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Systems-Level Analysis of Nitrogen Starvation—Induced Modifications of Carbon Metabolism in a Chlamydomonas reinhardtii Starchless Mutant
To understand the molecular basis underlying increased triacylglycerol (TAG) accumulation in starchless (sta) Chlamydomonas reinhardtii mutants, we undertook comparative time-course transcriptomics of strains CC-4348 (sta6 mutant), CC-4349, a cell wall—deficient (cw) strain purported to represent th...
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Published in: | The Plant cell 2013-11, Vol.25 (11), p.4305-4323 |
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creator | Blaby, Ian K. Glaesener, Anne G. Mettler, Tabea Gibbon, Sorel T. Fitz Gallaher, Sean D. Liu, Bensheng Boyle, Nanette R. Kropat, Janette Stitt, Mark Johnson, Shannon Benning, Christoph Pellegrini, Matteo Casero, David Merchant, Sabeeha S. |
description | To understand the molecular basis underlying increased triacylglycerol (TAG) accumulation in starchless (sta) Chlamydomonas reinhardtii mutants, we undertook comparative time-course transcriptomics of strains CC-4348 (sta6 mutant), CC-4349, a cell wall—deficient (cw) strain purported to represent the parental STA6 strain, and three independent STA6 strains generated by complementation of sta6 (CC-4565/STA6-C2, CC-4566/STA6-C4, and CC-4567/STA6-C6) in the context of N deprivation. Despite N starvation—induced dramatic remodeling of the transcriptome, there were relatively few differences (5 × 10 2 ) observed between sta6 and STA6, the most dramatic of which were increased abundance of transcripts encoding key regulated or rate-limiting steps in central carbon metabolism, specifically isocitrate lyase, malate synthase, transaldolase, fructose bisphosphatase and phosphoenolpyruvate carboxykinase (encoded by ICL1, MAS1, TAL1, FBP1, and PCK1 respectively), suggestive of increased carbon movement toward hexose-phosphate in sta6 by upregulation of the glyoxylate pathway and gluconeogenesis. Enzyme assays validated the increase in isocitrate lyase and malate synthase activities. Targeted metabolite analysis indicated increased succinate, malate, and Glc-6-P and decreased Fru-1,6-bisphosphate, illustrating the effect of these changes. Comparisons of independent data sets in multiple strains allowed the delineation of a sequence of events in the global N starvation response in C. reinhardtii, starting within minutes with the upregulation of alternative N assimilation routes and carbohydrate synthesis and subsequently a more gradual upregulation of genes encoding enzymes of TAG synthesis. Finally, genome resequencing analysis indicated that (1) the deletion in sta6 extends into the neighboring gene encoding respiratory burst oxidase, and (2) a commonly used STA6 strain (CC-4349) as well as the sequenced reference (CC-503) are not congenic with respect to sta6 (CC-4348), underscoring the importance of using complemented strains for more rigorous assignment of phenotype to genotype. |
doi_str_mv | 10.1105/tpc.113.117580 |
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Fitz ; Gallaher, Sean D. ; Liu, Bensheng ; Boyle, Nanette R. ; Kropat, Janette ; Stitt, Mark ; Johnson, Shannon ; Benning, Christoph ; Pellegrini, Matteo ; Casero, David ; Merchant, Sabeeha S.</creator><creatorcontrib>Blaby, Ian K. ; Glaesener, Anne G. ; Mettler, Tabea ; Gibbon, Sorel T. Fitz ; Gallaher, Sean D. ; Liu, Bensheng ; Boyle, Nanette R. ; Kropat, Janette ; Stitt, Mark ; Johnson, Shannon ; Benning, Christoph ; Pellegrini, Matteo ; Casero, David ; Merchant, Sabeeha S.