The downregulation of Fe-acquisition genes in the plasma membrane along with antioxidant defense and nitric oxide signaling confers Fe toxicity tolerance in tomato

Abstract

This study illustrates the mechanisms underlying differential tolerance to iron (Fe) toxicity in tomato. Excess Fe exhibited a substantial reduction in morphological parameters in Marglobe (sensitive), while Ratan (tolerant) remained unaffected. Excess Fe increased root and shoot Fe concentrations in Marglobe, but Ratan showed no changes accompanied by the downregulation of SlIRT1 (Fe-regulated transporter 1), SlNRAMP1 (Natural resistance-associated macrophage protein 1), and SlFRO1 (ferric chelate reductase 1) in the roots. Furthermore, the leaf chlorophyll score remained unchanged, but root Fe-chelate reductase substantially decreased in Ratan; while, these features significantly increased in Marglobe following Fe toxicity. The SlIRT1, SlNRAMP1 and SlFRO1 genes are located in the plasma membrane and possess a shared gene network generally consisting of NRAMP1(Natural resistance-associated macrophage protein 1),NRAMP3(Natural resistance-associated macrophage protein 3),FRO1 (ferric chelate reductase 1), FER (BHLH transcriptional regulator) and CHLN (nicotianamine synthase) that are linked to Fe uptake in plants. Further, the quantum yield of PSII in leaf showed no changes, but the photosynthetic performance index, electron transport flux, and active antenna size notably decreased in Marglobe, while Ratan showed steady status. Moreover, Fe toxicity showed an elevation in antioxidant enzymes (SOD, CAT, APX, GR), glutathione, and cysteine in roots of Ratan, providing defense to oxidative damage, while early Fe-toxicity possibly caused oxidative damage before photosynthetic impairment in Marglobe. Additionally, nitric oxide concentration and the expression of SlGSNOR (S-nitrosoglutathione reductase) gene were significantly induced in Ratan while this was unchanged in Marglobe under Fe toxicity. This SlGSNOR gene showed a close relationship with the Arabidopsis homolog, as evident in the sequence alignment. Further, nitric oxide donor improved plant length and biomass even in Marglobe, indicating the possible association of nitric oxide signaling in Fe-toxicity tolerance in tomato. This is the first to show the mechanistic consequence of differential tolerance to Fe toxicity in tomato.