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Growth performance and root transcriptome remodeling of Arabidopsis in response to Mars-like levels of magnesium sulfate.

Visscher AM, Paul AL, Kirst M, Guy CL, Schuerger AC, Ferl RJ - PLoS ONE (2010)

Bottom Line: Disabling ion transporters AtMRS2-10 and AtSULTR1;2, which are plasma membrane localized in peripheral root cells, is not an effective way to confer tolerance to magnesium sulfate soils.Arabidopsis mrs2-10 and sel1-10 knockout lines do not mitigate the growth inhibiting impacts of high MgSO(4).7H(2)O concentrations observed with wildtype plants.The results provide a solid basis for the understanding of the metabolic response of plants to elevated magnesium sulfate soils; it is the first transcriptome analysis of plants in this environment.

View Article: PubMed Central - PubMed

Affiliation: Horticultural Sciences Department, University of Florida, Gainesville, Florida, United States of America.

ABSTRACT

Background: Martian regolith (unconsolidated surface material) is a potential medium for plant growth in bioregenerative life support systems during manned missions on Mars. However, hydrated magnesium sulfate mineral levels in the regolith of Mars can reach as high as 10 wt%, and would be expected to be highly inhibitory to plant growth.

Methodology and principal findings: Disabling ion transporters AtMRS2-10 and AtSULTR1;2, which are plasma membrane localized in peripheral root cells, is not an effective way to confer tolerance to magnesium sulfate soils. Arabidopsis mrs2-10 and sel1-10 knockout lines do not mitigate the growth inhibiting impacts of high MgSO(4).7H(2)O concentrations observed with wildtype plants. A global approach was used to identify novel genes with potential to enhance tolerance to high MgSO(4).7H(2)O (magnesium sulfate) stress. The early Arabidopsis root transcriptome response to elevated concentrations of magnesium sulfate was characterized in Col-0, and also between Col-0 and the mutant line cax1-1, which was confirmed to be relatively tolerant of high levels of MgSO(4).7H(2)O in soil solution. Differentially expressed genes in Col-0 treated for 45 min. encode enzymes primarily involved in hormone metabolism, transcription factors, calcium-binding proteins, kinases, cell wall related proteins and membrane-based transporters. Over 200 genes encoding transporters were differentially expressed in Col-0 up to 180 min. of exposure, and one of the first down-regulated genes was CAX1. The importance of this early response in wildtype Arabidopsis is exemplified in the fact that only four transcripts were differentially expressed between Col-0 and cax1-1 at 180 min. after initiation of treatment.

Conclusions/significance: The results provide a solid basis for the understanding of the metabolic response of plants to elevated magnesium sulfate soils; it is the first transcriptome analysis of plants in this environment. The results foster the development of Mars soil-compatible plants by showing that cax1 mutants exhibit partial tolerance to magnesium sulfate, and by elucidating a small subset (500 vs. >10,000) of candidate genes for mutation or metabolic engineering that will enhance tolerance to magnesium sulfate soils.

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The shoot fresh weight biomass comparisons of mutant and wildtype lines grown on soil.Average fresh weight shoot biomass of (a) mrs2-10 and Col-0, (b) sel1-10 and Ws, (e) cax1-1 and Col-0, or (f) cax1/cax3 and Col-0 plants in response to increasing concentrations of MgSO4·7H2O in soil medium. Bars indicate standard error, n = 12. Average leaf chlorophyll content of (c) mrs2-10 and Col-0, (d) sel1-10 and Ws, (g) cax1-1 and Col-0, or (h) cax1/cax3 and Col-0 plants in response to increasing concentrations of MgSO4·7H2O in soil medium. Bars indicate standard error, n = 72. The asterisks indicate statistically significant differences between genotypes (p<0.05) at specific concentrations of MgSO4·7H2O based on ANOVA.
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pone-0012348-g005: The shoot fresh weight biomass comparisons of mutant and wildtype lines grown on soil.Average fresh weight shoot biomass of (a) mrs2-10 and Col-0, (b) sel1-10 and Ws, (e) cax1-1 and Col-0, or (f) cax1/cax3 and Col-0 plants in response to increasing concentrations of MgSO4·7H2O in soil medium. Bars indicate standard error, n = 12. Average leaf chlorophyll content of (c) mrs2-10 and Col-0, (d) sel1-10 and Ws, (g) cax1-1 and Col-0, or (h) cax1/cax3 and Col-0 plants in response to increasing concentrations of MgSO4·7H2O in soil medium. Bars indicate standard error, n = 72. The asterisks indicate statistically significant differences between genotypes (p<0.05) at specific concentrations of MgSO4·7H2O based on ANOVA.

