The synergistic effects of TaAGP.L-B1 and TaSSIVb-D mutations in wheat lead to alterations of gene expression patterns and starch content in grain development

Starch is synthesized from a series of reactions catalyzed by enzymes. ADP-glucose pyrophosphorylase (AGPase) initiates the synthesis pathway and synthesizes ADP-glucose, the substrate of starch synthase (SS), of which SSIV is an isoform. Mutations of the AGPase subunit and SSIV-coding genes affect...

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Veröffentlicht in:PloS one 2019-10, Vol.14 (10), p.e0223783
Hauptverfasser: Zhang, Shunlin, Guo, Huijun, Irshad, Ahsan, Xie, Yongdun, Zhao, Linshu, Xiong, Hongchun, Gu, Jiayu, Zhao, Shirong, Ding, Yuping, Liu, Luxiang
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container_issue 10
container_start_page e0223783
container_title PloS one
container_volume 14
creator Zhang, Shunlin
Guo, Huijun
Irshad, Ahsan
Xie, Yongdun
Zhao, Linshu
Xiong, Hongchun
Gu, Jiayu
Zhao, Shirong
Ding, Yuping
Liu, Luxiang
description Starch is synthesized from a series of reactions catalyzed by enzymes. ADP-glucose pyrophosphorylase (AGPase) initiates the synthesis pathway and synthesizes ADP-glucose, the substrate of starch synthase (SS), of which SSIV is an isoform. Mutations of the AGPase subunit and SSIV-coding genes affect starch content and cause variation in the number of granules. Here, we pyramided the functional mutation alleles of the AGPase subunit gene TaAGP.L-B1 and the SSIV-coding gene TaSSIVb-D to elucidate their synergistic effects on other key starch biosynthesis genes and their impact on starch content. Both the TaAGP.L-B1 and TaSSIVb-D genes were expressed in wheat grain development, and the expression level of TaAGP.L-B1 was higher than that of TaSSIVb-D. The TaAGP.L-B1 gene was downregulated in the agp.L-B1 single and agp.L-B1/ssIV-D double mutants at 12 to 18 days after flowering (DAF). TaSSIVb-D expression was significantly reduced at 6 DAF in both ssIV-D single and double mutants. In the agp.L-B1/ssIV-D double mutant, TaGBSSII was upregulated, while TaAGPSS, TaSSI, and TaSBEII were downregulated. Under the interaction of these genes, the total starch and amylopectin contents were significantly decreased in agp.L-B1 and agp.L-B1/ssIV-D mutants. The results suggested that the mutations of TaAGP.L-B1 and TaSSIVb-D genes resulted in variation in the expression patterns of the other four starch synthetic genes and led to a reduction in starch and amylopectin contents. These mutants could be used further as germplasm for resistant starch analysis.
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ADP-glucose pyrophosphorylase (AGPase) initiates the synthesis pathway and synthesizes ADP-glucose, the substrate of starch synthase (SS), of which SSIV is an isoform. Mutations of the AGPase subunit and SSIV-coding genes affect starch content and cause variation in the number of granules. Here, we pyramided the functional mutation alleles of the AGPase subunit gene TaAGP.L-B1 and the SSIV-coding gene TaSSIVb-D to elucidate their synergistic effects on other key starch biosynthesis genes and their impact on starch content. Both the TaAGP.L-B1 and TaSSIVb-D genes were expressed in wheat grain development, and the expression level of TaAGP.L-B1 was higher than that of TaSSIVb-D. The TaAGP.L-B1 gene was downregulated in the agp.L-B1 single and agp.L-B1/ssIV-D double mutants at 12 to 18 days after flowering (DAF). TaSSIVb-D expression was significantly reduced at 6 DAF in both ssIV-D single and double mutants. In the agp.L-B1/ssIV-D double mutant, TaGBSSII was upregulated, while TaAGPSS, TaSSI, and TaSBEII were downregulated. Under the interaction of these genes, the total starch and amylopectin contents were significantly decreased in agp.L-B1 and agp.L-B1/ssIV-D mutants. The results suggested that the mutations of TaAGP.L-B1 and TaSSIVb-D genes resulted in variation in the expression patterns of the other four starch synthetic genes and led to a reduction in starch and amylopectin contents. These mutants could be used further as germplasm for resistant starch analysis.