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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

Correlated expression of thiazole, pyrimidine, transport, and salvage genes of the thiamin biosynthesis pathway in Arabidopsis and maize. (A)Arabidopsis. A profile for each gene was calculated based on Pearson rank-order correlations with other thiamin pathway genes in the AtGeneExpress development dataset (Schmid et al., 2005). Genes were then clustered based on the matrix of pairwise correlations (R2 values) among the gene profiles. (B) Maize. A profile for each gene was constructed by calculating Pearson rank-order correlations with other thiamin pathway genes in the QTELLER transcriptome dataset (see Methods). Genes were then clustered based on the matrix of pairwise correlations (R2 values) among the gene profiles. TPC, mitochondrial thiamin diphosphate transporter; THI4, thiazole biosynthesis protein; HETK, hydroxyethyl thiazole kinase;. TDPK, thiamin diphosphokinase paralogs; TH1, hydroxymethylpyrimidine phosphate kinase/hydroxymethylpyrimidine kinase/thiamin-phosphate pyrophosphorylase, dual function protein; COG0212, putative thiamin related 5-formyltetrahydrofolate cycloligase-like protein, function unknown; TENA1 and TENA2, thiaminase II paralogs; NUDIX, putative thiamin related NUDIX type hydrolase; THIC, hydroxymethylpyrimidine phosphate synthase.
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Figure 2: Correlated expression of thiazole, pyrimidine, transport, and salvage genes of the thiamin biosynthesis pathway in Arabidopsis and maize. (A)Arabidopsis. A profile for each gene was calculated based on Pearson rank-order correlations with other thiamin pathway genes in the AtGeneExpress development dataset (Schmid et al., 2005). Genes were then clustered based on the matrix of pairwise correlations (R2 values) among the gene profiles. (B) Maize. A profile for each gene was constructed by calculating Pearson rank-order correlations with other thiamin pathway genes in the QTELLER transcriptome dataset (see Methods). Genes were then clustered based on the matrix of pairwise correlations (R2 values) among the gene profiles. TPC, mitochondrial thiamin diphosphate transporter; THI4, thiazole biosynthesis protein; HETK, hydroxyethyl thiazole kinase;. TDPK, thiamin diphosphokinase paralogs; TH1, hydroxymethylpyrimidine phosphate kinase/hydroxymethylpyrimidine kinase/thiamin-phosphate pyrophosphorylase, dual function protein; COG0212, putative thiamin related 5-formyltetrahydrofolate cycloligase-like protein, function unknown; TENA1 and TENA2, thiaminase II paralogs; NUDIX, putative thiamin related NUDIX type hydrolase; THIC, hydroxymethylpyrimidine phosphate synthase.

Mentions: To examine and compare coordinate regulation of the thiamin pathway in diverse organs of Arabidopsis and maize, we performed a rank correlation analysis of thiamin gene expression based on the AtGeneExpress development series (Schmid et al., 2005) for Arabidopsis (Figure 2A) and the QTELLER.org transcriptome database for maize (Figure 2B), respectively. In Arabidopsis, the genes encoding THI4 and THIC have highly correlated expression through development and indeed show the highest correlation (R2 = 0.98) of any pair of genes in the thiamin pathway. By contrast, THI4 and THIC genes exhibit divergent regulation in maize where they occupy distinct clusters in the correlation matrix (Figure 2B). While this difference may reflect biases in the organs represented in the Arabidopsis and maize datasets as well as fundamental differences in the regulation of the thiamin pathway in the two species, the propensity of species to exhibit different biases increases the power of comparative analysis much as it has in bacterial genomics. Hence, the maize system is potentially a source of new insights into the regulation of thiamin biosynthesis and transport in plants.


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)

Correlated expression of thiazole, pyrimidine, transport, and salvage genes of the thiamin biosynthesis pathway in Arabidopsis and maize. (A)Arabidopsis. A profile for each gene was calculated based on Pearson rank-order correlations with other thiamin pathway genes in the AtGeneExpress development dataset (Schmid et al., 2005). Genes were then clustered based on the matrix of pairwise correlations (R2 values) among the gene profiles. (B) Maize. A profile for each gene was constructed by calculating Pearson rank-order correlations with other thiamin pathway genes in the QTELLER transcriptome dataset (see Methods). Genes were then clustered based on the matrix of pairwise correlations (R2 values) among the gene profiles. TPC, mitochondrial thiamin diphosphate transporter; THI4, thiazole biosynthesis protein; HETK, hydroxyethyl thiazole kinase;. TDPK, thiamin diphosphokinase paralogs; TH1, hydroxymethylpyrimidine phosphate kinase/hydroxymethylpyrimidine kinase/thiamin-phosphate pyrophosphorylase, dual function protein; COG0212, putative thiamin related 5-formyltetrahydrofolate cycloligase-like protein, function unknown; TENA1 and TENA2, thiaminase II paralogs; NUDIX, putative thiamin related NUDIX type hydrolase; THIC, hydroxymethylpyrimidine phosphate synthase.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Correlated expression of thiazole, pyrimidine, transport, and salvage genes of the thiamin biosynthesis pathway in Arabidopsis and maize. (A)Arabidopsis. A profile for each gene was calculated based on Pearson rank-order correlations with other thiamin pathway genes in the AtGeneExpress development dataset (Schmid et al., 2005). Genes were then clustered based on the matrix of pairwise correlations (R2 values) among the gene profiles. (B) Maize. A profile for each gene was constructed by calculating Pearson rank-order correlations with other thiamin pathway genes in the QTELLER transcriptome dataset (see Methods). Genes were then clustered based on the matrix of pairwise correlations (R2 values) among the gene profiles. TPC, mitochondrial thiamin diphosphate transporter; THI4, thiazole biosynthesis protein; HETK, hydroxyethyl thiazole kinase;. TDPK, thiamin diphosphokinase paralogs; TH1, hydroxymethylpyrimidine phosphate kinase/hydroxymethylpyrimidine kinase/thiamin-phosphate pyrophosphorylase, dual function protein; COG0212, putative thiamin related 5-formyltetrahydrofolate cycloligase-like protein, function unknown; TENA1 and TENA2, thiaminase II paralogs; NUDIX, putative thiamin related NUDIX type hydrolase; THIC, hydroxymethylpyrimidine phosphate synthase.
Mentions: To examine and compare coordinate regulation of the thiamin pathway in diverse organs of Arabidopsis and maize, we performed a rank correlation analysis of thiamin gene expression based on the AtGeneExpress development series (Schmid et al., 2005) for Arabidopsis (Figure 2A) and the QTELLER.org transcriptome database for maize (Figure 2B), respectively. In Arabidopsis, the genes encoding THI4 and THIC have highly correlated expression through development and indeed show the highest correlation (R2 = 0.98) of any pair of genes in the thiamin pathway. By contrast, THI4 and THIC genes exhibit divergent regulation in maize where they occupy distinct clusters in the correlation matrix (Figure 2B). While this difference may reflect biases in the organs represented in the Arabidopsis and maize datasets as well as fundamental differences in the regulation of the thiamin pathway in the two species, the propensity of species to exhibit different biases increases the power of comparative analysis much as it has in bacterial genomics. Hence, the maize system is potentially a source of new insights into the regulation of thiamin biosynthesis and transport in plants.

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