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Increased sensitivity to iron deficiency in Arabidopsis thaliana overaccumulating nicotianamine.

Cassin G, Mari S, Curie C, Briat JF, Czernic P - J. Exp. Bot. (2009)

Bottom Line: Nevertheless, NA overaccumulation does not interfere with the iron uptake mechanisms since the iron levels are similar in the NA-overaccumulating line and wild-type plants in both roots and leaves under both sufficient and deficient conditions.However, NA overaccumulation triggers an enhanced sensitivity to iron starvation, associated with a decrease in iron availability.This study draws attention to a particular phenotype where NA in excess paradoxically leads to iron deficiency, probably because of an increase of the NA apoplastic pool sequestering iron.

View Article: PubMed Central - PubMed

Affiliation: Centre National de la Recherche Scientifique (UMR 5004), Institut National de la Recherche Agronomique, Université Montpellier 2, Ecole Nationale Supérieure d'Agronomie, 2 Place Viala, F-34060 Montpellier cedex 2, France.

ABSTRACT
Nicotianamine (NA) is a non-protein amino acid derivative synthesized from S-adenosyl L-methionine able to bind several metal ions such as iron, copper, manganese, zinc, or nickel. In plants, NA appears to be involved in iron availability and is essential for the plant to complete its biological cycle. In graminaceous plants, NA is also the precursor in the biosynthesis of phytosiderophores. Arabidopsis lines accumulating 4- and 100-fold more NA than wild-type plants were used in order to evaluate the impact of such an NA overaccumulation on iron homeostasis. The expression of iron-regulated genes including the IRT1/FRO2 iron uptake system is highly induced at the transcript level under both iron-sufficient and iron-deficient conditions. Nevertheless, NA overaccumulation does not interfere with the iron uptake mechanisms since the iron levels are similar in the NA-overaccumulating line and wild-type plants in both roots and leaves under both sufficient and deficient conditions. This observation also suggests that the translocation of iron from the root to the shoot is not affected in the NA-overaccumulating line. However, NA overaccumulation triggers an enhanced sensitivity to iron starvation, associated with a decrease in iron availability. This study draws attention to a particular phenotype where NA in excess paradoxically leads to iron deficiency, probably because of an increase of the NA apoplastic pool sequestering iron. This finding strengthens the notion that extracellular NA in the apoplast could be a major checkpoint to control plant iron homeostasis.

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Related in: MedlinePlus

The NA-overaccumulating line is highly sensitive to iron deficiency. (A) The phenotype of Col-0 plants and K1 plants overaccumulating NA sown and transferred after 5 d to an iron-deficient medium (no iron added) for 12 d. (B) Fresh weight and total chlorophyll content (C) of the entire rosette part of 10 wild-type plants (black bars) or 10 NA-overaccumulating plants (white bars) grown under iron-deficient conditions as described above. (D) Kinetics of the root growth of wild-type plants (filled squares) or the NA-overaccumulating line (open squares) transferred 5 d after germination on half-strength MS medium without iron added. Error bars represent the SE of 10 repetitions.
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fig2: The NA-overaccumulating line is highly sensitive to iron deficiency. (A) The phenotype of Col-0 plants and K1 plants overaccumulating NA sown and transferred after 5 d to an iron-deficient medium (no iron added) for 12 d. (B) Fresh weight and total chlorophyll content (C) of the entire rosette part of 10 wild-type plants (black bars) or 10 NA-overaccumulating plants (white bars) grown under iron-deficient conditions as described above. (D) Kinetics of the root growth of wild-type plants (filled squares) or the NA-overaccumulating line (open squares) transferred 5 d after germination on half-strength MS medium without iron added. Error bars represent the SE of 10 repetitions.

Mentions: Given the deregulation of the iron acquisition systems in the K1 NA-overaccumulating line under iron-sufficient conditions, it was decided to focus on this line and to investigate its behaviour under iron starvation further. After transfer to a medium without added iron for 14 d, the wild-type plants displayed delayed growth but the K1 line appeared highly sensitive to iron starvation (Fig. 2A). To evaluate the effect of the deficiency, the leaf biomass and the chlorophyll content of both wild-type and K1 plants grown under iron-deficient conditions were quantified. As shown in Fig. 2B and C, both the leaf biomass and the chlorophyll content were decreased by 50% in the K1 line compared with wild-type plants under iron starvation. This lower tolerance to iron deficiency was also observed at the root level since the root growth of the K1 line was clearly reduced compared with wild-type plants (Fig. 2D).