Mentions: The growth performance of transporter gene knockout mutant lines and their respective wildtype backgrounds grown for four weeks on soil treated with MgSO4·7H2O in solution (0–100 mM) was compared on the basis of shoot fresh weight (FW) biomass and leaf chlorophyll levels. Figure 4 shows the growth habit of mrs2-10 and sel1-10 plants compared to wildtype in the left hand panels, and of cax1-1 and cax1/cax3 compared to wildtype in the right-hand panels. Statistical analysis of the FW shoot biomass of wildtype Arabidopsis (Ws, Col-0) with ANOVA confirmed the significant phytotoxic effects of increasing concentrations of dissolved MgSO4·7H2O on wildtype plant growth (Table S1). Subsequent ANOVA analyses assessed whether selected mutant lines could alleviate the growth-limiting effects seen in wildtype. Results showed that FW shoot biomass and leaf chlorophyll content of mrs2-10 and sel1-10 lines were indistinguishable from that of wildtype at the tested concentrations (Fig. 5a–d, Table S1). Ionome analysis of the mrs2-10 mutant exposed to regular nutrient conditions furthermore did not reveal a statistically different leaf Mg content compared to Col-0 (http://www.ionomicshub.org/home/PiiMS). Although there was little difference between the mrs2-10 and sel1-10 lines and their respective wild-type backgrounds, the cax1-1 and cax1/cax3 lines showed relative improvement in their ability to grow on MgSO4·7H2O enriched soil. Cax1-1 plants had significantly higher FW shoot biomass and leaf chlorophyll content than Col-0 grown at 80 and 100 mM MgSO4·7H2O (Fig. 5e,g, Table S1). The increase in cax1-1 shoot biomass over that of Col-0 was 89% and 149% at 80 and 100 mM respectively. The CAX1 knockout mutation did not fully eliminate the effects of high magnesium sulfate on plant growth performance; the absolute FW shoot biomass of cax1-1 grown on soil for four weeks was still low (20%) compared to untreated Col-0 (Fig 5e). Cax1/cax3 plants showed significantly higher leaf chlorophyll content than Col-0 grown at 80, and 100 mM, but the average FW shoot biomass increases of 26.8% and 33.2%, at 80 and 100 mM, were not found to be statistically significant (Fig. 5f,h, Table S1). The significant differences in FW shoot biomass and leaf chlorophyll content between cax1/cax3 and Col-0 grown at 0 mM MgSO4·7H2O were described in detail by Cheng et al. (2005). In this study, 0 mM was only included as a point of reference for the high concentrations of MgSO4·7H2O.


Growth performance and root transcriptome remodeling of Arabidopsis in response to Mars-like levels of magnesium sulfate.

Visscher AM, Paul AL, Kirst M, Guy CL, Schuerger AC, Ferl RJ - PLoS ONE (2010)

The shoot fresh weight biomass comparisons of mutant and wildtype lines grown on soil.Average fresh weight shoot biomass of (a) mrs2-10 and Col-0, (b) sel1-10 and Ws, (e) cax1-1 and Col-0, or (f) cax1/cax3 and Col-0 plants in response to increasing concentrations of MgSO4·7H2O in soil medium. Bars indicate standard error, n = 12. Average leaf chlorophyll content of (c) mrs2-10 and Col-0, (d) sel1-10 and Ws, (g) cax1-1 and Col-0, or (h) cax1/cax3 and Col-0 plants in response to increasing concentrations of MgSO4·7H2O in soil medium. Bars indicate standard error, n = 72. The asterisks indicate statistically significant differences between genotypes (p<0.05) at specific concentrations of MgSO4·7H2O based on ANOVA.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2925951&req=5

