Regulation of sulfur assimilation in higher plants: A sulfate transporter induced in sulfate-starved roots plays  a central role in
            <i>Arabidopsis thaliana</i>

Takahashi, Hideki; Yamazaki, Mami; Sasakura, Noriko; Watanabe, Akiko; Leustek, Thomas; Engler, Janice de Almeida; Engler, Gilbert; Montagu, Marc Van; Saito, Kazuki

doi:10.1073/pnas.94.20.11102

Cited by 326 publications

(271 citation statements)

References 45 publications

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“…Relative mRNA accumulations of sulfate transporter (Sultr) 2;2 and APR 1 to ubiquitin5 in leaves were determined using real-time PCR analysis. Sultr2;2 and APR1 are involved in sulfate transport and assimilation, respectively, and mRNA levels are reported to be increased by sulfate deficiency (Setya et al, 1996;Takahashi et al, 1997Takahashi et al, , 2000. In agreement with these previous reports, mRNA levels of Sultr2;2 and APR1 were increased by S deficiency in wild-type plants (Fig.…”

Section: Isolation Of An S-response Mutant Osh1-1supporting

confidence: 82%

Isolation and Characterization of an Arabidopsis Mutant That Overaccumulates O-Acetyl-l-Ser

et al. 2004

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O-Acetyl-L-Ser (OAS) is a positive regulator for the expression of sulfur (S) deficiency-inducible genes. In this study, through the isolation and analysis of Arabidopsis mutants exhibiting altered expression of S-responsive genes, we identified a thiol reductase as a regulator of the OAS levels. Ethyl methanesulfonate-mutagenized M2 seeds of transgenic Arabidopsis NOB7 carrying a chimeric S-responsive promoter driving the green fluorescent protein gene were screened for mutants with altered levels of green fluorescence compared to parental NOB7 line. One of the lines exhibited elevated levels of green fluorescence and mRNA accumulation of several endogenous S-responsive genes and carried a single recessive mutation responsible for the phenotype. OAS concentration in the rosette leaves of the mutant was about five times higher than that of wild-type plants. Based upon the high OAS levels, the mutant was named osh1-1 (OAS high accumulation). The OSH1 locus was mapped to a 30-kb region in chromosome V. DNA sequence analysis revealed no base change in this region; however, a demethylated C residue was found in the first exon of At5g01580. At5g01580 mRNA accumulation was higher in osh1-1 than in wild type, while transcript levels of other genes in the mapped region were not significantly altered in osh1-1. A line of transgenic plants overexpressing At5g01580 had elevated levels of endogenous S-responsive genes. These results suggest that elevated expression of At5g01580 is the cause of osh1 phenotype. Based on sequence similarity to animal thiol reductases, At5g01580 was tested for and exhibited thiol reductase activity. Possible roles of a thiol reductase in OAS metabolism are discussed.

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Section: Isolation Of An S-response Mutant Osh1-1supporting

confidence: 82%

Isolation and Characterization of an Arabidopsis Mutant That Overaccumulates O-Acetyl-l-Ser

et al. 2004

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“…Arabidopsis SULTR2;1 is a low-affinity sulfate transporter localized in the pericycle and vascular parenchyma cells (Takahashi et al, 1997(Takahashi et al, , 2000. SULTR2;1 mRNA abundance significantly increased during sulfur starvation (Takahashi et al, 1997(Takahashi et al, , 2000.…”

Section: Introductionmentioning

confidence: 99%

Vacuolar Sulfate Transporters Are Essential Determinants Controlling Internal Distribution of Sulfate in Arabidopsis

et al. 2004

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Uptake of external sulfate from the environment and use of internal vacuolar sulfate pools are two important aspects of the acquisition of sulfur for metabolism. In this study, we demonstrated that the vacuolar SULTR4-type sulfate transporter facilitates the efflux of sulfate from the vacuoles and plays critical roles in optimizing the internal distribution of sulfate in Arabidopsis thaliana. SULTR4;1-green fluorescent protein (GFP) and SULTR4;2-GFP fusion proteins were expressed under the control of their own promoters in transgenic Arabidopsis. The fusion proteins were accumulated specifically in the tonoplast membranes and were localized predominantly in the pericycle and xylem parenchyma cells of roots and hypocotyls. In roots, SULTR4;1 was constantly accumulated regardless of the changes of sulfur conditions, whereas SULTR4;2 became abundant by sulfur limitation. In shoots, both transporters were accumulated by sulfur limitation. Vacuoles isolated from callus of the sultr4;1 sultr4;2 double knockout showed excess accumulation of sulfate, which was substantially decreased by overexpression of SULTR4;1-GFP. In seedlings, the supplied [ 35 S]sulfate was retained in the root tissue of the sultr4;1 sultr4;2 double knockout mutant. Comparison of the double and single knockouts suggested that SULTR4;1 plays a major role and SULTR4;2 has a supplementary function. Overexpression of SULTR4;1-GFP significantly decreased accumulation of [ 35 S]sulfate in the root tissue, complementing the phenotype of the double mutant. These results suggested that SULTR4-type transporters, particularly SULTR4;1, actively mediate the efflux of sulfate from the vacuole lumen into the cytoplasm and influence the capacity for vacuolar storage of sulfate in the root tissue. The efflux function will promote rapid turnover of sulfate from the vacuoles particularly in the vasculature under conditions of lowsulfur supply, which will optimize the symplastic (cytoplasmic) flux of sulfate channeled toward the xylem vessels.

