the flux of reduced sulfur during plant growth.

Project description:Although the impact of sulfur (S) availability on the seed yield and nutritional quality of seeds has been demonstrated, its impact coupled with nitrogen (N) availability remains poorly studied in oilseed rape. A deeper knowledge of S and N interactions on seed yield components and seed quality could improve S and N fertilization management in a sustainable manner. To address this question, our goals were to determine the effects of nine different S fertilization management strategies (i) in interaction with different levels of N fertilization and (ii) according to the timing of application (by delaying and fractionating the S inputs) on agronomic performances and components of seed yield. The impact of these various managements of S and N fertilizations was also investigated on the seed quality with a focus on the composition of SSPs (mainly represented by napins and cruciferins). Our results highlighted synergetic effects on S and N use efficiencies at optimum rates of S and N inputs and antagonistic effects at excessive rates of one of the two elements. The data indicated that adjustment of S and N fertilization may lead to high seed yield and seed protein quality in a sustainable manner, especially in the context of reductions in N inputs. Delaying S inputs improved the seed protein quality by significantly increasing the relative abundance of napin (a SSP rich in S-containing amino acids) and decreasing the level of a cruciferin at 30 kDa (a SSP with low content of S-amino acids). These observations suggest that fractionated or delayed S fertilizer inputs could provide additional insights into the development of N and S management strategies to maintain or improve seed yield and protein quality. Our results also demonstrated that the S% in seeds and the napin:30 kDa-cruciferin ratio are highly dependent on S/N fertilization in relation to S supply. In addition, we observed a strong relationship between S% in seeds and the abundance of napin as well as the napin:30 kDa-cruciferin ratio, suggesting that S% may be used as a relevant index for the determination of protein quality in seeds in terms of S-containing amino acids.

Dataset Information

Engineering sulfur storage in maize seed proteins without apparent yield loss.

Publications

Engineering sulfur storage in maize seed proteins without apparent yield loss.

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