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Arabidopsis plastidial folylpolyglutamate synthetase is required for seed reserve accumulation and seedling establishment in darkness
Interactions among metabolic pathways are important in plant biology. At present, not much is known about how folate metabolism affects other metabolic pathways in plants. Here we report a T-DNA insertion mutant (atdfb-3) of the plastidial folylpolyglutamate synthetase gene (AtDFB) was defective in...
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Published in: | PloS one 2014-07, Vol.9 (7), p.e101905 |
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description | Interactions among metabolic pathways are important in plant biology. At present, not much is known about how folate metabolism affects other metabolic pathways in plants. Here we report a T-DNA insertion mutant (atdfb-3) of the plastidial folylpolyglutamate synthetase gene (AtDFB) was defective in seed reserves and skotomorphogenesis. Lower carbon (C) and higher nitrogen (N) content in the mutant seeds than that of the wild type were indicative of an altered C and N partitioning capacity. Higher levels of organic acids and sugars were detected in the mutant seeds compared with the wild type. Further analysis revealed that atdfb-3 seeds contained less total amino acids and individual Asn and Glu as well as NO3-. These results indicate significant changes in seed storage in the mutant. Defects in hypocotyl elongation were observed in atdfb-3 in darkness under sufficient NO3- conditions, and further enhanced under NO3- limited conditions. The strong expression of AtDFB in cotyledons and hypocotyl during early developmental stage was consistent with the mutant sensitivity to limited NO3- during a narrow developmental window. Exogenous 5-formyl-tetrahydrofolate completely restored the hypocotyl length in atdfb-3 seedlings with NO3- as the sole N source. Further study demonstrated that folate profiling and N metabolism were perturbed in atdfb-3 etiolated seedlings. The activity of enzymes involved in N reduction and assimilation was altered in atdfb-3. Taken together, these results indicate that AtDFB is required for seed reserves, hypocotyl elongation and N metabolism in darkness, providing novel insights into potential associations of folate metabolism with seed reserve accumulation, N metabolism and hypocotyl development in Arabidopsis. |
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At present, not much is known about how folate metabolism affects other metabolic pathways in plants. Here we report a T-DNA insertion mutant (atdfb-3) of the plastidial folylpolyglutamate synthetase gene (AtDFB) was defective in seed reserves and skotomorphogenesis. Lower carbon (C) and higher nitrogen (N) content in the mutant seeds than that of the wild type were indicative of an altered C and N partitioning capacity. Higher levels of organic acids and sugars were detected in the mutant seeds compared with the wild type. Further analysis revealed that atdfb-3 seeds contained less total amino acids and individual Asn and Glu as well as NO3-. These results indicate significant changes in seed storage in the mutant. Defects in hypocotyl elongation were observed in atdfb-3 in darkness under sufficient NO3- conditions, and further enhanced under NO3- limited conditions. The strong expression of AtDFB in cotyledons and hypocotyl during early developmental stage was consistent with the mutant sensitivity to limited NO3- during a narrow developmental window. Exogenous 5-formyl-tetrahydrofolate completely restored the hypocotyl length in atdfb-3 seedlings with NO3- as the sole N source. Further study demonstrated that folate profiling and N metabolism were perturbed in atdfb-3 etiolated seedlings. The activity of enzymes involved in N reduction and assimilation was altered in atdfb-3. Taken together, these results indicate that AtDFB is required for seed reserves, hypocotyl elongation and N metabolism in darkness, providing novel insights into potential associations of folate metabolism with seed reserve accumulation, N metabolism and hypocotyl development in Arabidopsis.