The role of 5′-adenylylsulfate reductase in controlling sulfate reduction in plants

Melinda N. Martin; Mitchell C. Tarczynski; Bo Shen; Thomas Leustek

doi:10.1007/s11120-005-9006-z

The role of 5′-adenylylsulfate reductase in controlling sulfate reduction in plants

Melinda N. Martin, Mitchell C. Tarczynski, Bo Shen, Thomas Leustek

School of Environmental and Biological Sciences, Plant Biology

Rutgers, The State University

Research output: Contribution to journal › Review article › peer-review

58 Scopus citations

Abstract

Cysteine is the first organic product of sulfate assimilation and as such is the precursor of all molecules containing reduced sulfur including methionine, glutathione, and their many metabolites. In plants, 5′-adenylylsulfate (APS) reductase is hypothesized to be a key regulatory point in sulfate assimilation and reduction. APS reductase catalyzes the two-electron reduction of APS to sulfite using glutathione as an electron donor. This paper reviews the experimental basis for this hypothesis. In addition, the results of an experiment designed to test the hypothesis by bypassing the endogenous APS reductase and its regulatory mechanisms are described. Two different bacterial assimilatory reductases were expressed in transgenic Zea mays, the thioredoxin-dependent APS reductase from Pseudomonas aeruginosa and the thioredoxin-dependent 3′-phosphoadenylylsulfate reductase from Escherichia coli. Each of them was placed under transcriptional control of the ubiquitin promoter and the protein products were targeted to chloroplasts. The leaves of transgenic Z. mays lines showed significant accumulation of reduced organic thiol compounds including cysteine, γ-glutamylcysteine, and glutathione; and reduced inorganic forms of sulfur including sulfite and thiosulfate. Both bacterial enzymes appeared to be equally capable of deregulating the assimilative sulfate reduction pathway. The reduced sulfur compounds accumulated to such high levels that the transgenic plants showed evidence of toxicity. The results provide additional evidence that APS reductase is a major control point for sulfate reduction in Z. mays.

Original language	American English
Pages (from-to)	309-323
Number of pages	15
Journal	Photosynthesis research
Volume	86
Issue number	3
DOIs	https://doi.org/10.1007/s11120-005-9006-z
State	Published - Dec 2005

ASJC Scopus subject areas

Biochemistry
Plant Science
Cell Biology

Keywords

5′-adenylylsulfate
Sulfate assimilation
Sulfate reduction

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10.1007/s11120-005-9006-z

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title = "The role of 5′-adenylylsulfate reductase in controlling sulfate reduction in plants",

abstract = "Cysteine is the first organic product of sulfate assimilation and as such is the precursor of all molecules containing reduced sulfur including methionine, glutathione, and their many metabolites. In plants, 5′-adenylylsulfate (APS) reductase is hypothesized to be a key regulatory point in sulfate assimilation and reduction. APS reductase catalyzes the two-electron reduction of APS to sulfite using glutathione as an electron donor. This paper reviews the experimental basis for this hypothesis. In addition, the results of an experiment designed to test the hypothesis by bypassing the endogenous APS reductase and its regulatory mechanisms are described. Two different bacterial assimilatory reductases were expressed in transgenic Zea mays, the thioredoxin-dependent APS reductase from Pseudomonas aeruginosa and the thioredoxin-dependent 3′-phosphoadenylylsulfate reductase from Escherichia coli. Each of them was placed under transcriptional control of the ubiquitin promoter and the protein products were targeted to chloroplasts. The leaves of transgenic Z. mays lines showed significant accumulation of reduced organic thiol compounds including cysteine, γ-glutamylcysteine, and glutathione; and reduced inorganic forms of sulfur including sulfite and thiosulfate. Both bacterial enzymes appeared to be equally capable of deregulating the assimilative sulfate reduction pathway. The reduced sulfur compounds accumulated to such high levels that the transgenic plants showed evidence of toxicity. The results provide additional evidence that APS reductase is a major control point for sulfate reduction in Z. mays.",

keywords = "5′-adenylylsulfate, Sulfate assimilation, Sulfate reduction",

author = "Martin, {Melinda N.} and Tarczynski, {Mitchell C.} and Bo Shen and Thomas Leustek",

note = "Funding Information: The research was funded by the United States National Science Foundation IBN-9817594 (TL), MCB-0094062 (MNM), and Pioneer Hi-Bred International, Inc. The authors wish to acknowledge Kimberly Glassman for vector construction and Jerry Ranch for Zea mays transformation.",

year = "2005",

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doi = "10.1007/s11120-005-9006-z",

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T1 - The role of 5′-adenylylsulfate reductase in controlling sulfate reduction in plants

AU - Martin, Melinda N.

