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Transcriptome and metabolome analysis of plant sulfate starvation and resupply provides novel information on transcriptional regulation of metabolism associated with sulfur, nitrogen and phosphorus nutritional responses in Arabidopsis.

Bielecka M, Watanabe M, Morcuende R, Scheible WR, Hawkesford MJ, Hesse H, Hoefgen R - Front Plant Sci (2015)

Bottom Line: Additionally, combinations of transcriptome and metabolome data allowed identification of relationships between TFs and downstream responses, namely, expression changes in biosynthetic genes and subsequent metabolic responses.Effect chains on glucosinolate and polyamine biosynthesis are discussed in detail.The knowledge gained from this study provides a blueprint for an integrated analysis of transcriptomics and metabolomics and application for the identification of uncharacterized genes.

View Article: PubMed Central - PubMed

Affiliation: Department of Pharmaceutical Biotechnology, Faculty of Pharmacy, Wroclaw Medical University Wroclaw, Poland ; Max-Planck Institute of Molecular Plant Physiology Potsdam-Golm, Germany.

ABSTRACT
Sulfur is an essential macronutrient for plant growth and development. Reaching a thorough understanding of the molecular basis for changes in plant metabolism depending on the sulfur-nutritional status at the systems level will advance our basic knowledge and help target future crop improvement. Although the transcriptional responses induced by sulfate starvation have been studied in the past, knowledge of the regulation of sulfur metabolism is still fragmentary. This work focuses on the discovery of candidates for regulatory genes such as transcription factors (TFs) using 'omics technologies. For this purpose a short term sulfate-starvation/re-supply approach was used. ATH1 microarray studies and metabolite determinations yielded 21 TFs which responded more than 2-fold at the transcriptional level to sulfate starvation. Categorization by response behaviors under sulfate-starvation/re-supply and other nutrient starvations such as nitrate and phosphate allowed determination of whether the TF genes are specific for or common between distinct mineral nutrient depletions. Extending this co-behavior analysis to the whole transcriptome data set enabled prediction of putative downstream genes. Additionally, combinations of transcriptome and metabolome data allowed identification of relationships between TFs and downstream responses, namely, expression changes in biosynthetic genes and subsequent metabolic responses. Effect chains on glucosinolate and polyamine biosynthesis are discussed in detail. The knowledge gained from this study provides a blueprint for an integrated analysis of transcriptomics and metabolomics and application for the identification of uncharacterized genes.

No MeSH data available.


Related in: MedlinePlus

Levels of sulfur related metabolites in Arabidopsis seedlings grown in liquid cultures under different sulfate regimes. Values ± SD characterize the average of three independent measurements. Asterisks indicate values that are significantly different (P < 0.05) in comparison to the respective FN controls. (FN, full nutrition; S, re-supplied sulfate).
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Figure 1: Levels of sulfur related metabolites in Arabidopsis seedlings grown in liquid cultures under different sulfate regimes. Values ± SD characterize the average of three independent measurements. Asterisks indicate values that are significantly different (P < 0.05) in comparison to the respective FN controls. (FN, full nutrition; S, re-supplied sulfate).

Mentions: The tissue content of sulfate was determined as an indicator for the status of sulfate starvation of the plant. As expected, strong decreases of sulfate content after 2 days of sulfate starvation were observed (Figure 1). Starved seedlings contained only 4–6% of the sulfate level measured in control plants grown on FN medium. Despite re-supply of sulfate, only a slight 1.5-fold increase of sulfate was detected 3 h after re-supply in experiment 1, compared to continually starved plants. The content of organic sulfur compounds such as cysteine (Cys) and glutathione (GSH) were reduced upon sulfate starvation (Figure 1). In contrast to the slight changes of inorganic sulfate upon resupply, the levels of Cys and GSH were significantly increased after re-supply of sulfate (Figure 1). Interestingly, the GSH precursor gamma-glutamylcysteine (GEC) abundance peaks even before the accumulation of GSH, showing a delay in the conversion of GEC to GSH in experiment 2.


