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Leaves of the Arabidopsis maltose exporter1 mutant exhibit a metabolic profile with features of cold acclimation in the warm.

Purdy SJ, Bussell JD, Nunn CP, Smith SM - PLoS ONE (2013)

Bottom Line: Grown at 21 °C, mex1-1 plants were much smaller, with fewer leaves, and elevated carbohydrates and amino acids compared to WT.After prolonged growth at 4 °C, the shoot biomass, rosette diameter and number of leaves at bolting were similar in mex1-1 and WT.This may in turn compromise growth of mex1-1 in the warm relative to WT.

View Article: PubMed Central - PubMed

Affiliation: Australian Research Council Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, Western Australia, Australia ; Institute of Biological, Environmental & Rural Sciences, Aberystwyth University, Aberystwyth, United Kingdom.

ABSTRACT

Background: Arabidopsis plants accumulate maltose from starch breakdown during cold acclimation. The Arabidopsis mutant, maltose excess1-1, accumulates large amounts of maltose in the plastid even in the warm, due to a deficient plastid envelope maltose transporter. We therefore investigated whether the elevated maltose level in mex1-1 in the warm could result in changes in metabolism and physiology typical of WT plants grown in the cold.

Principal findings: Grown at 21 °C, mex1-1 plants were much smaller, with fewer leaves, and elevated carbohydrates and amino acids compared to WT. However, after transfer to 4 °C the total soluble sugar pool and amino acid concentration was in equal abundance in both genotypes, although the most abundant sugar in mex1-1 was still maltose whereas sucrose was in greatest abundance in WT. The chlorophyll a/b ratio in WT was much lower in the cold than in the warm, but in mex1-1 it was low in both warm and cold. After prolonged growth at 4 °C, the shoot biomass, rosette diameter and number of leaves at bolting were similar in mex1-1 and WT.

Conclusions: The mex1-1 mutation in warm-grown plants confers aspects of cold acclimation, including elevated levels of sugars and amino acids and low chlorophyll a/b ratio. This may in turn compromise growth of mex1-1 in the warm relative to WT. We suggest that elevated maltose in the plastid could be responsible for key aspects of cold acclimation.

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Changes in the amino acid profile of Col-0 and mex1-1 rosette leaves grown at 21 °C and after cold acclimation at 4 °C for 5 days.A, Heatmap showing changes in amino acid abundance normalised to Col-0 in the warm. B, Total amino acid content before and after cold acclimation µmol mg-1 FW. C, Fold-change in amino acids (cold/warm). D, Glycine/Serine ratio before and after acclimation. D,. Data is the mean of 5 biological replicates, ± SE. Different letters indicate significant differences, Student’s T test P ≤ 0.05.
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pone-0079412-g001: Changes in the amino acid profile of Col-0 and mex1-1 rosette leaves grown at 21 °C and after cold acclimation at 4 °C for 5 days.A, Heatmap showing changes in amino acid abundance normalised to Col-0 in the warm. B, Total amino acid content before and after cold acclimation µmol mg-1 FW. C, Fold-change in amino acids (cold/warm). D, Glycine/Serine ratio before and after acclimation. D,. Data is the mean of 5 biological replicates, ± SE. Different letters indicate significant differences, Student’s T test P ≤ 0.05.

Mentions: Nearly all amino acids showed an increase in abundance after cold acclimation (Table 1). The most abundant amino acid in WT was Gln both before and after acclimation whereas Glu and Pro were in greatest abundance in mex1-1 in warm and cold conditions, respectively. In both treatments GABA was in lowest abundance in mex1-1 and also in WT in the warm, after acclimation Ornithine was of lowest abundance in the WT (Table 1). To visualise the differences, and to compare amino acid levels in all treatments, we have also presented them in the form of a heatmap, normalised to the level of each amino acid in Col-0 in the warm (Figure 1A). Of the 28 amino acids quantified, 25 were present in greater amount in mex1-1 than in WT in the warm, and of these, about half were present at levels equal to or greater than the levels in WT in the cold. The total amino acid abundance was 30%, higher in mex1-1 than in WT in the warm but in the cold the total amino acid abundance increased to similar levels in both genotypes (Figure 1B). Thus, in amino acid content, mex1-1 in the warm exhibits some characteristics of WT in the cold. Clear exceptions were Pro and its family members citrulline and ornithine. The amino acids most elevated in mex1-1 in the warm do not fall into any particular chemical or biosynthetic classes, and their accumulation could in part be explained by slower growth of the mutant.