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“…Over the course of sulfur starvation, expression of several genes that encode enzymes or polypeptides responsible for acquisition and assimilation of sulfur are induced. Such genes encode sulfate transporters (Yildiz et al, 1994;Smith et al, 1997;Takahashi et al, 2000), arylsulfatase (de Hostos et al, 1988), and enzymes required for the reduction and assimilation of sulfate (Gutierrez-Marcos et al, 1996;Setya et al, 1996;Yildiz et al, 1996;Takahashi et al, 1997). The accumulation of these polypeptides following sulfur deprivation would increase the cell's capacity to access and take up the limited amount of sulfate in the environment and facilitate the synthesis of Cys and Met.…”

Section: Discussionmentioning

confidence: 99%

“…In Chlamydomonas reinhardtii and Volvox carteri, an extracellular arylsulfatase (encoded by the Ars1 and Ars2 genes in C. reinhardtii) can facilitate utilization of exogenous, esterified sulfate (de Hostos et al, 1988; Hallman and Sumper, 1994;Davies and Grossman, 1998). The induction of genes encoding ATP sulfurylase (Ats1), adenosine 5Ј-phosphosulfate reductase (adenosine 5Ј-phosphosulfate sulfotransferase), and Ser acetyltransferase during sulfur-limited growth may facilitate reduction of sulfate and the synthesis of Cys and Met (Gutierrez-Marcos et al, 1996;Setya et al, 1996;Yildiz et al, 1996;Takahashi et al, 1997). Sulfur limitation may also result in functional substitutions of proteins rich in sulfur with those having few sulfur-containing amino acids (Naito et al, 1994;Petrucco et al, 1996) and provoke protein degradation and recapture of the sulfur contained in Cys and Met (Collier and Grossman, 1992; Ferreira and Teixeira, 1992).…”

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confidence: 99%

Sulfur Economy and Cell Wall Biosynthesis during Sulfur Limitation of Chlamydomonas reinhardtii

2001

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We have identified two novel periplasmic/cell wall polypeptides that specifically accumulate during sulfur limitation of Chlamydomonas reinhardtii. These polypeptides, present at high levels in the extracellular polypeptide fraction from a sulfur-deprived, cell wall-minus C. reinhardtii strain, have apparent molecular masses of 76 and 88 kD and are designated Ecp76 and Ecp88. N-terminal sequences of these polypeptides facilitated the isolation of full-length Ecp76 and Ecp88 cDNAs. Ecp76 and Ecp88 polypeptides are deduced to be 583 and 595 amino acids, respectively. Their amino acid sequences are similar to each other, with features characteristic of cell wall-localized hydroxyproline-rich glycoproteins; the N terminus of each polypeptide contains a predicted signal sequence, whereas the C terminus is rich in proline, alanine, and serine. Ecp76 and Ecp88 have either no (Ecp88) or one (Ecp76) sulfur-containing amino acid and transcripts encoding these polypeptides are not detected in cultures maintained on complete medium, but accumulate when cells are deprived of sulfur. This accumulation is temporally delayed relative to the accumulation of sulfur stress-induced arylsulfatase and ATP sulfurylase transcripts. The addition of sulfate back to sulfur-starved cultures caused a rapid decline in Ecp76 and Ecp88 mRNAs (half lives Ͻ 10 min). Furthermore, the C. reinhardtii sac1 mutant, which lacks a regulatory protein critical for acclimation to sulfur limitation, does not accumulate Ecp76 or Ecp88 transcripts. These results suggest that the Ecp76 and Ecp88 genes are under SacI control, and that restructuring of the C. reinhardtii cell wall during sulfur limitation may be important for redistribution of internal and efficient utilization of environmental sulfur-containing molecules.Sulfur is an essential macronutrient that is taken up by plant, algal, and microbial cells, primarily as the inorganic sulfate anion. Limitations for sulfur in the environment can inhibit plant growth and productivity (Grossman and Takahashi, 2001). However, plants are able to acclimate to sulfur-limited growth conditions by synthesizing enzymes that function in the efficient acquisition and utilization of both external and internal sulfur sources. Sulfur limitation may promote expression of genes encoding sulfatases and high-affinity sulfate transporters in both plants and algae (de Hostos et al., 1989;Yildiz et al., 1994;Smith et al., 1997;Takahashi et al., 2000). In Chlamydomonas reinhardtii and Volvox carteri, an extracellular arylsulfatase (encoded by the Ars1 and Ars2 genes in C. reinhardtii) can facilitate utilization of exogenous, esterified sulfate (de Hostos et al., 1988; Hallman and Sumper, 1994;Davies and Grossman, 1998). The induction of genes encoding ATP sulfurylase (Ats1), adenosine 5Ј-phosphosulfate reductase (adenosine 5Ј-phosphosulfate sulfotransferase), and Ser acetyltransferase during sulfur-limited growth may facilitate reduction of sulfate and the synthesis of Cys and Met (Gutierrez-Marcos et al., 1996;Setya et al., 199...

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Regulation of sulfur assimilation in higher plants: A sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana

Cited by 326 publications

References 45 publications

Isolation and Characterization of an Arabidopsis Mutant That Overaccumulates O-Acetyl-l-Ser

Isolation and Characterization of an Arabidopsis Mutant That Overaccumulates O-Acetyl-l-Ser

Vacuolar Sulfate Transporters Are Essential Determinants Controlling Internal Distribution of Sulfate in Arabidopsis

Sulfur Economy and Cell Wall Biosynthesis during Sulfur Limitation of Chlamydomonas reinhardtii

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