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0101905</identifier><identifier>PMID: 25000295</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Accumulation ; Amino acids ; Analysis ; Arabidopsis ; Arabidopsis - cytology ; Arabidopsis - enzymology ; Arabidopsis - genetics ; Arabidopsis - growth & development ; Arabidopsis thaliana ; Biology and Life Sciences ; Biosynthesis ; Biotechnology ; Cell division ; Cotyledons ; Darkness ; Deoxyribonucleic acid ; DNA ; DNA, Bacterial - genetics ; Elongation ; Enzymes ; Folic acid ; Folic Acid - metabolism ; Gene Expression Regulation, Plant - drug effects ; Gene Expression Regulation, Plant - radiation effects ; Genes ; Germination - drug effects ; Germination - radiation effects ; Hypocotyl - drug effects ; Hypocotyl - growth & development ; Hypocotyl - radiation effects ; Leucovorin - pharmacology ; Ligases ; Metabolic pathways ; Metabolism ; Metabolites ; Mutation ; Nitrates - metabolism ; Nitrogen ; Organ Size ; Organic acids ; Peptide Synthases - genetics ; Peptide Synthases - metabolism ; Physiological aspects ; Plant physiology ; Plant sciences ; Plastids - drug effects ; Plastids - enzymology ; Plastids - radiation effects ; Proteins ; Reserves ; Seedlings ; Seedlings - drug effects ; Seedlings - growth & development ; Seedlings - radiation effects ; Seeds ; Seeds - drug effects ; Seeds - growth & development ; Seeds - radiation effects ; Skotomorphogenesis ; Sugar ; T-DNA ; Tetrahydrofolic acid ; Toxicology ; Vitamin B</subject><ispartof>PloS one, 2014-07, Vol.9 (7), p.e101905</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 Meng 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>2014 Meng et al 2014 Meng et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-98c557f06bbb0db4e9f6ba581a5f4cdd4986de54abf418ce9915b37b169d00e73</citedby><cites>FETCH-LOGICAL-c692t-98c557f06bbb0db4e9f6ba581a5f4cdd4986de54abf418ce9915b37b169d00e73</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2013290287/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2013290287?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,725,778,782,883,25736,27907,27908,36995,44573,53774,53776,74877</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25000295$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Bassham, Diane</contributor><creatorcontrib>Meng, Hongyan</creatorcontrib><creatorcontrib>Jiang, Ling</creatorcontrib><creatorcontrib>Xu, Bosi</creatorcontrib><creatorcontrib>Guo, Wenzhu</creatorcontrib><creatorcontrib>Li, Jinglai</creatorcontrib><creatorcontrib>Zhu, Xiuqing</creatorcontrib><creatorcontrib>Qi, Xiaoquan</creatorcontrib><creatorcontrib>Duan, Lixin</creatorcontrib><creatorcontrib>Meng, Xianbin</creatorcontrib><creatorcontrib>Fan, Yunliu</creatorcontrib><creatorcontrib>Zhang, Chunyi</creatorcontrib><title>Arabidopsis plastidial folylpolyglutamate synthetase is required for seed reserve accumulation and seedling establishment in darkness</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Interactions among metabolic pathways are important in plant biology. At present, not much is known about how folate metabolism affects other metabolic pathways in plants. Here we report a T-DNA insertion mutant (atdfb-3) of the plastidial folylpolyglutamate synthetase gene (AtDFB) was defective in seed reserves and skotomorphogenesis. Lower carbon (C) and higher nitrogen (N) content in the mutant seeds than that of the wild type were indicative of an altered C and N partitioning capacity. Higher levels of organic acids and sugars were detected in the mutant seeds compared with the wild type. Further analysis revealed that atdfb-3 seeds contained less total amino acids and individual Asn and Glu as well as NO3-. These results indicate significant changes in seed storage in the mutant. Defects in hypocotyl elongation were observed in atdfb-3 in darkness under sufficient NO3- conditions, and further enhanced under NO3- limited conditions. The strong expression of AtDFB in cotyledons and hypocotyl during early developmental stage was consistent with the mutant sensitivity to limited NO3- during a narrow developmental window. Exogenous 5-formyl-tetrahydrofolate completely restored the hypocotyl length in atdfb-3 seedlings with NO3- as the sole N source. Further study demonstrated that folate profiling and N metabolism were perturbed in atdfb-3 etiolated seedlings. The activity of enzymes involved in N reduction and assimilation was altered in atdfb-3. Taken together, these results indicate that AtDFB is required for seed reserves, hypocotyl elongation and N metabolism in darkness, providing novel insights into potential associations of folate metabolism with seed reserve accumulation, N metabolism and hypocotyl development in Arabidopsis.