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

Guan JC, Hasnain G, Garrett TJ, Chase CD, Gregory J, Hanson AD, McCarty DR - Front Plant Sci (2014)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Genetics Institute and Horticultural Sciences Department, Institute of Food and Agricultural Sciences, University of Florida Gainesville, FL, USA.

ABSTRACT
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.

No MeSH data available.


Related in: MedlinePlus

Genes encoding thiamin assembly and salvage steps are ubiquitously expressed in maize. TH1 (blue), TDPK1 and TDPK2 (red) function in primary synthesis and thiamin salvage pathways. HETK functions in thiazole salvage. Error bars are standard error of the mean (n = 3).
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Figure 8: Genes encoding thiamin assembly and salvage steps are ubiquitously expressed in maize. TH1 (blue), TDPK1 and TDPK2 (red) function in primary synthesis and thiamin salvage pathways. HETK functions in thiazole salvage. Error bars are standard error of the mean (n = 3).

Mentions: The opposing patterns of THIC and THI4 expression observed in meristems vs. filial organs of the seed raises the possibility that the relative flux through thiazole and pyrimidine salvage pathways, respectively, may differ in meristems and seed organs. Consistent with that hypothesis, relative expression of TH1, which functions in pyrimidine salvage as well as de novo synthesis, is high in the embryo compared to roots (Figure 8). However, expression of HETK was comparable in seed organs and root tips indicating a significant capacity for thiazole salvage in both contexts. As noted above, HETK clusters more strongly with THI4 than it does with TH1 or THIC (Figure 2B) suggesting it is broadly correlated with thiazole demand. By contrast, in the organs assayed in Figure 8, and in organs overall (Figure 4), TDPK2 correlated more strongly with TH1 and THIC than with the thiazole biosynthetic genes (Thi1 and Thi2). This pattern is consistent with the rate of pyrimidine biosynthesis being key to the overall control of thiamin biosynthesis (Bocobza et al., 2007, 2013). While the full metabolic implications of independent regulation of the thiazole biosynthetic pathway in maize organs remain to be elucidated, studies in rice implicate induction of THI4 in disease resistance (Wang et al., 2006).


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

Guan JC, Hasnain G, Garrett TJ, Chase CD, Gregory J, Hanson AD, McCarty DR - Front Plant Sci (2014)

Genes encoding thiamin assembly and salvage steps are ubiquitously expressed in maize. TH1 (blue), TDPK1 and TDPK2 (red) function in primary synthesis and thiamin salvage pathways. HETK functions in thiazole salvage. Error bars are standard error of the mean (n = 3).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4120688&req=5

Figure 8: Genes encoding thiamin assembly and salvage steps are ubiquitously expressed in maize. TH1 (blue), TDPK1 and TDPK2 (red) function in primary synthesis and thiamin salvage pathways. HETK functions in thiazole salvage. Error bars are standard error of the mean (n = 3).
Mentions: The opposing patterns of THIC and THI4 expression observed in meristems vs. filial organs of the seed raises the possibility that the relative flux through thiazole and pyrimidine salvage pathways, respectively, may differ in meristems and seed organs. Consistent with that hypothesis, relative expression of TH1, which functions in pyrimidine salvage as well as de novo synthesis, is high in the embryo compared to roots (Figure 8). However, expression of HETK was comparable in seed organs and root tips indicating a significant capacity for thiazole salvage in both contexts. As noted above, HETK clusters more strongly with THI4 than it does with TH1 or THIC (Figure 2B) suggesting it is broadly correlated with thiazole demand. By contrast, in the organs assayed in Figure 8, and in organs overall (Figure 4), TDPK2 correlated more strongly with TH1 and THIC than with the thiazole biosynthetic genes (Thi1 and Thi2). This pattern is consistent with the rate of pyrimidine biosynthesis being key to the overall control of thiamin biosynthesis (Bocobza et al., 2007, 2013). While the full metabolic implications of independent regulation of the thiazole biosynthetic pathway in maize organs remain to be elucidated, studies in rice implicate induction of THI4 in disease resistance (Wang et al., 2006).

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Genetics Institute and Horticultural Sciences Department, Institute of Food and Agricultural Sciences, University of Florida Gainesville, FL, USA.

ABSTRACT
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.

No MeSH data available.


Related in: MedlinePlus