pone-0012348-g005: The shoot fresh weight biomass comparisons of mutant and wildtype lines grown on soil.Average fresh weight shoot biomass of (a) mrs2-10 and Col-0, (b) sel1-10 and Ws, (e) cax1-1 and Col-0, or (f) cax1/cax3 and Col-0 plants in response to increasing concentrations of MgSO4·7H2O in soil medium. Bars indicate standard error, n = 12. Average leaf chlorophyll content of (c) mrs2-10 and Col-0, (d) sel1-10 and Ws, (g) cax1-1 and Col-0, or (h) cax1/cax3 and Col-0 plants in response to increasing concentrations of MgSO4·7H2O in soil medium. Bars indicate standard error, n = 72. The asterisks indicate statistically significant differences between genotypes (p<0.05) at specific concentrations of MgSO4·7H2O based on ANOVA.
Mentions: The growth performance of transporter gene knockout mutant lines and their respective wildtype backgrounds grown for four weeks on soil treated with MgSO4·7H2O in solution (0–100 mM) was compared on the basis of shoot fresh weight (FW) biomass and leaf chlorophyll levels. Figure 4 shows the growth habit of mrs2-10 and sel1-10 plants compared to wildtype in the left hand panels, and of cax1-1 and cax1/cax3 compared to wildtype in the right-hand panels. Statistical analysis of the FW shoot biomass of wildtype Arabidopsis (Ws, Col-0) with ANOVA confirmed the significant phytotoxic effects of increasing concentrations of dissolved MgSO4·7H2O on wildtype plant growth (Table S1). Subsequent ANOVA analyses assessed whether selected mutant lines could alleviate the growth-limiting effects seen in wildtype. Results showed that FW shoot biomass and leaf chlorophyll content of mrs2-10 and sel1-10 lines were indistinguishable from that of wildtype at the tested concentrations (Fig. 5a–d, Table S1). Ionome analysis of the mrs2-10 mutant exposed to regular nutrient conditions furthermore did not reveal a statistically different leaf Mg content compared to Col-0 (http://www.ionomicshub.org/home/PiiMS). Although there was little difference between the mrs2-10 and sel1-10 lines and their respective wild-type backgrounds, the cax1-1 and cax1/cax3 lines showed relative improvement in their ability to grow on MgSO4·7H2O enriched soil. Cax1-1 plants had significantly higher FW shoot biomass and leaf chlorophyll content than Col-0 grown at 80 and 100 mM MgSO4·7H2O (Fig. 5e,g, Table S1). The increase in cax1-1 shoot biomass over that of Col-0 was 89% and 149% at 80 and 100 mM respectively. The CAX1 knockout mutation did not fully eliminate the effects of high magnesium sulfate on plant growth performance; the absolute FW shoot biomass of cax1-1 grown on soil for four weeks was still low (20%) compared to untreated Col-0 (Fig 5e). Cax1/cax3 plants showed significantly higher leaf chlorophyll content than Col-0 grown at 80, and 100 mM, but the average FW shoot biomass increases of 26.8% and 33.2%, at 80 and 100 mM, were not found to be statistically significant (Fig. 5f,h, Table S1). The significant differences in FW shoot biomass and leaf chlorophyll content between cax1/cax3 and Col-0 grown at 0 mM MgSO4·7H2O were described in detail by Cheng et al. (2005). In this study, 0 mM was only included as a point of reference for the high concentrations of MgSO4·7H2O.

Bottom Line: Disabling ion transporters AtMRS2-10 and AtSULTR1;2, which are plasma membrane localized in peripheral root cells, is not an effective way to confer tolerance to magnesium sulfate soils.Arabidopsis mrs2-10 and sel1-10 knockout lines do not mitigate the growth inhibiting impacts of high MgSO(4).7H(2)O concentrations observed with wildtype plants.The results provide a solid basis for the understanding of the metabolic response of plants to elevated magnesium sulfate soils; it is the first transcriptome analysis of plants in this environment.

View Article: PubMed Central - PubMed

Affiliation: Horticultural Sciences Department, University of Florida, Gainesville, Florida, United States of America.

ABSTRACT

Background: Martian regolith (unconsolidated surface material) is a potential medium for plant growth in bioregenerative life support systems during manned missions on Mars. However, hydrated magnesium sulfate mineral levels in the regolith of Mars can reach as high as 10 wt%, and would be expected to be highly inhibitory to plant growth.

Methodology and principal findings: Disabling ion transporters AtMRS2-10 and AtSULTR1;2, which are plasma membrane localized in peripheral root cells, is not an effective way to confer tolerance to magnesium sulfate soils. Arabidopsis mrs2-10 and sel1-10 knockout lines do not mitigate the growth inhibiting impacts of high MgSO(4).7H(2)O concentrations observed with wildtype plants. A global approach was used to identify novel genes with potential to enhance tolerance to high MgSO(4).7H(2)O (magnesium sulfate) stress. The early Arabidopsis root transcriptome response to elevated concentrations of magnesium sulfate was characterized in Col-0, and also between Col-0 and the mutant line cax1-1, which was confirmed to be relatively tolerant of high levels of MgSO(4).7H(2)O in soil solution. Differentially expressed genes in Col-0 treated for 45 min. encode enzymes primarily involved in hormone metabolism, transcription factors, calcium-binding proteins, kinases, cell wall related proteins and membrane-based transporters. Over 200 genes encoding transporters were differentially expressed in Col-0 up to 180 min. of exposure, and one of the first down-regulated genes was CAX1. The importance of this early response in wildtype Arabidopsis is exemplified in the fact that only four transcripts were differentially expressed between Col-0 and cax1-1 at 180 min. after initiation of treatment.

Conclusions/significance: The results provide a solid basis for the understanding of the metabolic response of plants to elevated magnesium sulfate soils; it is the first transcriptome analysis of plants in this environment. The results foster the development of Mars soil-compatible plants by showing that cax1 mutants exhibit partial tolerance to magnesium sulfate, and by elucidating a small subset (500 vs. >10,000) of candidate genes for mutation or metabolic engineering that will enhance tolerance to magnesium sulfate soils.

Show MeSH
Related in: MedlinePlus