Leaves of the Arabidopsis maltose exporter1 mutant exhibit a metabolic profile with features of cold acclimation in the warm.

Purdy SJ, Bussell JD, Nunn CP, Smith SM - PLoS ONE (2013)

Changes in the amino acid profile of Col-0 and mex1-1 rosette leaves grown at 21 °C and after cold acclimation at 4 °C for 5 days.A, Heatmap showing changes in amino acid abundance normalised to Col-0 in the warm. B, Total amino acid content before and after cold acclimation µmol mg-1 FW. C, Fold-change in amino acids (cold/warm). D, Glycine/Serine ratio before and after acclimation. D,. Data is the mean of 5 biological replicates, ± SE. Different letters indicate significant differences, Student’s T test P ≤ 0.05.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3818174&req=5

pone-0079412-g001: Changes in the amino acid profile of Col-0 and mex1-1 rosette leaves grown at 21 °C and after cold acclimation at 4 °C for 5 days.A, Heatmap showing changes in amino acid abundance normalised to Col-0 in the warm. B, Total amino acid content before and after cold acclimation µmol mg-1 FW. C, Fold-change in amino acids (cold/warm). D, Glycine/Serine ratio before and after acclimation. D,. Data is the mean of 5 biological replicates, ± SE. Different letters indicate significant differences, Student’s T test P ≤ 0.05.
Mentions: Nearly all amino acids showed an increase in abundance after cold acclimation (Table 1). The most abundant amino acid in WT was Gln both before and after acclimation whereas Glu and Pro were in greatest abundance in mex1-1 in warm and cold conditions, respectively. In both treatments GABA was in lowest abundance in mex1-1 and also in WT in the warm, after acclimation Ornithine was of lowest abundance in the WT (Table 1). To visualise the differences, and to compare amino acid levels in all treatments, we have also presented them in the form of a heatmap, normalised to the level of each amino acid in Col-0 in the warm (Figure 1A). Of the 28 amino acids quantified, 25 were present in greater amount in mex1-1 than in WT in the warm, and of these, about half were present at levels equal to or greater than the levels in WT in the cold. The total amino acid abundance was 30%, higher in mex1-1 than in WT in the warm but in the cold the total amino acid abundance increased to similar levels in both genotypes (Figure 1B). Thus, in amino acid content, mex1-1 in the warm exhibits some characteristics of WT in the cold. Clear exceptions were Pro and its family members citrulline and ornithine. The amino acids most elevated in mex1-1 in the warm do not fall into any particular chemical or biosynthetic classes, and their accumulation could in part be explained by slower growth of the mutant.

Bottom Line: Grown at 21 °C, mex1-1 plants were much smaller, with fewer leaves, and elevated carbohydrates and amino acids compared to WT.After prolonged growth at 4 °C, the shoot biomass, rosette diameter and number of leaves at bolting were similar in mex1-1 and WT.This may in turn compromise growth of mex1-1 in the warm relative to WT.

View Article: PubMed Central - PubMed

Affiliation: Australian Research Council Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, Western Australia, Australia ; Institute of Biological, Environmental & Rural Sciences, Aberystwyth University, Aberystwyth, United Kingdom.

ABSTRACT

Background: Arabidopsis plants accumulate maltose from starch breakdown during cold acclimation. The Arabidopsis mutant, maltose excess1-1, accumulates large amounts of maltose in the plastid even in the warm, due to a deficient plastid envelope maltose transporter. We therefore investigated whether the elevated maltose level in mex1-1 in the warm could result in changes in metabolism and physiology typical of WT plants grown in the cold.

Principal findings: Grown at 21 °C, mex1-1 plants were much smaller, with fewer leaves, and elevated carbohydrates and amino acids compared to WT. However, after transfer to 4 °C the total soluble sugar pool and amino acid concentration was in equal abundance in both genotypes, although the most abundant sugar in mex1-1 was still maltose whereas sucrose was in greatest abundance in WT. The chlorophyll a/b ratio in WT was much lower in the cold than in the warm, but in mex1-1 it was low in both warm and cold. After prolonged growth at 4 °C, the shoot biomass, rosette diameter and number of leaves at bolting were similar in mex1-1 and WT.

Conclusions: The mex1-1 mutation in warm-grown plants confers aspects of cold acclimation, including elevated levels of sugars and amino acids and low chlorophyll a/b ratio. This may in turn compromise growth of mex1-1 in the warm relative to WT. We suggest that elevated maltose in the plastid could be responsible for key aspects of cold acclimation.

Show MeSH
Related in: MedlinePlus