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Divisions of labor in the thiamin biosynthetic pathway among organs of maize

The B vitamin thiamin is essential for central metabolism in all cellular organisms including plants. While plants synthesize thiamin de novo, organs vary widely in their capacities for thiamin synthesis. We use a transcriptomics approach to appraise the distribution of de novo synthesis and thiamin...

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Autores principales: Guan, Jiahn-Chou, Hasnain, Ghulam, Garrett, Timothy J., Chase, Christine D., Gregory, Jesse, Hanson, Andrew D., McCarty, Donald R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4120688/
https://www.ncbi.nlm.nih.gov/pubmed/25136345
http://dx.doi.org/10.3389/fpls.2014.00370
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author Guan, Jiahn-Chou
Hasnain, Ghulam
Garrett, Timothy J.
Chase, Christine D.
Gregory, Jesse
Hanson, Andrew D.
McCarty, Donald R.
author_facet Guan, Jiahn-Chou
Hasnain, Ghulam
Garrett, Timothy J.
Chase, Christine D.
Gregory, Jesse
Hanson, Andrew D.
McCarty, Donald R.
author_sort Guan, Jiahn-Chou
collection PubMed
description The B vitamin thiamin is essential for central metabolism in all cellular organisms including plants. While plants synthesize thiamin de novo, organs vary widely in their capacities for thiamin synthesis. We use a transcriptomics approach to appraise the distribution of de novo synthesis and thiamin salvage pathways among organs of maize. We identify at least six developmental contexts in which metabolically active, non-photosynthetic organs exhibit low expression of one or both branches of the de novo thiamin biosynthetic pathway indicating a dependence on inter-cellular transport of thiamin and/or thiamin precursors. Neither the thiazole (THI4) nor pyrimidine (THIC) branches of the pathway are expressed in developing pollen implying a dependence on import of thiamin from surrounding floral and inflorescence organs. Consistent with that hypothesis, organs of the male inflorescence and flowers are shown to have high relative expression of the thiamin biosynthetic pathway and comparatively high thiamin contents. By contrast, divergent patterns of THIC and THI4 expression occur in the shoot apical meristem, embyro sac, embryo, endosperm, and root-tips suggesting that these sink organs acquire significant amounts of thiamin via salvage pathways. In the root and shoot meristems, expression of THIC in the absence of THI4 indicates a capacity for thiamin synthesis via salvage of thiazole, whereas the opposite pattern obtains in embryo and endosperm implying that seed storage organs are poised for pyrimidine salvage. Finally, stable isotope labeling experiments set an upper limit on the rate of de novo thiamin biosynthesis in maize leaf explants. Overall, the observed patterns of thiamin biosynthetic gene expression mirror the strategies for thiamin acquisition that have evolved in bacteria.
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spelling pubmed-41206882014-08-18 Divisions of labor in the thiamin biosynthetic pathway among organs of maize Guan, Jiahn-Chou Hasnain, Ghulam Garrett, Timothy J. Chase, Christine D. Gregory, Jesse Hanson, Andrew D. McCarty, Donald R. Front Plant Sci Plant Science The B vitamin thiamin is essential for central metabolism in all cellular organisms including plants. While plants synthesize thiamin de novo, organs vary widely in their capacities for thiamin synthesis. We use a transcriptomics approach to appraise the distribution of de novo synthesis and thiamin salvage pathways among organs of maize. We identify at least six developmental contexts in which metabolically active, non-photosynthetic organs exhibit low expression of one or both branches of the de novo thiamin biosynthetic pathway indicating a dependence on inter-cellular transport of thiamin and/or thiamin precursors. Neither the thiazole (THI4) nor pyrimidine (THIC) branches of the pathway are expressed in developing pollen implying a dependence on import of thiamin from surrounding floral and inflorescence organs. Consistent with that hypothesis, organs of the male inflorescence and flowers are shown to have high relative expression of the thiamin biosynthetic pathway and comparatively high thiamin contents. By contrast, divergent patterns of THIC and THI4 expression occur in the shoot apical meristem, embyro sac, embryo, endosperm, and root-tips suggesting that these sink organs acquire significant amounts of thiamin via salvage pathways. In the root and shoot meristems, expression of THIC in the absence of THI4 indicates a capacity for thiamin synthesis via salvage of thiazole, whereas the opposite pattern obtains in embryo and endosperm implying that seed storage organs are poised for pyrimidine salvage. Finally, stable isotope labeling experiments set an upper limit on the rate of de novo thiamin biosynthesis in maize leaf explants. Overall, the observed patterns of thiamin biosynthetic gene expression mirror the strategies for thiamin acquisition that have evolved in bacteria. Frontiers Media S.A. 2014-08-04 /pmc/articles/PMC4120688/ /pubmed/25136345 http://dx.doi.org/10.3389/fpls.2014.00370 Text en Copyright © 2014 Guan, Hasnain, Garrett, Chase, Gregory, Hanson and McCarty. http://creativecommons.org/licenses/by/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Guan, Jiahn-Chou
Hasnain, Ghulam
Garrett, Timothy J.
Chase, Christine D.
Gregory, Jesse
Hanson, Andrew D.
McCarty, Donald R.
Divisions of labor in the thiamin biosynthetic pathway among organs of maize
title Divisions of labor in the thiamin biosynthetic pathway among organs of maize
title_full Divisions of labor in the thiamin biosynthetic pathway among organs of maize
title_fullStr Divisions of labor in the thiamin biosynthetic pathway among organs of maize
title_full_unstemmed Divisions of labor in the thiamin biosynthetic pathway among organs of maize
title_short Divisions of labor in the thiamin biosynthetic pathway among organs of maize
title_sort divisions of labor in the thiamin biosynthetic pathway among organs of maize
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4120688/
https://www.ncbi.nlm.nih.gov/pubmed/25136345
http://dx.doi.org/10.3389/fpls.2014.00370
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