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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

THIC and THI4 expression in Arabidopsis tissues. AtGeneExpress values (log2) for THIC and THI4 were normalized to the respective overall mean of each gene. Relative THI4 expression is strongly correlated with THIC expression except in the later stages of seed development (open squares, red is mature stage) where THIC expression declines sharply during embryo maturation while THI4 expression remains high. Seed at earlier stages (black open squares), stamens containing developing pollen (black open diamonds) and mature pollen (red open diamond) conform to the pattern of proportional expression of THI4 and THIC observed in other tissues (blue solid diamonds).
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Figure 3: THIC and THI4 expression in Arabidopsis tissues. AtGeneExpress values (log2) for THIC and THI4 were normalized to the respective overall mean of each gene. Relative THI4 expression is strongly correlated with THIC expression except in the later stages of seed development (open squares, red is mature stage) where THIC expression declines sharply during embryo maturation while THI4 expression remains high. Seed at earlier stages (black open squares), stamens containing developing pollen (black open diamonds) and mature pollen (red open diamond) conform to the pattern of proportional expression of THI4 and THIC observed in other tissues (blue solid diamonds).

Mentions: The close correlation of THI4 and THIC expression in most Arabidopsis organs is depicted in Figure 3. A striking exception occurs during later stages of embryo development where THIC expression declines sharply while relative THI4 expression remains high. By comparison, the distribution of thiamin gene expression in the maize QTELLER dataset (Figure 4) revealed at least five developmental contexts where expression levels of THIC and THI4 diverge, and a sixth context, mature pollen, where gene expression for the thiamin de novo pathway overall is very low. As is the case for the Arabidopsis embryo, the relative expression of maize THI4 paralogs Thi1 and Thi2 is high compared to relative THIC expression in the developing embryo and endosperm (14 days after pollination, DAP), whereas in the shoot apical meristem (SAM) and in seedling roots the opposite pattern obtains in which THIC expression is high relative to THI4. Consistent with results of Woodward et al. (2010), the Thi1 and Thi2 paralogs exhibit divergent expression in 14 DAP endosperm, silks, seedlings and mature leaves, a pattern indicative of partial sub-functionalization at the level of gene regulation. Woodward et al. (2010) concluded that expression of Thi2 in leaf primordia surrounding the SAM is essential for maintenance of the SAM in maize implying that thiamin is transported to the SAM from surrounding organs. However, the transcriptome profile (Figure 4) indicated that in contrast to the THI4 paralogs, THIC is expressed in the SAM suggesting that the de novo pyrimidine biosynthesis pathway is potentially active in meristem cells which would enable thiamin synthesis via salvage of thiazole. In that case, it is plausible that the SAM is sustained at least partly by import of thiazole intermediates (e.g., HET) from surrounding leaves as well as thiamin.


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)

THIC and THI4 expression in Arabidopsis tissues. AtGeneExpress values (log2) for THIC and THI4 were normalized to the respective overall mean of each gene. Relative THI4 expression is strongly correlated with THIC expression except in the later stages of seed development (open squares, red is mature stage) where THIC expression declines sharply during embryo maturation while THI4 expression remains high. Seed at earlier stages (black open squares), stamens containing developing pollen (black open diamonds) and mature pollen (red open diamond) conform to the pattern of proportional expression of THI4 and THIC observed in other tissues (blue solid diamonds).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: THIC and THI4 expression in Arabidopsis tissues. AtGeneExpress values (log2) for THIC and THI4 were normalized to the respective overall mean of each gene. Relative THI4 expression is strongly correlated with THIC expression except in the later stages of seed development (open squares, red is mature stage) where THIC expression declines sharply during embryo maturation while THI4 expression remains high. Seed at earlier stages (black open squares), stamens containing developing pollen (black open diamonds) and mature pollen (red open diamond) conform to the pattern of proportional expression of THI4 and THIC observed in other tissues (blue solid diamonds).
Mentions: The close correlation of THI4 and THIC expression in most Arabidopsis organs is depicted in Figure 3. A striking exception occurs during later stages of embryo development where THIC expression declines sharply while relative THI4 expression remains high. By comparison, the distribution of thiamin gene expression in the maize QTELLER dataset (Figure 4) revealed at least five developmental contexts where expression levels of THIC and THI4 diverge, and a sixth context, mature pollen, where gene expression for the thiamin de novo pathway overall is very low. As is the case for the Arabidopsis embryo, the relative expression of maize THI4 paralogs Thi1 and Thi2 is high compared to relative THIC expression in the developing embryo and endosperm (14 days after pollination, DAP), whereas in the shoot apical meristem (SAM) and in seedling roots the opposite pattern obtains in which THIC expression is high relative to THI4. Consistent with results of Woodward et al. (2010), the Thi1 and Thi2 paralogs exhibit divergent expression in 14 DAP endosperm, silks, seedlings and mature leaves, a pattern indicative of partial sub-functionalization at the level of gene regulation. Woodward et al. (2010) concluded that expression of Thi2 in leaf primordia surrounding the SAM is essential for maintenance of the SAM in maize implying that thiamin is transported to the SAM from surrounding organs. However, the transcriptome profile (Figure 4) indicated that in contrast to the THI4 paralogs, THIC is expressed in the SAM suggesting that the de novo pyrimidine biosynthesis pathway is potentially active in meristem cells which would enable thiamin synthesis via salvage of thiazole. In that case, it is plausible that the SAM is sustained at least partly by import of thiazole intermediates (e.g., HET) from surrounding leaves as well as thiamin.

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