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0223783</identifier><identifier>PMID: 31603940</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adenosine diphosphate ; Alleles ; Amylopectin ; Amylopectin - metabolism ; B1 gene ; Binding sites ; Biology and Life Sciences ; Biosynthesis ; Biosynthetic Pathways ; Chemical reactions ; Crop science ; Edible Grain - genetics ; Edible Grain - growth &amp; development ; Edible Grain - metabolism ; Engineering ; Engineering and Technology ; Enzymes ; Flowering ; Gene expression ; Gene Expression Profiling ; Gene Expression Regulation, Developmental ; Gene Expression Regulation, Plant ; Gene mutation ; Genes ; Genetic aspects ; Genomes ; Genomics ; Germplasm ; Glucose ; Glucose-1-Phosphate Adenylyltransferase - genetics ; Glucose-1-Phosphate Adenylyltransferase - metabolism ; Grain ; Laboratories ; Metabolism ; Mutagenesis ; Mutants ; Mutation ; Physical Sciences ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Rice ; Starch ; Starch - biosynthesis ; Starch synthase ; Starch Synthase - genetics ; Starch Synthase - metabolism ; Substrates ; Synergistic effect ; Triticum - genetics ; Triticum - growth &amp; development ; Triticum - metabolism ; Wheat</subject><ispartof>PloS one, 2019-10, Vol.14 (10), p.e0223783</ispartof><rights>COPYRIGHT 2019 Public Library of Science</rights><rights>2019 Zhang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2019 Zhang et al 2019 Zhang et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-feb04f71b6c3844b0406e0494bdd3c7c97a0a2724f2fc999a85c41c15e0620853</citedby><cites>FETCH-LOGICAL-c692t-feb04f71b6c3844b0406e0494bdd3c7c97a0a2724f2fc999a85c41c15e0620853</cites><orcidid>0000-0001-6912-1482</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6788705/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6788705/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31603940$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Shunlin</creatorcontrib><creatorcontrib>Guo, Huijun</creatorcontrib><creatorcontrib>Irshad, Ahsan</creatorcontrib><creatorcontrib>Xie, Yongdun</creatorcontrib><creatorcontrib>Zhao, Linshu</creatorcontrib><creatorcontrib>Xiong, Hongchun</creatorcontrib><creatorcontrib>Gu, Jiayu</creatorcontrib><creatorcontrib>Zhao, Shirong</creatorcontrib><creatorcontrib>Ding, Yuping</creatorcontrib><creatorcontrib>Liu, Luxiang</creatorcontrib><title>The synergistic effects of TaAGP.L-B1 and TaSSIVb-D mutations in wheat lead to alterations of gene expression patterns and starch content in grain development</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Starch is synthesized from a series of reactions catalyzed by enzymes. ADP-glucose pyrophosphorylase (AGPase) initiates the synthesis pathway and synthesizes ADP-glucose, the substrate of starch synthase (SS), of which SSIV is an isoform. Mutations of the AGPase subunit and SSIV-coding genes affect starch content and cause variation in the number of granules. Here, we pyramided the functional mutation alleles of the AGPase subunit gene TaAGP.L-B1 and the SSIV-coding gene TaSSIVb-D to elucidate their synergistic effects on other key starch biosynthesis genes and their impact on starch content. Both the TaAGP.L-B1 and TaSSIVb-D genes were expressed in wheat grain development, and the expression level of TaAGP.L-B1 was higher than that of TaSSIVb-D. The TaAGP.L-B1 gene was downregulated in the agp.L-B1 single and agp.L-B1/ssIV-D double mutants at 12 to 18 days after flowering (DAF). TaSSIVb-D expression was significantly reduced at 6 DAF in both ssIV-D single and double mutants. In the agp.L-B1/ssIV-D double mutant, TaGBSSII was upregulated, while TaAGPSS, TaSSI, and TaSBEII were downregulated. Under the interaction of these genes, the total starch and amylopectin contents were significantly decreased in agp.L-B1 and agp.L-B1/ssIV-D mutants. The results suggested that the mutations of TaAGP.L-B1 and TaSSIVb-D genes resulted in variation in the expression patterns of the other four starch synthetic genes and led to a reduction in starch and amylopectin contents. These mutants could be used further as germplasm for resistant starch analysis.