Where do root exudates come from? Metabolic reprogramming under nutrient deficiency: Fe nutrition as a case study

Root exudates could be considered as communicating molecules used by plants to interact with soil. In response to particular environmental conditions, plants specifically synthetize such molecules by the induction of specific reprogramming of the whole metabolism. Therefore, to fully understand the origin of root exudates, the investigation on the metabolic adjusted mechanisms induced in plants by soil factors becomes crucial. Iron (Fe) deficiency chlorosis is a major nutritional disorder for crops growing in calcareous soils, causing decrease in vegetative growth. Notwithstanding its abundance Fe mainly exists, in well aerated soils, as scarcely soluble compounds not freely available to plant uptake. However, Fe is an essential element for the plant growth, since it is fundamental in many metabolic reactions. Indeed, Fe is required as cofactor for a wide range of enzymes belonging to both respiratory and photosynthetic electron transport chains in mitochondria and in chloroplast, respectively. Therefore, its imbalance would affect the whole cellular metabolism, leading to a decrease in crop yield. To overcome this nutritional disorder, plants have evolved particular adapting strategies aimed at reprogramming the whole metabolism in order to take up more Fe from soil and to survive in a low Fe condition at the same time (for instance the induction of glycolysis and fermentative pathways bypassing the affected mitochondrial functionality). Under Fe deficiency several plant species extrude a huge amount of compounds/metabolites (ROCs) into the root apoplast and rhizosphere. The main ROCs are i) carboxylates (i.e. citrate and malate), originated by the primary metabolism and ii) a plethora of compounds such as phenolics and flavins, which are produced by the secondary metabolism. Iron deficiency affects mitochondrial activity in root tissues leading to an accumulation of carboxylate compounds which provide, for instance, carbon skeletons to chlorotic leaves as well as reducing equivalents for Fe uptake mechanisms. Carboxylates act also inside the plant as Fe-chelators, allowing Fe translocation through the plant,. As well, phenols act as Fe-chelators in plant tissues. It was demonstrated that phenolics could play an important role in facilitating the reutilization of apoplastic Fe in roots. Under Fe deficiency, carbohydrates could be diverted into secondary metabolism to produce phenols, which can be accumulated in plant tissues and/or extruded into the rhizosphere. Both oxidative pentose phosphate pathway and Calvin cycle provide carbon skeletons as erythrose-4-phosphate, which along with PEP formed from glycolysis, are used as precursors for the shikimic acid pathway. This pathway converts carbohydrates into aromatic amino acids leading to the synthesis of various phenolic compounds. All the findings obtained so far suggest that root exudates can be synthesized both as a specific response to mobilize Fe compounds outside the cell (i.e. phenols) and as unused/accumulated compounds in the cell (i.e. Rbfl, citrate/malate) as a result of reprogramming some metabolism pathways in response to Fe deficiency.