Nitric oxide accumulation is required for molecular and physiological responses to iron deficiency in tomato roots

Iron is an essential and commonly limited nutrient for plants. To increase the uptake of iron during times of low iron supply, plants, except the grasses, activate a set of physiological and morphological responses in their roots that include iron reduction, soil acidification, Fe(II) transport and proliferation of root hairs. It is not known how root cells sense and transduce the changes that occur after the onset of iron deficiency. This work presents evidence that nitric oxide (NO) is produced rapidly in the root epidermis of tomato plants (Solanum lycopersicum) that are grown in iron-deficient conditions. The scavenging of NO prevented iron-deficiency-induced upregulation of the basic helix-loop-helix transcription factor FER, the ferric-chelate reductase LeFRO1 and the Fe(II) transporter LeIRT1 genes. On the other hand, exogenous application of the NO donor S-nitrosoglutathione enhanced the accumulation of FER, LeFRO1 and LeIRT1 mRNA in roots of iron-deficient plants. The activity of the root ferric-chelate reductase and the proliferation of root hairs induced by iron deficiency were stimulated by NO supplementation and suppressed by NO scavenging. Nitric oxide was ineffective in inducing iron-deficiency responses in the tomato fer mutant, which indicates that the FER protein is necessary to mediate the action of NO. Furthermore, NO supplementation improved plant growth under low iron supply, which suggests that NO is a key component of the regulatory mechanisms that control iron uptake and homeostasis in plants. In summary, the results of this investigation indicate that an increase in NO production is an early response of roots to iron deprivation that contributes to the improvement of iron availability by (i) modulating the expression of iron uptake-related genes and (ii) regulating the physiological and morphological adaptive responses of roots to iron-deficient conditions.