Transcriptome and metabolome analysis of plant sulfate starvation and resupply provides novel information on transcriptional regulation of metabolism associated with sulfur, nitrogen and phosphorus nutritional responses in Arabidopsis.

Bielecka M, Watanabe M, Morcuende R, Scheible WR, Hawkesford MJ, Hesse H, Hoefgen R - Front Plant Sci (2015)

Levels of sulfur related metabolites in Arabidopsis seedlings grown in liquid cultures under different sulfate regimes. Values ± SD characterize the average of three independent measurements. Asterisks indicate values that are significantly different (P < 0.05) in comparison to the respective FN controls. (FN, full nutrition; S, re-supplied sulfate).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4309162&req=5

Figure 1: Levels of sulfur related metabolites in Arabidopsis seedlings grown in liquid cultures under different sulfate regimes. Values ± SD characterize the average of three independent measurements. Asterisks indicate values that are significantly different (P < 0.05) in comparison to the respective FN controls. (FN, full nutrition; S, re-supplied sulfate).
Mentions: The tissue content of sulfate was determined as an indicator for the status of sulfate starvation of the plant. As expected, strong decreases of sulfate content after 2 days of sulfate starvation were observed (Figure 1). Starved seedlings contained only 4–6% of the sulfate level measured in control plants grown on FN medium. Despite re-supply of sulfate, only a slight 1.5-fold increase of sulfate was detected 3 h after re-supply in experiment 1, compared to continually starved plants. The content of organic sulfur compounds such as cysteine (Cys) and glutathione (GSH) were reduced upon sulfate starvation (Figure 1). In contrast to the slight changes of inorganic sulfate upon resupply, the levels of Cys and GSH were significantly increased after re-supply of sulfate (Figure 1). Interestingly, the GSH precursor gamma-glutamylcysteine (GEC) abundance peaks even before the accumulation of GSH, showing a delay in the conversion of GEC to GSH in experiment 2.

Bottom Line: Additionally, combinations of transcriptome and metabolome data allowed identification of relationships between TFs and downstream responses, namely, expression changes in biosynthetic genes and subsequent metabolic responses.Effect chains on glucosinolate and polyamine biosynthesis are discussed in detail.The knowledge gained from this study provides a blueprint for an integrated analysis of transcriptomics and metabolomics and application for the identification of uncharacterized genes.

View Article: PubMed Central - PubMed

Affiliation: Department of Pharmaceutical Biotechnology, Faculty of Pharmacy, Wroclaw Medical University Wroclaw, Poland ; Max-Planck Institute of Molecular Plant Physiology Potsdam-Golm, Germany.

ABSTRACT
Sulfur is an essential macronutrient for plant growth and development. Reaching a thorough understanding of the molecular basis for changes in plant metabolism depending on the sulfur-nutritional status at the systems level will advance our basic knowledge and help target future crop improvement. Although the transcriptional responses induced by sulfate starvation have been studied in the past, knowledge of the regulation of sulfur metabolism is still fragmentary. This work focuses on the discovery of candidates for regulatory genes such as transcription factors (TFs) using 'omics technologies. For this purpose a short term sulfate-starvation/re-supply approach was used. ATH1 microarray studies and metabolite determinations yielded 21 TFs which responded more than 2-fold at the transcriptional level to sulfate starvation. Categorization by response behaviors under sulfate-starvation/re-supply and other nutrient starvations such as nitrate and phosphate allowed determination of whether the TF genes are specific for or common between distinct mineral nutrient depletions. Extending this co-behavior analysis to the whole transcriptome data set enabled prediction of putative downstream genes. Additionally, combinations of transcriptome and metabolome data allowed identification of relationships between TFs and downstream responses, namely, expression changes in biosynthetic genes and subsequent metabolic responses. Effect chains on glucosinolate and polyamine biosynthesis are discussed in detail. The knowledge gained from this study provides a blueprint for an integrated analysis of transcriptomics and metabolomics and application for the identification of uncharacterized genes.

No MeSH data available.


Related in: MedlinePlus