New insights into ferritin synthesis and function highlight a link between iron homeostasis and oxidative stress in plants

Abstract

Background: Iron is an essential element for both plant productivity and nutritional quality. Improving plant iron content was attempted through genetic engineering of plants overexpressing ferritins. However, both the roles of these proteins in plant physiology, and the mechanisms involved in the regulation of their expression are largely unknown. Although the structure of ferritins is highly conserved between plants and animals, their cellular localization differs. Furthermore, regulation of ferritin gene expression in response to iron excess occurs at the transcriptional level in plants, in contrast to animals which regulate ferritin expression at the translational level.

Scope: In this review, an overview of our knowledge of bacterial and mammalian ferritin synthesis and functions is presented. Then the following will be reviewed: (a) the specific features of plant ferritins; (b) the regulation of their synthesis during development and in response to various environmental cues; and (c) their function in plant physiology, with special emphasis on the role that both bacterial and plant ferritins play during plant-bacteria interactions. Arabidopsis ferritins are encoded by a small nuclear gene family of four members which are differentially expressed. Recent results obtained by using this model plant enabled progress to be made in our understanding of the regulation of the synthesis and the in planta function of these various ferritins.

Conclusions: Studies on plant ferritin functions and regulation of their synthesis revealed strong links between these proteins and protection against oxidative stress. In contrast, their putative iron-storage function to furnish iron during various development processes is unlikely to be essential. Ferritins, by buffering iron, exert a fine tuning of the quantity of metal required for metabolic purposes, and help plants to cope with adverse situations, the deleterious effects of which would be amplified if no system had evolved to take care of free reactive iron.

Fig. 1.

Tissue-specific expression and developmental regulation of ferritin synthesis in Arabidopsis. The expression of the AtFer2 ferritin gene is restricted to mature seeds. In vegetative and reproductive organs, from the germination stage to flowering, AtFer-1, -3 and -4 genes are kinetically and differentially expressed in various tissues and organs (Petit et al., 2001a; Ravet et al., 2009)

Fig. 2.

Differential expression of Arabidopsis ferritin genes in response to exogenous signals. Iron excess treatment (Fe) leads to AtFer-1, -3 and -4 gene expression, whereas H₂O₂ application impacts positively only on the expression of the AtFer1 gene. Consistent with its seed-specific expression, the AtFer2 gene is the only Arabidopsis ferritin gene to be expressed in response to application of exogenous abscisic acid (ABA; Petit et al., 2001a).

Fig. 3.

Sequence aligment of the C-terminal parts of soybean and Arabidopsis ferritin subunits. Identical and similar residues between at least three proteins are boxed in black and grey, respectively. Amino acids are numbered from the translational start methionine. The arginine in position 234 of Soy H-1 subunit was shown to be the last residue of the processed 26·5-kDa form (Masuda et al., 2001). This residue and the corresponding arginines in Arabidopsis subunits are indicated in red.

Fig. 4.

A working model to explain the control of the AtFer1 gene expression in response to iron. (A) Under low-iron conditions, a repressor not directly bound to the AtFer1 promoter would interact with the transcription factor which recognizes the iron-dependent regulatory sequence (IDRS), leading to the repression of AtFer1 gene expression. (B) Under high-iron conditions, an enzymatically produced nitric oxide (NO) burst occurs within the plastids, preceding ubiquitination and proteasome-dependent degradation of the repressor. De-phosphorylation events depending upon a PP2A phosphatase activity would also occur. These events lead to a de-repression of the AtFer1 gene expression (Arnaud et al., 2006). The corresponding ferritin transcript is then translated to give the ferritin precursor polypeptide which is transported to plastids where it is assembled in the 24-mers ferritin protein.