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Are changes in sulfate assimilation pathway needed for evolution of C4 photosynthesis?

Weckopp SC, Kopriva S - Front Plant Sci (2015)

Bottom Line: It was, therefore, concluded that the bundle sheath localization of sulfate assimilation occurs only in C4 monocots.However, recently the sulfate assimilation pathway was found coordinately enriched in BSC of Arabidopsis, opening new questions about the significance of such cell-specific localization of the pathway.Indeed, such gradient, with higher expression of genes for sulfate reduction in C4 species, has been observed within the genus Flaveria.

View Article: PubMed Central - PubMed

Affiliation: Botanical Institute and Cluster of Excellence on Plant Sciences, Cologne Biocenter, University of Cologne , Cologne, Germany.

ABSTRACT
C4 photosynthesis characteristically features a cell-specific localization of enzymes involved in CO2 assimilation in bundle sheath cells (BSC) or mesophyll cells. Interestingly, enzymes of sulfur assimilation are also specifically present in BSC of maize and many other C4 species. This localization, however, could not be confirmed in C4 species of the genus Flaveria. It was, therefore, concluded that the bundle sheath localization of sulfate assimilation occurs only in C4 monocots. However, recently the sulfate assimilation pathway was found coordinately enriched in BSC of Arabidopsis, opening new questions about the significance of such cell-specific localization of the pathway. In addition, next generation sequencing revealed expression gradients of many genes from C3 to C4 species and mathematical modeling proposed a sequence of adaptations during the evolutionary path from C3 to C4. Indeed, such gradient, with higher expression of genes for sulfate reduction in C4 species, has been observed within the genus Flaveria. These new tools provide the basis for reexamining the intriguing question of compartmentalization of sulfur assimilation. Therefore, this review summarizes the findings on spatial separation of sulfur assimilation in C4 plants and Arabidopsis, assesses the information on sulfur assimilation provided by the recent transcriptomics data and discusses their possible impact on understanding this interesting feature of plant sulfur metabolism to find out whether changes in sulfate assimilation are part of a general evolutionary trajectory toward C4 photosynthesis.

No MeSH data available.


Related in: MedlinePlus

Intercellular compartmentation of sulfate assimilation and glutathione biosynthesis in maize. Sulfate is taken up from the soil and transported to the bundle sheath cells (BSC) through the xylem. The reduction of sulfate takes place exclusively in the plastids of BSC and is mediated by ATP sulfurylase (1), APS reductase (2), and sulfite reductase (3). Sulfide is further incorporated into the amino acid backbone of OAS by OAS (thiol)lyase (5) to form cysteine in chloroplasts, cytosol and mitochondria (not included) of BSC. OAS is derived from serine by serine acetyltransferase-mediated acetylation (4). Reduced sulfur is transported in form of cysteine to mesophyll cells where glutathione (GSH) synthesis is predominantly localized. GSH synthesis is driven by γ-EC synthetase (6) and GSH synthethase (7). APS, adenosine-5′-phosphosulfate; GSH, glutathione; OAS, O-acetylserine; γ-EC, γ-glutamylcysteine.
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Figure 1: Intercellular compartmentation of sulfate assimilation and glutathione biosynthesis in maize. Sulfate is taken up from the soil and transported to the bundle sheath cells (BSC) through the xylem. The reduction of sulfate takes place exclusively in the plastids of BSC and is mediated by ATP sulfurylase (1), APS reductase (2), and sulfite reductase (3). Sulfide is further incorporated into the amino acid backbone of OAS by OAS (thiol)lyase (5) to form cysteine in chloroplasts, cytosol and mitochondria (not included) of BSC. OAS is derived from serine by serine acetyltransferase-mediated acetylation (4). Reduced sulfur is transported in form of cysteine to mesophyll cells where glutathione (GSH) synthesis is predominantly localized. GSH synthesis is driven by γ-EC synthetase (6) and GSH synthethase (7). APS, adenosine-5′-phosphosulfate; GSH, glutathione; OAS, O-acetylserine; γ-EC, γ-glutamylcysteine.

Mentions: The question of intercellular compartmentation of sulfate assimilation in C4 species was first addressed by Gerwick and Black (1979) in the crabgrass Digitaria sanguinalis. They focused on the initial step of sulfur assimilation, the activation of sulfate by ATPS, and showed that more than 90% of total leaf ATPS activity was restricted to BSC in crabgrass. Similar results could be obtained for 17 additional C4 monocot species, representing each of the three C4 subtypes (Gerwick et al., 1980; Passera and Ghisi, 1982; Burnell, 1984; Schmutz and Brunold, 1984; Burgener et al., 1998). Analyses of the spatial separation of sulfate assimilation in maize leaves could additionally show restriction of APR activity to BSC (Figure 1; Schmutz and Brunold, 1984; Burgener et al., 1998), whereas activity of SIR and OASTL was equally detected in MC and BSC (Passera and Ghisi, 1982; Schmutz and Brunold, 1984, 1985).