</description><subject>Accumulation</subject><subject>Amino acids</subject><subject>Analysis</subject><subject>Arabidopsis</subject><subject>Arabidopsis - cytology</subject><subject>Arabidopsis - enzymology</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis thaliana</subject><subject>Biology and Life Sciences</subject><subject>Biosynthesis</subject><subject>Biotechnology</subject><subject>Cell division</subject><subject>Cotyledons</subject><subject>Darkness</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA, Bacterial - genetics</subject><subject>Elongation</subject><subject>Enzymes</subject><subject>Folic acid</subject><subject>Folic Acid - metabolism</subject><subject>Gene Expression Regulation, Plant - drug effects</subject><subject>Gene Expression Regulation, Plant - radiation effects</subject><subject>Genes</subject><subject>Germination - drug effects</subject><subject>Germination - radiation effects</subject><subject>Hypocotyl - drug effects</subject><subject>Hypocotyl - growth & development</subject><subject>Hypocotyl - radiation effects</subject><subject>Leucovorin - pharmacology</subject><subject>Ligases</subject><subject>Metabolic pathways</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Mutation</subject><subject>Nitrates - metabolism</subject><subject>Nitrogen</subject><subject>Organ Size</subject><subject>Organic acids</subject><subject>Peptide Synthases - genetics</subject><subject>Peptide Synthases - metabolism</subject><subject>Physiological aspects</subject><subject>Plant physiology</subject><subject>Plant sciences</subject><subject>Plastids - drug effects</subject><subject>Plastids - enzymology</subject><subject>Plastids - radiation effects</subject><subject>Proteins</subject><subject>Reserves</subject><subject>Seedlings</subject><subject>Seedlings - drug effects</subject><subject>Seedlings - growth & development</subject><subject>Seedlings - radiation effects</subject><subject>Seeds</subject><subject>Seeds - drug effects</subject><subject>Seeds - growth & development</subject><subject>Seeds - radiation effects</subject><subject>Skotomorphogenesis</subject><subject>Sugar</subject><subject>T-DNA</subject><subject>Tetrahydrofolic acid</subject><subject>Toxicology</subject><subject>Vitamin B</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqNk2trFDEUhgdRbK3-A9EBQfDDrsnc86WwFC8LhYK3r-EkOTObmplsk0xxf4D_22x3WnZAQQLJIXnOm-TlnCR5ScmS5jV9f21HN4BZbu2AS0IJZaR8lJxSlmeLKiP546P4JHnm_TUhZd5U1dPkJCsJIRkrT5PfKwdCK7v12qdbAz5opcGkrTU7s41TZ8YAPQRM_W4IGwzgMY2sw5tRO1SRdKnHGDj06G4xBSnHfjQQtB1SGNTdqdFDl6IPIIz2mx6HkOohVeB-Duj98-RJC8bji2k9S75__PDt4vPi8urT-mJ1uZAVy8KCNbIs65ZUQgiiRIGsrQSUDYWyLaRSBWsqhWUBoi1oI5ExWoq8FrRiihCs87Pk9UF3a6znk4OeZ4TmGSNZsyfWB0JZuOZbp3twO25B87sN6zoOLmhpkFNoshygyGpRFTVm8W7VVpUgEpFCIaLW-XTbKHpUMn7agZmJzk8GveGdveUFaYqG5VHgzSTg7M0Y3fvHkyeqg_gqPbQ2islee8lX0YY6itEyUsu_UHEo7LWMNdTquD9LeDdLiEzAX6GD0Xu-_vrl_9mrH3P27RG7QTBh422sslgufg4WB1A6673D9sE5Svi-Be7d4PsW4FMLxLRXx64_JN3XfP4HioIF0A</recordid><startdate>20140707</startdate><enddate>20140707</enddate><creator>Meng, Hongyan</creator><creator>Jiang, Ling</creator><creator>Xu, Bosi</creator><creator>Guo, Wenzhu</creator><creator>Li, Jinglai</creator><creator>Zhu, Xiuqing</creator><creator>Qi, Xiaoquan</creator><creator>Duan, Lixin</creator><creator>Meng, Xianbin</creator><creator>Fan, Yunliu</creator><creator>Zhang, Chunyi</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>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20140707</creationdate><title>Arabidopsis plastidial folylpolyglutamate synthetase is required for seed reserve accumulation and seedling establishment in darkness</title><author>Meng, Hongyan ; Jiang, Ling ; Xu, Bosi ; Guo, Wenzhu ; Li, Jinglai ; Zhu, Xiuqing ; Qi, Xiaoquan ; Duan, Lixin ; Meng, Xianbin ; Fan, Yunliu ; Zhang, Chunyi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-98c557f06bbb0db4e9f6ba581a5f4cdd4986de54abf418ce9915b37b169d00e73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Accumulation</topic><topic>Amino acids</topic><topic>Analysis</topic><topic>Arabidopsis</topic><topic>Arabidopsis - 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Academic</collection><collection>ProQuest