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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

Thiamin biosynthesis pathway in plants. Abbreviations (bold) used for enzyme and transport functions assigned to genes of Arabidopsis and maize (Table 1): THIC, hydroxymethylpyrimidine phosphate synthase; THI4, thiazole biosynthetic protein; TH1, hydroxymethylpyrimidine phosphate kinase/hydroxymethylpyrimidine kinase/thiamin-phosphate pyrophosphorylase (dual function enzyme); HETK, hydroxyethylthiazole kinase; TDPK, thiamin diphosphokinase; TPC, mitochondrial thiamin diphosphate carrier. Pathway intermediates and products include HMP-P, hydroxymethylpyrimidine phosphate; HMP-PP, hydroxymethylpyrimidine diphosphate; thiamin; ThDP, thiamin diphosphate; HET, hydroxyethylthiazole; HET-P, hydroxyethylthiazole phosphate. Dashed horizontal lines separate plastidial, cytosolic and mitochondrial compartments of the cell.
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Figure 1: Thiamin biosynthesis pathway in plants. Abbreviations (bold) used for enzyme and transport functions assigned to genes of Arabidopsis and maize (Table 1): THIC, hydroxymethylpyrimidine phosphate synthase; THI4, thiazole biosynthetic protein; TH1, hydroxymethylpyrimidine phosphate kinase/hydroxymethylpyrimidine kinase/thiamin-phosphate pyrophosphorylase (dual function enzyme); HETK, hydroxyethylthiazole kinase; TDPK, thiamin diphosphokinase; TPC, mitochondrial thiamin diphosphate carrier. Pathway intermediates and products include HMP-P, hydroxymethylpyrimidine phosphate; HMP-PP, hydroxymethylpyrimidine diphosphate; thiamin; ThDP, thiamin diphosphate; HET, hydroxyethylthiazole; HET-P, hydroxyethylthiazole phosphate. Dashed horizontal lines separate plastidial, cytosolic and mitochondrial compartments of the cell.

Mentions: In order to explore the distribution of thiamin biosynthetic capacity among plant organs, we took advantage of the thorough annotation of maize and Arabidopsis thiamin pathway genes provided in the PlantSEED (Figure 1; Gerdes et al., 2012). To minimize confusion due to inconsistency of genes names used in various species, for this study we have adopted the abbreviations listed in Table 1. In the de novo biosynthesis pathway, THIC and TH1 are encoded by single genes in maize and Arabidopsis, whereas two genes encode the thiamin diphospokinase (TDPK) and mitochondrial thiamin diphospate transporter (TPC) activities in both species (Zallot et al., 2013). Arabidopsis has a single THI4 gene, while the maize genome contains two THI4 paralogs (Thi1 and Thi2; Belanger et al., 1995; Woodward et al., 2010). In addition, we included in our analysis several salvage pathway genes (HETK, Goyer et al., 2013; NUDIX, Yazdani et al., 2013), and two genes of the TenA family that are implicated in salvage of the pyrimidine moiety (Zallot et al., 2014), as well as a COG0212 gene of unknown function implicated in thiamin metabolism by associations in plants and bacteria (Pribat et al., 2011).


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)

Thiamin biosynthesis pathway in plants. Abbreviations (bold) used for enzyme and transport functions assigned to genes of Arabidopsis and maize (Table 1): THIC, hydroxymethylpyrimidine phosphate synthase; THI4, thiazole biosynthetic protein; TH1, hydroxymethylpyrimidine phosphate kinase/hydroxymethylpyrimidine kinase/thiamin-phosphate pyrophosphorylase (dual function enzyme); HETK, hydroxyethylthiazole kinase; TDPK, thiamin diphosphokinase; TPC, mitochondrial thiamin diphosphate carrier. Pathway intermediates and products include HMP-P, hydroxymethylpyrimidine phosphate; HMP-PP, hydroxymethylpyrimidine diphosphate; thiamin; ThDP, thiamin diphosphate; HET, hydroxyethylthiazole; HET-P, hydroxyethylthiazole phosphate. Dashed horizontal lines separate plastidial, cytosolic and mitochondrial compartments of the cell.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Thiamin biosynthesis pathway in plants. Abbreviations (bold) used for enzyme and transport functions assigned to genes of Arabidopsis and maize (Table 1): THIC, hydroxymethylpyrimidine phosphate synthase; THI4, thiazole biosynthetic protein; TH1, hydroxymethylpyrimidine phosphate kinase/hydroxymethylpyrimidine kinase/thiamin-phosphate pyrophosphorylase (dual function enzyme); HETK, hydroxyethylthiazole kinase; TDPK, thiamin diphosphokinase; TPC, mitochondrial thiamin diphosphate carrier. Pathway intermediates and products include HMP-P, hydroxymethylpyrimidine phosphate; HMP-PP, hydroxymethylpyrimidine diphosphate; thiamin; ThDP, thiamin diphosphate; HET, hydroxyethylthiazole; HET-P, hydroxyethylthiazole phosphate. Dashed horizontal lines separate plastidial, cytosolic and mitochondrial compartments of the cell.
Mentions: In order to explore the distribution of thiamin biosynthetic capacity among plant organs, we took advantage of the thorough annotation of maize and Arabidopsis thiamin pathway genes provided in the PlantSEED (Figure 1; Gerdes et al., 2012). To minimize confusion due to inconsistency of genes names used in various species, for this study we have adopted the abbreviations listed in Table 1. In the de novo biosynthesis pathway, THIC and TH1 are encoded by single genes in maize and Arabidopsis, whereas two genes encode the thiamin diphospokinase (TDPK) and mitochondrial thiamin diphospate transporter (TPC) activities in both species (Zallot et al., 2013). Arabidopsis has a single THI4 gene, while the maize genome contains two THI4 paralogs (Thi1 and Thi2; Belanger et al., 1995; Woodward et al., 2010). In addition, we included in our analysis several salvage pathway genes (HETK, Goyer et al., 2013; NUDIX, Yazdani et al., 2013), and two genes of the TenA family that are implicated in salvage of the pyrimidine moiety (Zallot et al., 2014), as well as a COG0212 gene of unknown function implicated in thiamin metabolism by associations in plants and bacteria (Pribat et al., 2011).

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