Ferritin Overexpression In Transgenic Plants And Its Consequences

Iron accumulation in various plant tissues is under genetic control and this is evidenced by alteration of Fe homeostasis either in plant mutants altered in Fe signalling or in transgenic plants overexpressing ferritin ectopically.

Our knowledge of the role that ferritins play in plant physiology is still very limited. Their functions have been recently addressed by an approach based on their over-expression in transgenic plants, either in the plastids (their natural cytological localization) or in the cytoplasm, to evaluate the consequences of such a deregulation on plant development and physiology (Deak et al., 1999; Goto et al., 1999; Van Wuytswinkel et al., 1999). An illegitimate ferritin accumulation was obtained in leaves and in seeds. Although no major phenotypic alterations were reported to occur in these transgenic plants, in tobacco leaves grown in vitro on a media containing 25 ^M Fe(III)-EDTA yellow zones were observed, consistent with a 20% decrease in chlorophyll concentration. Indeed, in these plants, some chloroplasts had an altered sub-structure with diffused thylakoids, and large stromal areas with very weak electron density (Briat et al., 1999).

Iron and oxygen metabolisms can interact to promote oxidative stress. Therefore, Fe sequestration in ferritin of transformed plants could have a beneficial effect against Fe-mediated oxidative stress. Methylviologen, the active molecule of the herbicide paraquat, acts by promoting an oxidative stress in the chloroplast, leading to proteolysis, lipid peroxidation and ultimately to cell death (Dodge, 1994). The toxic effect of methyl viologen requires free Fe to take place, and can be antagonized by Fe chelators such as desferrioxamine (Korbaschi et al., 1986; Zer et al., 1994). Indeed plants overexpressing ferritin are more resistant to methylviologen toxicity, confirming that the transgenic ferritins were functional in vivo - i.e. able to sequester Fe atoms (Deak et al., 1999; Van Wuytswinkel et al., 1999). However, it has been documented in animal cells, that ferritin can act either as anti- or pro-oxidant (Cairo et al., 1995). Therefore, the increased resistance to paraquat treatment mentioned above could have also resulted, at least in part, from a general activation of plant defense against oxidative stress generated in response to illegitimate accumulation of ferritin in leaves. This point was addressed by measuring various enzyme activities involved in oxygen detoxification in leaf discs of control tobacco plants, and tobacco plants overexpressing ferritin. All the enzyme activities measured (catalase, ascorbate peroxidase, guaiacol peroxidase and glutathione reductase) were indeed increased by 1.5- to 3-fold in the ferritin overexpressors (Briat et al., 1999). Therefore, although resistant to methylviologen treatment, transgenic tobacco plants overexpressing ferritin experience an oxidative stress.

The major consequence of the ferritin accumulation in transgenic plants was to increase leaf or seed Fe concentration by 2- to 3-fold (Goto et al., 1999; Van Wuytswinkel et al., 1999), concomitantly with an increase in root ferric reductase and root H+ - ATPase activities (Vansuyt et al., 2000; Vansuyt et al., 2003; Van Wuytswinkel et al., 1999), two key determinants of Fe uptake by dicotyledonous plants (Curie and Briat, 2003). This can be explained by the increased Fe storage capacity of the ferritin overexpressing plants in which excessive Fe sequestration disturb the metabolism, driving leaf physiology towards an Fe deficient state. As a consequence the transgenic plants, sensing an Fe deficiency, logically activate the Fe uptake systems (Curie and Briat, 2003). Such a situation of increased Fe uptake in plants which sense their Fe status as deficient whereas they paradoxically accumulate too much Fe has already been described in the case of the brz and dgl pea mutants (Grusak and Pezeshgi, 1996; Marinos, 1967), and of the chloronerva tomato mutant (Ling et al., 1999). However, the mechanism of Fe over-accumulation in these mutant plants differs regarding ferritin synthesis, which was observed to be activated in brz and dgl pea mutants (Becker et al., 1998) but not in chloronerva tomato mutant (Becker et al., 1995).

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