Increased sensitivity to iron deficiency in Arabidopsis thaliana overaccumulating nicotianamine.

Cassin G, Mari S, Curie C, Briat JF, Czernic P - J. Exp. Bot. (2009)

The NA-overaccumulating line is highly sensitive to iron deficiency. (A) The phenotype of Col-0 plants and K1 plants overaccumulating NA sown and transferred after 5 d to an iron-deficient medium (no iron added) for 12 d. (B) Fresh weight and total chlorophyll content (C) of the entire rosette part of 10 wild-type plants (black bars) or 10 NA-overaccumulating plants (white bars) grown under iron-deficient conditions as described above. (D) Kinetics of the root growth of wild-type plants (filled squares) or the NA-overaccumulating line (open squares) transferred 5 d after germination on half-strength MS medium without iron added. Error bars represent the SE of 10 repetitions.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC2657549&req=5

fig2: The NA-overaccumulating line is highly sensitive to iron deficiency. (A) The phenotype of Col-0 plants and K1 plants overaccumulating NA sown and transferred after 5 d to an iron-deficient medium (no iron added) for 12 d. (B) Fresh weight and total chlorophyll content (C) of the entire rosette part of 10 wild-type plants (black bars) or 10 NA-overaccumulating plants (white bars) grown under iron-deficient conditions as described above. (D) Kinetics of the root growth of wild-type plants (filled squares) or the NA-overaccumulating line (open squares) transferred 5 d after germination on half-strength MS medium without iron added. Error bars represent the SE of 10 repetitions.
Mentions: Given the deregulation of the iron acquisition systems in the K1 NA-overaccumulating line under iron-sufficient conditions, it was decided to focus on this line and to investigate its behaviour under iron starvation further. After transfer to a medium without added iron for 14 d, the wild-type plants displayed delayed growth but the K1 line appeared highly sensitive to iron starvation (Fig. 2A). To evaluate the effect of the deficiency, the leaf biomass and the chlorophyll content of both wild-type and K1 plants grown under iron-deficient conditions were quantified. As shown in Fig. 2B and C, both the leaf biomass and the chlorophyll content were decreased by 50% in the K1 line compared with wild-type plants under iron starvation. This lower tolerance to iron deficiency was also observed at the root level since the root growth of the K1 line was clearly reduced compared with wild-type plants (Fig. 2D).

Bottom Line: Nevertheless, NA overaccumulation does not interfere with the iron uptake mechanisms since the iron levels are similar in the NA-overaccumulating line and wild-type plants in both roots and leaves under both sufficient and deficient conditions.However, NA overaccumulation triggers an enhanced sensitivity to iron starvation, associated with a decrease in iron availability.This study draws attention to a particular phenotype where NA in excess paradoxically leads to iron deficiency, probably because of an increase of the NA apoplastic pool sequestering iron.

View Article: PubMed Central - PubMed

Affiliation: Centre National de la Recherche Scientifique (UMR 5004), Institut National de la Recherche Agronomique, Université Montpellier 2, Ecole Nationale Supérieure d'Agronomie, 2 Place Viala, F-34060 Montpellier cedex 2, France.

ABSTRACT
Nicotianamine (NA) is a non-protein amino acid derivative synthesized from S-adenosyl L-methionine able to bind several metal ions such as iron, copper, manganese, zinc, or nickel. In plants, NA appears to be involved in iron availability and is essential for the plant to complete its biological cycle. In graminaceous plants, NA is also the precursor in the biosynthesis of phytosiderophores. Arabidopsis lines accumulating 4- and 100-fold more NA than wild-type plants were used in order to evaluate the impact of such an NA overaccumulation on iron homeostasis. The expression of iron-regulated genes including the IRT1/FRO2 iron uptake system is highly induced at the transcript level under both iron-sufficient and iron-deficient conditions. Nevertheless, NA overaccumulation does not interfere with the iron uptake mechanisms since the iron levels are similar in the NA-overaccumulating line and wild-type plants in both roots and leaves under both sufficient and deficient conditions. This observation also suggests that the translocation of iron from the root to the shoot is not affected in the NA-overaccumulating line. However, NA overaccumulation triggers an enhanced sensitivity to iron starvation, associated with a decrease in iron availability. This study draws attention to a particular phenotype where NA in excess paradoxically leads to iron deficiency, probably because of an increase of the NA apoplastic pool sequestering iron. This finding strengthens the notion that extracellular NA in the apoplast could be a major checkpoint to control plant iron homeostasis.

Show MeSH
Related in: MedlinePlus