</description><subject>Adenosine diphosphate</subject><subject>Alleles</subject><subject>Amylopectin</subject><subject>Amylopectin - metabolism</subject><subject>B1 gene</subject><subject>Binding sites</subject><subject>Biology and Life Sciences</subject><subject>Biosynthesis</subject><subject>Biosynthetic Pathways</subject><subject>Chemical reactions</subject><subject>Crop science</subject><subject>Edible Grain - genetics</subject><subject>Edible Grain - growth &amp; development</subject><subject>Edible Grain - metabolism</subject><subject>Engineering</subject><subject>Engineering and Technology</subject><subject>Enzymes</subject><subject>Flowering</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene mutation</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Germplasm</subject><subject>Glucose</subject><subject>Glucose-1-Phosphate Adenylyltransferase - genetics</subject><subject>Glucose-1-Phosphate Adenylyltransferase - metabolism</subject><subject>Grain</subject><subject>Laboratories</subject><subject>Metabolism</subject><subject>Mutagenesis</subject><subject>Mutants</subject><subject>Mutation</subject><subject>Physical Sciences</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Rice</subject><subject>Starch</subject><subject>Starch - biosynthesis</subject><subject>Starch synthase</subject><subject>Starch Synthase - genetics</subject><subject>Starch Synthase - metabolism</subject><subject>Substrates</subject><subject>Synergistic effect</subject><subject>Triticum - genetics</subject><subject>Triticum - growth &amp; development</subject><subject>Triticum - metabolism</subject><subject>Wheat</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNk12L1DAUhoso7rr6D0QDguBFx3z160YYV10HBlaccW9Dmp50unSamqTr7p_xt5qZ6S5TUJBC25zznLenb3Ki6CXBM8Iy8v7aDLaT7aw3HcwwpSzL2aPolBSMxinF7PHR-0n0zLlrjBOWp-nT6ISRFLOC49Po93oDyN11YOvG-UYh0BqUd8hotJbzi2-zZfyRINlVYblaLa7K-BPaDl76xnQONR36tQHpUQuyQt4g2XqwYzJI1NABgtvegnMhhnrpQz7kdoLOS6s2SJnOQ-d3WrWV4V7BDbSm34bg8-iJlq2DF-PzLPrx5fP6_Gu8vLxYnM-XsUoL6mMNJeY6I2WqWM55WOAUMC94WVVMZarIJJY0o1xTrYqikHmiOFEkARzsyRN2Fr0-6PatcWK01gnKMCc445gFYnEgKiOvRW-brbR3wshG7APG1kLaYGALoiJFWQKhJE8lLzNSJFRpUvAk9EJzVgatD-PXhnILlQo_amU7EZ1mumYjanMj0izPM7xr980oYM3PAZz_R8sjVcvQVdNpE8TUtnFKzFNMOc3DAQnU7C9UuCrYNmFvQDchPil4NynY79-tr-XgnFisvv8_e3k1Zd8eseFUtX7jTDvsD9MU5AdQWeOcBf3gHMFiNxv3bojdbIhxNkLZq2PXH4ruh4H9ASRKChA</recordid><startdate>20191011</startdate><enddate>20191011</enddate><creator>Zhang, Shunlin</creator><creator>Guo, Huijun</creator><creator>Irshad, Ahsan</creator><creator>Xie, Yongdun</creator><creator>Zhao, Linshu</creator><creator>Xiong, Hongchun</creator><creator>Gu, Jiayu</creator><creator>Zhao, Shirong</creator><creator>Ding, Yuping</creator><creator>Liu, Luxiang</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-6912-1482</orcidid></search><sort><creationdate>20191011</creationdate><title>The synergistic effects of TaAGP.L-B1 and TaSSIVb-D mutations in wheat lead to alterations of gene expression patterns and starch content in grain development</title><author>Zhang, Shunlin ; Guo, Huijun ; Irshad, Ahsan ; Xie, Yongdun ; Zhao, Linshu ; Xiong, Hongchun ; Gu, Jiayu ; Zhao, Shirong ; Ding, Yuping ; Liu, Luxiang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-feb04f71b6c3844b0406e0494bdd3c7c97a0a2724f2fc999a85c41c15e0620853</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Adenosine diphosphate</topic><topic>Alleles</topic><topic>Amylopectin</topic><topic>Amylopectin - metabolism</topic><topic>B1 gene</topic><topic>Binding sites</topic><topic>Biology and Life Sciences</topic><topic>Biosynthesis</topic><topic>Biosynthetic Pathways</topic><topic>Chemical reactions</topic><topic>Crop science</topic><topic>Edible Grain - genetics</topic><topic>Edible Grain - growth &amp; development</topic><topic>Edible Grain - metabolism</topic><topic>Engineering</topic><topic>Engineering and Technology</topic><topic>Enzymes</topic><topic>Flowering</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene mutation</topic><topic>Genes</topic><topic>Genetic aspects</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Germplasm</topic><topic>Glucose</topic><topic>Glucose-1-Phosphate Adenylyltransferase - genetics</topic><topic>Glucose-1-Phosphate Adenylyltransferase - metabolism</topic><topic>Grain</topic><topic>Laboratories</topic><topic>Metabolism</topic><topic>Mutagenesis</topic><topic>Mutants</topic><topic>Mutation</topic><topic>Physical Sciences</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Rice</topic><topic>Starch</topic><topic>Starch - biosynthesis</topic><topic>Starch synthase</topic><topic>Starch Synthase - genetics</topic><topic>Starch Synthase - metabolism</topic><topic>Substrates</topic><topic>Synergistic effect</topic><topic>Triticum - genetics</topic><topic>Triticum - growth &amp; 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Allied Health Database (Alumni Edition)</collection><collection>Meteorological &amp; Geoastrophysical Abstracts - Academic</collection><collection>ProQuest Engineering Collection</collection><collection>Biological Sciences</collection><collection>Agriculture