Soil metals, chloroplasts, and secure crop production: a review

An increasing number of soils of poor quality with unbalanced metal concentrations are used worldwide for crop cultivation. Even though plants are able to develop strategies to cope with metal stress, either metal deficiency or excess, this unbalance affects the whole plant. Chloroplasts are key organelles for organic matter synthesis and biomass production. Under metal stress, chloroplasts suffer severe alterations of their ultrastructure, associated with profound molecular and metabolic damages. These alterations are accompanied by unbalanced metal distribution in plants, in particular in edible crop organs. Toxic metals get either accumulated or there is a deficiency of nutrients, resulting in a weak nutritional value. Nonetheless, there is more and more knowledge on the functioning and regulation of metal transporters in plants. Such knowledge will allow growing crops with well-balanced metal concentrations in edible parts even on metal unbalanced soils. This review shows that almost all vital functions of chloroplasts, such as photosynthesis, CO2 fixation, nitrogen and sulfur assimilation, and protein and nucleic acid metabolism, require metals. Therefore, the uptake of essential metals is necessary for the proper functioning of chloroplasts and, in turn, for crop productivity. We describe nutrient uptake mechanisms of plants and processes that influence essential and non-essential metal concentrations in different plant organs. We present an overview of metal transporters in chloroplasts. Several questions still need to be elucidated about the uptake and the trafficking of essential and non-essential metals into and within chloroplasts. Similarly to transporters present in other cellular compartments, the carriers are often not metal-specific. Therefore, essential and non-essential metals may compete for carriers. As a result, unbalanced soil metal concentrations can be reflected in the plants and in the chloroplasts. Metal deficiency or excess causes reduced growth and decreased productivity of crops. It can lead to human malnutrition. Several complex physiological processes can be responsible for the reduced biomass observed in plants with unbalanced metal concentration. In this review, we have focused on the structural and functional alterations of chloroplasts under metal deficiency or excess. Interestingly, besides specific differences, our data indicate several similarities in the response of chloroplasts to metal deficiency or excess. Indeed, oxidative stress and several ultrastructural alterations, e.g., increase in the number and size of plastoglobuli, disorganized grana and disturbed thylakoids, and swelling of the intrathylakoidal space, are observed in both cases. This indicates that changes in chloroplast ion homeostasis rather than the specific effect of a metal are responsible for decreased plant productivity. Therefore, sustainable agriculture has to take into consideration solutions that enable undisturbed metal and ion homeostasis in chloroplasts of crop plants grown even in soils with unbalanced metal concentrations.