AU - Tarczynski, Mitchell C.

AU - Shen, Bo

AU - Leustek, Thomas

N1 - Funding Information: The research was funded by the United States National Science Foundation IBN-9817594 (TL), MCB-0094062 (MNM), and Pioneer Hi-Bred International, Inc. The authors wish to acknowledge Kimberly Glassman for vector construction and Jerry Ranch for Zea mays transformation.

PY - 2005/12

Y1 - 2005/12

N2 - Cysteine is the first organic product of sulfate assimilation and as such is the precursor of all molecules containing reduced sulfur including methionine, glutathione, and their many metabolites. In plants, 5′-adenylylsulfate (APS) reductase is hypothesized to be a key regulatory point in sulfate assimilation and reduction. APS reductase catalyzes the two-electron reduction of APS to sulfite using glutathione as an electron donor. This paper reviews the experimental basis for this hypothesis. In addition, the results of an experiment designed to test the hypothesis by bypassing the endogenous APS reductase and its regulatory mechanisms are described. Two different bacterial assimilatory reductases were expressed in transgenic Zea mays, the thioredoxin-dependent APS reductase from Pseudomonas aeruginosa and the thioredoxin-dependent 3′-phosphoadenylylsulfate reductase from Escherichia coli. Each of them was placed under transcriptional control of the ubiquitin promoter and the protein products were targeted to chloroplasts. The leaves of transgenic Z. mays lines showed significant accumulation of reduced organic thiol compounds including cysteine, γ-glutamylcysteine, and glutathione; and reduced inorganic forms of sulfur including sulfite and thiosulfate. Both bacterial enzymes appeared to be equally capable of deregulating the assimilative sulfate reduction pathway. The reduced sulfur compounds accumulated to such high levels that the transgenic plants showed evidence of toxicity. The results provide additional evidence that APS reductase is a major control point for sulfate reduction in Z. mays.

AB - Cysteine is the first organic product of sulfate assimilation and as such is the precursor of all molecules containing reduced sulfur including methionine, glutathione, and their many metabolites. In plants, 5′-adenylylsulfate (APS) reductase is hypothesized to be a key regulatory point in sulfate assimilation and reduction. APS reductase catalyzes the two-electron reduction of APS to sulfite using glutathione as an electron donor. This paper reviews the experimental basis for this hypothesis. In addition, the results of an experiment designed to test the hypothesis by bypassing the endogenous APS reductase and its regulatory mechanisms are described. Two different bacterial assimilatory reductases were expressed in transgenic Zea mays, the thioredoxin-dependent APS reductase from Pseudomonas aeruginosa and the thioredoxin-dependent 3′-phosphoadenylylsulfate reductase from Escherichia coli. Each of them was placed under transcriptional control of the ubiquitin promoter and the protein products were targeted to chloroplasts. The leaves of transgenic Z. mays lines showed significant accumulation of reduced organic thiol compounds including cysteine, γ-glutamylcysteine, and glutathione; and reduced inorganic forms of sulfur including sulfite and thiosulfate. Both bacterial enzymes appeared to be equally capable of deregulating the assimilative sulfate reduction pathway. The reduced sulfur compounds accumulated to such high levels that the transgenic plants showed evidence of toxicity. The results provide additional evidence that APS reductase is a major control point for sulfate reduction in Z. mays.

KW - 5′-adenylylsulfate

KW - Sulfate assimilation

KW - Sulfate reduction

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JO - Photosynthesis research

JF - Photosynthesis research

IS - 3

ER -

The role of 5′-adenylylsulfate reductase in controlling sulfate reduction in plants

Abstract

ASJC Scopus subject areas

Keywords

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