Science Database</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>ProQuest Engineering Database</collection><collection>Nursing &amp; Allied Health Premium</collection><collection>ProQuest advanced technologies &amp; aerospace journals</collection><collection>ProQuest Advanced Technologies &amp; Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content (ProQuest)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Engineering collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Shunlin</au><au>Guo, Huijun</au><au>Irshad, Ahsan</au><au>Xie, Yongdun</au><au>Zhao, Linshu</au><au>Xiong, Hongchun</au><au>Gu, Jiayu</au><au>Zhao, Shirong</au><au>Ding, Yuping</au><au>Liu, Luxiang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The synergistic effects of TaAGP.L-B1 and TaSSIVb-D mutations in wheat lead to alterations of gene expression patterns and starch content in grain development</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2019-10-11</date><risdate>2019</risdate><volume>14</volume><issue>10</issue><spage>e0223783</spage><pages>e0223783-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Starch is synthesized from a series of reactions catalyzed by enzymes. ADP-glucose pyrophosphorylase (AGPase) initiates the synthesis pathway and synthesizes ADP-glucose, the substrate of starch synthase (SS), of which SSIV is an isoform. Mutations of the AGPase subunit and SSIV-coding genes affect starch content and cause variation in the number of granules. Here, we pyramided the functional mutation alleles of the AGPase subunit gene TaAGP.L-B1 and the SSIV-coding gene TaSSIVb-D to elucidate their synergistic effects on other key starch biosynthesis genes and their impact on starch content. Both the TaAGP.L-B1 and TaSSIVb-D genes were expressed in wheat grain development, and the expression level of TaAGP.L-B1 was higher than that of TaSSIVb-D. The TaAGP.L-B1 gene was downregulated in the agp.L-B1 single and agp.L-B1/ssIV-D double mutants at 12 to 18 days after flowering (DAF). TaSSIVb-D expression was significantly reduced at 6 DAF in both ssIV-D single and double mutants. In the agp.L-B1/ssIV-D double mutant, TaGBSSII was upregulated, while TaAGPSS, TaSSI, and TaSBEII were downregulated. Under the interaction of these genes, the total starch and amylopectin contents were significantly decreased in agp.L-B1 and agp.L-B1/ssIV-D mutants. The results suggested that the mutations of TaAGP.L-B1 and TaSSIVb-D genes resulted in variation in the expression patterns of the other four starch synthetic genes and led to a reduction in starch and amylopectin contents. These mutants could be used further as germplasm for resistant starch analysis.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>31603940</pmid><doi>10.1371/journal.pone.0223783</doi><tpages>e0223783</tpages><orcidid>https://orcid.org/0000-0001-6912-1482</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1932-6203
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issn 1932-6203
1932-6203
language eng
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source MEDLINE; Public Library of Science; Full-Text Journals in Chemistry (Open access); PubMed Central; Directory of Open Access Journals; EZB Electronic Journals Library
subjects Adenosine diphosphate
Alleles
Amylopectin
Amylopectin - metabolism
B1 gene
Binding sites
Biology and Life Sciences
Biosynthesis
Biosynthetic Pathways
Chemical reactions
Crop science
Edible Grain - genetics
Edible Grain - growth & development
Edible Grain - metabolism
Engineering
Engineering and Technology
Enzymes
Flowering
Gene expression
Gene Expression Profiling
Gene Expression Regulation, Developmental
Gene Expression Regulation, Plant
Gene mutation
Genes
Genetic aspects
Genomes
Genomics
Germplasm
Glucose
Glucose-1-Phosphate Adenylyltransferase - genetics
Glucose-1-Phosphate Adenylyltransferase - metabolism
Grain
Laboratories
Metabolism
Mutagenesis
Mutants
Mutation
Physical Sciences
Plant Proteins - genetics
Plant Proteins - metabolism
Rice
Starch
Starch - biosynthesis
Starch synthase
Starch Synthase - genetics
Starch Synthase - metabolism
Substrates
Synergistic effect
Triticum - genetics
Triticum - growth & development
Triticum - metabolism
Wheat
title The synergistic effects of TaAGP.L-B1 and TaSSIVb-D mutations in wheat lead to alterations of gene expression patterns and starch content in grain development
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