</creatorcontrib><description>To understand the molecular basis underlying increased triacylglycerol (TAG) accumulation in starchless (sta) Chlamydomonas reinhardtii mutants, we undertook comparative time-course transcriptomics of strains CC-4348 (sta6 mutant), CC-4349, a cell wall—deficient (cw) strain purported to represent the parental STA6 strain, and three independent STA6 strains generated by complementation of sta6 (CC-4565/STA6-C2, CC-4566/STA6-C4, and CC-4567/STA6-C6) in the context of N deprivation. Despite N starvation—induced dramatic remodeling of the transcriptome, there were relatively few differences (5 × 10 2 ) observed between sta6 and STA6, the most dramatic of which were increased abundance of transcripts encoding key regulated or rate-limiting steps in central carbon metabolism, specifically isocitrate lyase, malate synthase, transaldolase, fructose bisphosphatase and phosphoenolpyruvate carboxykinase (encoded by ICL1, MAS1, TAL1, FBP1, and PCK1 respectively), suggestive of increased carbon movement toward hexose-phosphate in sta6 by upregulation of the glyoxylate pathway and gluconeogenesis. Enzyme assays validated the increase in isocitrate lyase and malate synthase activities. Targeted metabolite analysis indicated increased succinate, malate, and Glc-6-P and decreased Fru-1,6-bisphosphate, illustrating the effect of these changes. Comparisons of independent data sets in multiple strains allowed the delineation of a sequence of events in the global N starvation response in C. reinhardtii, starting within minutes with the upregulation of alternative N assimilation routes and carbohydrate synthesis and subsequently a more gradual upregulation of genes encoding enzymes of TAG synthesis. Finally, genome resequencing analysis indicated that (1) the deletion in sta6 extends into the neighboring gene encoding respiratory burst oxidase, and (2) a commonly used STA6 strain (CC-4349) as well as the sequenced reference (CC-503) are not congenic with respect to sta6 (CC-4348), underscoring the importance of using complemented strains for more rigorous assignment of phenotype to genotype.</description><identifier>ISSN: 1040-4651</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1105/tpc.113.117580</identifier><identifier>PMID: 24280389</identifier><language>eng</language><publisher>United States: American Society of Plant Biologists</publisher><subject>Acetates ; Acetates - metabolism ; Carbohydrate Metabolism ; Carbon - metabolism ; Cell Wall - genetics ; Cell Wall - metabolism ; Chlamydomonas reinhardtii - genetics ; Chlamydomonas reinhardtii - metabolism ; Datasets ; Enzymes ; Enzymes - genetics ; Enzymes - metabolism ; Genes ; Genome, Plant ; Genomes ; Large-Scale Biology ; LARGE-SCALE BIOLOGY ARTICLE ; Lipid metabolism ; Lipids ; Messenger RNA ; Molecular Sequence Data ; Mutation ; Nitrogen - metabolism ; Plant cells ; Polymorphism, Single Nucleotide ; Reproducibility of Results ; Starch - genetics ; Starch - metabolism ; Starches ; Transcriptome</subject><ispartof>The Plant cell, 2013-11, Vol.25 (11), p.4305-4323</ispartof><rights>2013 American Society of Plant Biologists</rights><rights>2013 American Society of Plant Biologists. All rights reserved. 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c412t-d8ce7a764dc11c1bbdf88cecf2128e4647ece7f2bef4da6cc3c4b96512f2b7f73</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/23598474$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/23598474$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,885,27924,27925,58238,58471</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24280389$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Blaby, Ian K.</creatorcontrib><creatorcontrib>Glaesener, Anne G.</creatorcontrib><creatorcontrib>Mettler, Tabea</creatorcontrib><creatorcontrib>Gibbon, Sorel T. Fitz</creatorcontrib><creatorcontrib>Gallaher, Sean D.</creatorcontrib><creatorcontrib>Liu, Bensheng</creatorcontrib><creatorcontrib>Boyle, Nanette R.</creatorcontrib><creatorcontrib>Kropat, Janette</creatorcontrib><creatorcontrib>Stitt, Mark</creatorcontrib><creatorcontrib>Johnson, Shannon</creatorcontrib><creatorcontrib>Benning, Christoph</creatorcontrib><creatorcontrib>Pellegrini, Matteo</creatorcontrib><creatorcontrib>Casero, David</creatorcontrib><creatorcontrib>Merchant, Sabeeha S.