Signals from chloroplasts and mitochondria for iron homeostasis regulation

doi:10.1016/j.tplants.2013.01.006

Trends in Plant Science

Volume 18, Issue 6, June 2013, Pages 305-311

https://doi.org/10.1016/j.tplants.2013.01.006 Get rights and content

Iron (Fe) is an essential element for human nutrition. Given that plants represent a major dietary source of Fe worldwide, it is crucial to understand plant Fe homeostasis fully. A major breakthrough in the understanding of Fe sensing and signaling was the identification of several transcription factor cascades regulating Fe homeostasis. However, the mechanisms of activation of these cascades still remain to be elucidated. In this opinion, we focus on the possible roles of mitochondria and chloroplasts as cellular Fe sensing and signaling sites, offering a new perspective on the integrated regulation of Fe homeostasis and its interplay with cellular metabolism.

Highlights

► The understanding of plant iron homeostasis must be fully elucidated. ► We review the knowledge of metabolic adaptation in response to altered iron availability. ► Mitochondria and chloroplasts are proposed to act as cellular iron sensing and signaling sites.

Section snippets

Metabolic adaptation to the Fe status of a plant

Fe is essential for most living organisms, and plants represent the main dietary source of Fe in human nutrition. Consequently, Fe uptake by roots, its distribution throughout organs, tissues and subcellular compartments (Box 1, Box 2), the synthesis of prosthetic groups, such as heme or Fe–sulfur (S) clusters, and Fe storage were major focuses of scientific research during the past decade (for overview see [1]). Fe is essential for vital metabolic reactions in organelles, such as respiratory

Fe deficiency-induced changes in plant mitochondria and chloroplasts

Mitochondria are a major subcellular compartment for Fe metabolism, because Fe is an essential cofactor for several proteins belonging to RET and the tricarboxylic acid (TCA) cycle. Moreover, part of Fe–S cluster and heme biosynthesis is located in the mitochondria and is strictly linked to Fe homeostasis. Hence, alteration of the cellular Fe status dramatically influences mitochondrial functionality and thereby cellular metabolism 3, 4, 17, 18, 19.

Fe deficiency decreases RET activity [20].

Mitochondria and chloroplasts in Fe-dependent oxidative stress signal production and nitric oxide-mediated control of Fe homeostasis

Iron imbalance is known to induce oxidative stress in cells by promoting the generation and accumulation of ROS, causing oxidation of cellular components, hindering metabolic activities, and affecting organelle integrity [34]. Indeed, Fe is a cofactor of many antioxidant enzymes, including catalase, peroxidases, ascorbate peroxidase, and Fe-superoxide dismutase. These enzymes are strongly affected by Fe deficiency, leading to a consistent unbalance of the detoxification processes in plants,

Putative retrograde signals from Fe-stressed plastids and mitochondria

The coordination between organelle gene expression (OGE) and NGE requires both anterograde and retrograde signals [54] (Box 3). The retrograde pathway communicates changes in the metabolic status of the organelles to the nucleus and consequently changes the anterograde signals. Changes in the metabolic status of chloroplasts and/or mitochondria (e.g., in response to an altered Fe nutritional status) have profound effects on the rest of the plant cell, and involve massive changes in the

Concluding remarks and outlook

Despite great progress in understanding Fe homeostasis in plants, little insight has been gained concerning the effects of Fe nutritional status on the metabolism of organelles, and the consequences for Fe signaling.

Both Fe-deficient or Fe-excess conditions are known to affect mitochondrial and chloroplast metabolism through post-transcriptional and/or translational modifications of key enzymes. Such modifications are fast and enable a quicker response to environmental changes than via

Acknowledgments

We acknowledge Guilhem Reyt for helpful discussions on chloroplast retrograde signaling and Lesley Currah for carefully editing the manuscript. Furthermore, we thank the anonymous reviewers for their valuable comments, which were useful for improving the manuscript. Research of J-F.B. and K.P. was supported in the framework of the European Transnational Cooperation within the PLANT-KBBE Initiative funded by the Bundesministerium für Bildung und Forschung (BMBF, framework of the GABI initiative,

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Trends in Plant Science

OpinionSignals from chloroplasts and mitochondria for iron homeostasis regulation

Highlights

Section snippets

Metabolic adaptation to the Fe status of a plant

Fe deficiency-induced changes in plant mitochondria and chloroplasts

Mitochondria and chloroplasts in Fe-dependent oxidative stress signal production and nitric oxide-mediated control of Fe homeostasis

Putative retrograde signals from Fe-stressed plastids and mitochondria

Concluding remarks and outlook

Acknowledgments

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J. Biol. Chem.

J. Biol. Chem.

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Trends Plant Sci.

Mol. Plant

Curr. Biol.

Metabolic changes in iron-stressed dicotyledonous plants

Iron utilization and metabolism in plants

Curr. Opin. Plant Biol.

Responses of sugar beet roots to iron deficiency. Changes in carbon assimilation and oxygen use

Plant Physiol.

Proteomic response to iron deficiency in tomato root

Proteomics

The fate and the role of mitochondria in Fe-deficient roots of Strategy I plants

Plant Signal. Behav.

Changes in the proteomic and metabolic profiles of Beta vulgaris root tips in response to iron deficiency and resupply

BMC Plant Biol.

Proteomic characterization of iron deficiency responses in Cucumis sativus L. roots

BMC Plant Biol.

Organic acids and Fe deficiency: a review

Plant Soil

Iron uptake and loading into rice grains

Rice

Iron uptake, translocation and regulation in higher plants

Annu. Rev. Plant Biol.

Deficiency of Arabidopsis thaliana frataxin alters activity of mitochondrial Fe-S proteins and induces oxidative stress

Plant J.

The mitochondrial protein frataxin is essential for heme biosynthesis in plants

FEBS J.

The rice mitochondrial iron transporter is essential for plant growth

Nat. Commun.

Iron availability affects the function of mitochondria in cucumber roots

New Phytol.

Response of Arabidopsis to iron deficiency stress as revealed by microarray analysis

Plant Physiol.

iTRAQ protein profile analysis of Arabidopsis roots reveals new aspects critical for iron homeostasis

Plant Physiol.

Divalent metal ions in plant mitochondria and their role in interactions with proteins and oxidative stress-induced damage to respiratory function

Plant Physiol.

Opinion
Signals from chloroplasts and mitochondria for iron homeostasis regulation