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...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2014-08-01
|
| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | http://journal.frontiersin.org/article/10.3389/fpls.2014.00370/full |
| _version_ | 1818621405835558912 |
|---|---|
| author | Jiahn-Chou Guan Ghulam Hasnain Timothy J. Garrett Christine D. Chase Jesse Gregory Andrew D. Hanson Donald R. McCarty |
| author_facet | Jiahn-Chou Guan Ghulam Hasnain Timothy J. Garrett Christine D. Chase Jesse Gregory Andrew D. Hanson Donald R. McCarty |
| author_sort | Jiahn-Chou Guan |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-16T18:08:45Z |
| format | Article |
| id | doaj.art-ea66e2aa97e04c70aa34e011d27b9e84 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-16T18:08:45Z |
| publishDate | 2014-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-ea66e2aa97e04c70aa34e011d27b9e842022-12-21T22:21:51ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2014-08-01510.3389/fpls.2014.0037098585Divisions of labor in the thiamin biosynthetic pathway among organs of maizeJiahn-Chou Guan0Ghulam Hasnain1Timothy J. Garrett2Christine D. Chase3Jesse Gregory4Andrew D. Hanson5Donald R. McCarty6Genetics Institute and Horticultural Sciences Department, Institute of Food and Agricultural Sciences, University of FloridaGainesville, FL, USAHorticultural Sciences Department, Institute of Food and Agricultural Sciences, University of FloridaGainesville, FL, USADepartment of Pathology, Immunology, and Laboratory Medicine, College of Medicine, University of FloridaGainesville, FL, USAGenetics Institute and Horticultural Sciences Department, Institute of Food and Agricultural Sciences, University of FloridaGainesville, FL, USADepartment of Food Science and Human Nutrition, Institute of Food and Agricultural Sciences, University of FloridaGainesville, FL, USAHorticultural Sciences Department, Institute of Food and Agricultural Sciences, University of FloridaGainesville, FL, USAGenetics Institute and Horticultural Sciences Department, Institute of Food and Agricultural Sciences, University of FloridaGainesville, FL, USAThe 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.http://journal.frontiersin.org/article/10.3389/fpls.2014.00370/fullthiamin biosynthesiscomparative transcriptomicsmaize developmentpollen developmentmeristem metabolism |
| spellingShingle | Jiahn-Chou Guan Ghulam Hasnain Timothy J. Garrett Christine D. Chase Jesse Gregory Andrew D. Hanson Donald R. McCarty Divisions of labor in the thiamin biosynthetic pathway among organs of maize Frontiers in Plant Science thiamin biosynthesis comparative transcriptomics maize development pollen development meristem metabolism |
| 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 | thiamin biosynthesis comparative transcriptomics maize development pollen development meristem metabolism |
| url | http://journal.frontiersin.org/article/10.3389/fpls.2014.00370/full |
| work_keys_str_mv | AT jiahnchouguan divisionsoflaborinthethiaminbiosyntheticpathwayamongorgansofmaize AT ghulamhasnain divisionsoflaborinthethiaminbiosyntheticpathwayamongorgansofmaize AT timothyjgarrett divisionsoflaborinthethiaminbiosyntheticpathwayamongorgansofmaize AT christinedchase divisionsoflaborinthethiaminbiosyntheticpathwayamongorgansofmaize AT jessegregory divisionsoflaborinthethiaminbiosyntheticpathwayamongorgansofmaize AT andrewdhanson divisionsoflaborinthethiaminbiosyntheticpathwayamongorgansofmaize AT donaldrmccarty divisionsoflaborinthethiaminbiosyntheticpathwayamongorgansofmaize |