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      Contrasting gene expression patterns in grain of high and low asparagine wheat genotypes in response to sulphur supply

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          Abstract

          Background

          Free asparagine is the precursor for acrylamide formation during cooking and processing of grains, tubers, beans and other crop products. In wheat grain, free asparagine, free glutamine and total free amino acids accumulate to high levels in response to sulphur deficiency. In this study, RNA-seq data were acquired for the embryo and endosperm of two genotypes of bread wheat, Spark and SR3, growing under conditions of sulphur sufficiency and deficiency, and sampled at 14 and 21 days post anthesis (dpa). The aim was to provide new knowledge and understanding of the genetic control of asparagine accumulation and breakdown in wheat grain.

          Results

          There were clear differences in gene expression patterns between the genotypes. Sulphur responses were greater at 21 dpa than 14 dpa, and more evident in SR3 than Spark. TaASN2 was the most highly expressed asparagine synthetase gene in the grain, with expression in the embryo much higher than in the endosperm, and higher in Spark than SR3 during early development. There was a trend for genes encoding enzymes of nitrogen assimilation to be more highly expressed in Spark than SR3 when sulphur was supplied. TaASN2 expression in the embryo of SR3 increased in response to sulphur deficiency at 21 dpa, although this was not observed in Spark. This increase in TaASN2 expression was accompanied by an increase in glutamine synthetase gene expression and a decrease in asparaginase gene expression. Asparagine synthetase and asparaginase gene expression in the endosperm responded in the opposite way. Genes encoding regulatory protein kinases, SnRK1 and GCN2, both implicated in regulating asparagine synthetase gene expression, also responded to sulphur deficiency. Genes encoding bZIP transcription factors, including Opaque2/bZIP9, SPA/bZIP25 and BLZ1/OHP1/bZIP63, all of which contain SnRK1 target sites, were also expressed. Homeologues of many genes showed differential expression patterns and responses, including TaASN2.

          Conclusions

          Data on the genetic control of free asparagine accumulation in wheat grain and its response to sulphur supply showed grain asparagine levels to be determined in the embryo, and identified genes encoding signalling and metabolic proteins involved in asparagine metabolism that respond to sulphur availability.

          Electronic supplementary material

          The online version of this article (10.1186/s12864-019-5991-8) contains supplementary material, which is available to authorized users.

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          Most cited references37

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          Acrylamide formation mechanism in heated foods.

          Recent findings of a potential human carcinogen, acrylamide, in foods have focused research on the possible mechanisms of formation. We present a mechanism for the formation of acrylamide from the reaction of the amino acid asparagine and a carbonyl-containing compound at typical cooking temperatures. The mechanism involves formation of a Schiff base followed by decarboxylation and elimination of either ammonia or a substituted imine under heat to yield acrylamide. Isotope substitution studies and mass spectrometric analysis of heated model systems confirm the presence of key reaction intermediates. Further confirmation of this mechanism is accomplished through selective removal of asparagine with asparaginase that results in a reduced level of acrylamide in a selected heated food.
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            Scientific Opinion on acrylamide in food

            (2015)
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              Asparagine in plants

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                Author and article information

                Contributors
                curtistanya4@gmail.com
                sarah.raffan@rothamsted.ac.uk
                yongfang.wan@rothamsted.ac.uk
                robert.king@rothamsted.ac.uk
                gonzaleza@ebi.ac.uk
                44 1582 938203 , nigel.halford@rothamsted.ac.uk
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                1 August 2019
                1 August 2019
                2019
                : 20
                : 628
                Affiliations
                [1 ]ISNI 0000 0001 2227 9389, GRID grid.418374.d, Plant Sciences Department, , Rothamsted Research, ; Harpenden, Hertfordshire AL5 2JQ UK
                [2 ]ISNI 0000 0001 2227 9389, GRID grid.418374.d, Computational and Analytical Sciences Department, , Rothamsted Research, ; Harpenden, Hertfordshire AL5 2JQ UK
                [3 ]Present Address: Curtis Analytics Ltd, Daniel Hall Building, Rothamsted RoCRE, Harpenden, AL5 2JQ UK
                [4 ]Present Address: The European Bioinformatics Institute (EMBL-EBI), Wellcome Genome Campus, Hinxton, Cambridgeshire, CB10 1SD UK
                Author information
                http://orcid.org/0000-0001-6488-2530
                Article
                5991
                10.1186/s12864-019-5991-8
                6676566
                31370780
                27210170-a3c1-4ba5-a0d6-f7cba0377808
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 1 May 2019
                : 23 July 2019
                Funding
                Funded by: Biotechnology and Biological Sciences Research Council
                Award ID: BB/I020918/1
                Award ID: SWBio iCASE DTP Studentship
                Award ID: BB/P016855/1
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Genetics
                asparagine synthetase,amino acid metabolism,acrylamide,bzip,crop composition,food safety,rna-seq,sulphur,triticum aestivum,wheat

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