</creatorcontrib><title>Systems-Level Analysis of Nitrogen Starvation—Induced Modifications of Carbon Metabolism in a Chlamydomonas reinhardtii Starchless Mutant</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>To understand the molecular basis underlying increased triacylglycerol (TAG) accumulation in starchless (sta) Chlamydomonas reinhardtii mutants, we undertook comparative time-course transcriptomics of strains CC-4348 (sta6 mutant), CC-4349, a cell wall—deficient (cw) strain purported to represent the parental STA6 strain, and three independent STA6 strains generated by complementation of sta6 (CC-4565/STA6-C2, CC-4566/STA6-C4, and CC-4567/STA6-C6) in the context of N deprivation. Despite N starvation—induced dramatic remodeling of the transcriptome, there were relatively few differences (5 × 10 2 ) observed between sta6 and STA6, the most dramatic of which were increased abundance of transcripts encoding key regulated or rate-limiting steps in central carbon metabolism, specifically isocitrate lyase, malate synthase, transaldolase, fructose bisphosphatase and phosphoenolpyruvate carboxykinase (encoded by ICL1, MAS1, TAL1, FBP1, and PCK1 respectively), suggestive of increased carbon movement toward hexose-phosphate in sta6 by upregulation of the glyoxylate pathway and gluconeogenesis. Enzyme assays validated the increase in isocitrate lyase and malate synthase activities. Targeted metabolite analysis indicated increased succinate, malate, and Glc-6-P and decreased Fru-1,6-bisphosphate, illustrating the effect of these changes. 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Despite N starvation—induced dramatic remodeling of the transcriptome, there were relatively few differences (5 × 10 2 ) observed between sta6 and STA6, the most dramatic of which were increased abundance of transcripts encoding key regulated or rate-limiting steps in central carbon metabolism, specifically isocitrate lyase, malate synthase, transaldolase, fructose bisphosphatase and phosphoenolpyruvate carboxykinase (encoded by ICL1, MAS1, TAL1, FBP1, and PCK1 respectively), suggestive of increased carbon movement toward hexose-phosphate in sta6 by upregulation of the glyoxylate pathway and gluconeogenesis. Enzyme assays validated the increase in isocitrate lyase and malate synthase activities. Targeted metabolite analysis indicated increased succinate, malate, and Glc-6-P and decreased Fru-1,6-bisphosphate, illustrating the effect of these changes. Comparisons of independent data sets in multiple strains allowed the delineation of a sequence of events in the global N starvation response in C. reinhardtii, starting within minutes with the upregulation of alternative N assimilation routes and carbohydrate synthesis and subsequently a more gradual upregulation of genes encoding enzymes of TAG synthesis. Finally, genome resequencing analysis indicated that (1) the deletion in sta6 extends into the neighboring gene encoding respiratory burst oxidase, and (2) a commonly used STA6 strain (CC-4349) as well as the sequenced reference (CC-503) are not congenic with respect to sta6 (CC-4348), underscoring the importance of using complemented strains for more rigorous assignment of phenotype to genotype.</abstract><cop>United States</cop><pub>American Society of Plant Biologists</pub><pmid>24280389</pmid><doi>10.1105/tpc.113.117580</doi><tpages>19</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Acetates Acetates - metabolism Carbohydrate Metabolism Carbon - metabolism Cell Wall - genetics Cell Wall - metabolism Chlamydomonas reinhardtii - genetics Chlamydomonas reinhardtii - metabolism Datasets Enzymes Enzymes - genetics Enzymes - metabolism Genes Genome, Plant Genomes Large-Scale Biology LARGE-SCALE BIOLOGY ARTICLE Lipid metabolism Lipids Messenger RNA Molecular Sequence Data Mutation Nitrogen - metabolism Plant cells Polymorphism, Single Nucleotide Reproducibility of Results Starch - genetics Starch - metabolism Starches Transcriptome |
title | Systems-Level Analysis of Nitrogen Starvation—Induced Modifications of Carbon Metabolism in a Chlamydomonas reinhardtii Starchless Mutant |
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