Are changes in sulfate assimilation pathway needed for evolution of C4 photosynthesis?

Weckopp SC, Kopriva S - Front Plant Sci (2015)

Intercellular compartmentation of sulfate assimilation and glutathione biosynthesis in maize. Sulfate is taken up from the soil and transported to the bundle sheath cells (BSC) through the xylem. The reduction of sulfate takes place exclusively in the plastids of BSC and is mediated by ATP sulfurylase (1), APS reductase (2), and sulfite reductase (3). Sulfide is further incorporated into the amino acid backbone of OAS by OAS (thiol)lyase (5) to form cysteine in chloroplasts, cytosol and mitochondria (not included) of BSC. OAS is derived from serine by serine acetyltransferase-mediated acetylation (4). Reduced sulfur is transported in form of cysteine to mesophyll cells where glutathione (GSH) synthesis is predominantly localized. GSH synthesis is driven by γ-EC synthetase (6) and GSH synthethase (7). APS, adenosine-5′-phosphosulfate; GSH, glutathione; OAS, O-acetylserine; γ-EC, γ-glutamylcysteine.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4292454&req=5

Figure 1: Intercellular compartmentation of sulfate assimilation and glutathione biosynthesis in maize. Sulfate is taken up from the soil and transported to the bundle sheath cells (BSC) through the xylem. The reduction of sulfate takes place exclusively in the plastids of BSC and is mediated by ATP sulfurylase (1), APS reductase (2), and sulfite reductase (3). Sulfide is further incorporated into the amino acid backbone of OAS by OAS (thiol)lyase (5) to form cysteine in chloroplasts, cytosol and mitochondria (not included) of BSC. OAS is derived from serine by serine acetyltransferase-mediated acetylation (4). Reduced sulfur is transported in form of cysteine to mesophyll cells where glutathione (GSH) synthesis is predominantly localized. GSH synthesis is driven by γ-EC synthetase (6) and GSH synthethase (7). APS, adenosine-5′-phosphosulfate; GSH, glutathione; OAS, O-acetylserine; γ-EC, γ-glutamylcysteine.
Mentions: The question of intercellular compartmentation of sulfate assimilation in C4 species was first addressed by Gerwick and Black (1979) in the crabgrass Digitaria sanguinalis. They focused on the initial step of sulfur assimilation, the activation of sulfate by ATPS, and showed that more than 90% of total leaf ATPS activity was restricted to BSC in crabgrass. Similar results could be obtained for 17 additional C4 monocot species, representing each of the three C4 subtypes (Gerwick et al., 1980; Passera and Ghisi, 1982; Burnell, 1984; Schmutz and Brunold, 1984; Burgener et al., 1998). Analyses of the spatial separation of sulfate assimilation in maize leaves could additionally show restriction of APR activity to BSC (Figure 1; Schmutz and Brunold, 1984; Burgener et al., 1998), whereas activity of SIR and OASTL was equally detected in MC and BSC (Passera and Ghisi, 1982; Schmutz and Brunold, 1984, 1985).

Bottom Line: It was, therefore, concluded that the bundle sheath localization of sulfate assimilation occurs only in C4 monocots.However, recently the sulfate assimilation pathway was found coordinately enriched in BSC of Arabidopsis, opening new questions about the significance of such cell-specific localization of the pathway.Indeed, such gradient, with higher expression of genes for sulfate reduction in C4 species, has been observed within the genus Flaveria.

View Article: PubMed Central - PubMed

Affiliation: Botanical Institute and Cluster of Excellence on Plant Sciences, Cologne Biocenter, University of Cologne , Cologne, Germany.

ABSTRACT
C4 photosynthesis characteristically features a cell-specific localization of enzymes involved in CO2 assimilation in bundle sheath cells (BSC) or mesophyll cells. Interestingly, enzymes of sulfur assimilation are also specifically present in BSC of maize and many other C4 species. This localization, however, could not be confirmed in C4 species of the genus Flaveria. It was, therefore, concluded that the bundle sheath localization of sulfate assimilation occurs only in C4 monocots. However, recently the sulfate assimilation pathway was found coordinately enriched in BSC of Arabidopsis, opening new questions about the significance of such cell-specific localization of the pathway. In addition, next generation sequencing revealed expression gradients of many genes from C3 to C4 species and mathematical modeling proposed a sequence of adaptations during the evolutionary path from C3 to C4. Indeed, such gradient, with higher expression of genes for sulfate reduction in C4 species, has been observed within the genus Flaveria. These new tools provide the basis for reexamining the intriguing question of compartmentalization of sulfur assimilation. Therefore, this review summarizes the findings on spatial separation of sulfur assimilation in C4 plants and Arabidopsis, assesses the information on sulfur assimilation provided by the recent transcriptomics data and discusses their possible impact on understanding this interesting feature of plant sulfur metabolism to find out whether changes in sulfate assimilation are part of a general evolutionary trajectory toward C4 photosynthesis.

No MeSH data available.


Related in: MedlinePlus