Engineering Collection</collection><collection>Biological Sciences</collection><collection>Agriculture Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Meng, Hongyan</au><au>Jiang, Ling</au><au>Xu, Bosi</au><au>Guo, Wenzhu</au><au>Li, Jinglai</au><au>Zhu, Xiuqing</au><au>Qi, Xiaoquan</au><au>Duan, Lixin</au><au>Meng, Xianbin</au><au>Fan, Yunliu</au><au>Zhang, Chunyi</au><au>Bassham, Diane</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Arabidopsis plastidial folylpolyglutamate synthetase is required for seed reserve accumulation and seedling establishment in darkness</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2014-07-07</date><risdate>2014</risdate><volume>9</volume><issue>7</issue><spage>e101905</spage><pages>e101905-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Interactions among metabolic pathways are important in plant biology. At present, not much is known about how folate metabolism affects other metabolic pathways in plants. Here we report a T-DNA insertion mutant (atdfb-3) of the plastidial folylpolyglutamate synthetase gene (AtDFB) was defective in seed reserves and skotomorphogenesis. Lower carbon (C) and higher nitrogen (N) content in the mutant seeds than that of the wild type were indicative of an altered C and N partitioning capacity. Higher levels of organic acids and sugars were detected in the mutant seeds compared with the wild type. Further analysis revealed that atdfb-3 seeds contained less total amino acids and individual Asn and Glu as well as NO3-. These results indicate significant changes in seed storage in the mutant. Defects in hypocotyl elongation were observed in atdfb-3 in darkness under sufficient NO3- conditions, and further enhanced under NO3- limited conditions. The strong expression of AtDFB in cotyledons and hypocotyl during early developmental stage was consistent with the mutant sensitivity to limited NO3- during a narrow developmental window. Exogenous 5-formyl-tetrahydrofolate completely restored the hypocotyl length in atdfb-3 seedlings with NO3- as the sole N source. Further study demonstrated that folate profiling and N metabolism were perturbed in atdfb-3 etiolated seedlings. The activity of enzymes involved in N reduction and assimilation was altered in atdfb-3. Taken together, these results indicate that AtDFB is required for seed reserves, hypocotyl elongation and N metabolism in darkness, providing novel insights into potential associations of folate metabolism with seed reserve accumulation, N metabolism and hypocotyl development in Arabidopsis.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25000295</pmid><doi>10.1371/journal.pone.0101905</doi><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 1932-6203 |
ispartof | PloS one, 2014-07, Vol.9 (7), p.e101905 |
issn | 1932-6203 1932-6203 |
language | eng |
recordid | cdi_plos_journals_2013290287 |
source | Publicly Available Content Database; PubMed Central |
subjects | Accumulation Amino acids Analysis Arabidopsis Arabidopsis - cytology Arabidopsis - enzymology Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis thaliana Biology and Life Sciences Biosynthesis Biotechnology Cell division Cotyledons Darkness Deoxyribonucleic acid DNA DNA, Bacterial - genetics Elongation Enzymes Folic acid Folic Acid - metabolism Gene Expression Regulation, Plant - drug effects Gene Expression Regulation, Plant - radiation effects Genes Germination - drug effects Germination - radiation effects Hypocotyl - drug effects Hypocotyl - growth & development Hypocotyl - radiation effects Leucovorin - pharmacology Ligases Metabolic pathways Metabolism Metabolites Mutation Nitrates - metabolism Nitrogen Organ Size Organic acids Peptide Synthases - genetics Peptide Synthases - metabolism Physiological aspects Plant physiology Plant sciences Plastids - drug effects Plastids - enzymology Plastids - radiation effects Proteins Reserves Seedlings Seedlings - drug effects Seedlings - growth & development Seedlings - radiation effects Seeds Seeds - drug effects Seeds - growth & development Seeds - radiation effects Skotomorphogenesis Sugar T-DNA Tetrahydrofolic acid Toxicology Vitamin B |
title | Arabidopsis plastidial folylpolyglutamate synthetase is required for seed reserve accumulation and seedling establishment in darkness |
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