This study aimed to elucidate the physiological, biochemical, and transcriptional regulatory responses of potato plants to iron deficiency stress. Two potato varieties were selected for analysis: 05P (high tuber iron content) and CI5 (low tuber iron content). Tissue culture seedlings of both varieties were subjected to iron deficiency, and the effects on stem length, root length, fresh weight, soluble sugar and protein contents, as well as the activities of superoxide dismutase (SOD), peroxidase (POD), malondialdehyde (MDA), and leaf chlorophyll content (SPAD) values were evaluated. Additionally, the impact of iron deficiency on zinc (Zn), magnesium (Mg), calcium (Ca), manganese (Mn), and copper (Cu) concentrations in different tissues were analyzed. Transcriptomic sequencing and quantitative real-time PCR (qRT-PCR) were performed on various seedling tissues. The results showed that iron deficiency significantly inhibited seedling growth and development, resulting in reduced plant height and fresh weight, increased root length, decreased leaf SPAD content, and elevated soluble sugar and protein concentration. SOD, POD, and MDA activities were also significantly increased. Elemental analysis revealed that iron deficiency enhanced the uptake and accumulation of Zn, Mg, Ca, Mn, and Cu across different tissues. Transcriptomic analysis identified differentially expressed genes (DEGs) significantly enriched in pathways related to photosynthesis, carbon metabolism, and ribosome function in roots, stems, and leaves. Iron deficiency induced the upregulation of H⁺-ATPase genes in roots (PGSC0003DMG400004101, PGSC0003DMG400033034), acidifying the rhizosphere to increase active iron availability. Subsequently, this was followed by the upregulation of FRO genes (PGSC0003DMG400000184, PGSC0003DMG400010125, PGSC0003DMG401009494, PGSC0003DMG401018223), which reduce Fe³⁺ to Fe²⁺, and activation of IRT genes, facilitating Fe²⁺ transport to various tissues. Iron deficiency also reduced SPAD content in leaves, negatively impacting photosynthesis and overall plant growth. In response, the osmotic regulation and antioxidant defense systems were activated, enabling the plant to mitigate iron deficiency stress. Additionally, the absorption and accumulation of other metal ions were enhanced, likely as a compensatory mechanism for iron scarcity. At the transcriptional level, iron deficiency induced the expression of genes involved in metal absorption and transport, as well as those related to photosynthesis, carbon metabolism, and ribosomal function, thereby supporting iron homeostasis and maintaining metabolic balance under stress conditions.

Iron (Fe) is an essential micronutrient for plant growth, serving as a cofactor in chlorophyll synthesis, photosynthetic electron transport, and redox reactions. Both Fe deficiency and excess disrupt mineral nutrient homeostasis, but the ionomic and transcriptomic mechanisms underlying genotype-specific responses in potato remain elusive. We profiled the ionome and transcriptome of two potato genotypes, 05P and CI5, grown under Fe-deficient, Fe-sufficient and Fe-excess conditions represented by 1, 40.4 and 120 mg L⁻¹ FeNaEDTA, respectively. Ionomic analysis detected significant alterations in Fe, Mn, Zn, Ca, Mg, and Cu concentrations across roots, stems, and leaves, with the direction and magnitude of change varying by organ and genotype. Under Fe deficiency, CI5 showed steeper declines in root and stem Fe than 05P, while 05P retained higher leaf Fe, reflecting genotype-dependent patterns of shoot Fe distribution. Fe excess caused Fe accumulation in both genotypes, but coincided with Mn depletion in shoots, raising Fe/Mn ratios, consistent with potential antagonistic Fe–Mn interactions at the transport level. This pattern is consistent with potential antagonistic Fe–Mn interactions, although alternative mechanisms such as Mn uptake inhibition or dilution effects cannot be ruled out without direct experimental evidence. Transcriptome analysis showed organ-biased responses: Fe deficiency upregulated more genes in stems, whereas Fe excess triggered stronger transcriptional shifts in roots. No KEGG pathways remained significant after false discovery rate (FDR) correction, suggesting that genotype-dependent Fe-responsive divergence was not concentrated in a limited number of canonical KEGG pathways under the present analytical framework. Joint analysis of ionomic and transcriptomic data highlighted ferric-chelate reductase oxidase (FRO) and zinc-regulated transporter/iron-regulated transporter-like protein (IRT/ZIP) family members as genes associated with Fe reduction, divalent metal uptake, and Fe–Mn balance based on differential expression and orthology with functionally characterized Arabidopsis homologs. Comparative genomics showed that FRO and ZIP families have expanded in potato, with conserved domain architectures but divergent gene structures and promoter architectures, consistent with potential functional diversification related to metal transport. In conclusion, under Fe deficiency, genotype-dependent transcriptional divergence was most pronounced in stems, whereas under Fe excess it was more evident in roots, jointly maintaining systemic Fe–Mn homeostasis in potato.