Fig. 3 in Zinc uptake and HMA4 activity are required for micro- and macroelement balance in tobacco (Nicotiana tabacum)

Fig. 3. Working model of metabolic changes in HMA4-impaired plants based on the gene expression changes observed in the roots and leaves of HMA4 RNAi and HMA4-mutant N. tabacum plants relative to their controls. The lack of HMA4 function causes Zn deficiency in leaves, leading to a local Zn-deficiency response. In roots, a Fe-deficiency response is observed, caused either by a high Zn:Fe ratio in the roots or by a systemic Zn-deficiency signal. The Fe-deficiency signal leads—via the transcription factor FIT1—to upregulation of the Fe- and Mn- transporter genes IRT1 and NRAMP1 and also induces the synthesis and export of iron-binding compounds (IBC), thus additionally assisting Fe uptake. At the same time, a P-deficiency signal involving the transcription factor HHO2 is generated in the leaves. In roots, the P-deficiency signal leads to increased expression of genes encoding acid phosphatases, enabling increased phosphate uptake from the rhizosphere. Consequently, Fe, Mn, Cu, and P accumulate in the leaves. P is stored in vacuoles (via PHT5; 1, PHT5; 3) and also exported to mitochondria and chloroplasts. Cu is detoxified by transport to the chloroplasts, which are a major site of Cu use because of Cu-containing plastocyanin production. However, high levels of Cu are toxic for the photosynthetic electron transport system, especially for photosystem II, which is reflected in the upregulation of PII light harvesting complex genes (LHCB). At the same time, Cu uptake to the cells is limited by downregulation of COPT1. Ion uptake might cause a lower osmotic potential, leading to water influx via various aquaporin genes. High turgor pressure or Fe excess ultimately affects the cell wall, as observed by the increased expression of genes involved in cell wall biosynthesis, expansion, and crosslinking. bHLH115: basic helix-loop-helix transcription factor; CA: carbonic anhydrase; CESA: cellulose synthase; COPT: copper transporter; DMRL: dimethyl-8-ribityllumazine synthase; EXPA: expansin; FIT: FER-like regulator of iron uptake (transcription factor); HHO2: hypersensitivity to low phosphate-elicited primary root shortening 1 homolog 2 (myb-like transcription factor); HMA: heavy metal ATPase; IBC: iron binding compound; IRT: iron-regulated transporter; LAC: laccase; LHCB: photosystem II light harvesting complex; NA: nicotianamine; NAS: nicotianamine synthase; NRAMP: natural resistance-associated macrophage protein (metal ion transporter); PDR: pleiotropic drug resistance (ATP-binding cassette transporter); PHT: phosphate transporter; PIP: plasma membrane intrinsic protein; PME: pectin methyl esterase; PMEI: pectin methyl esterase inhibitor; PRX: peroxidase; RBCS: ribulose bisphosphate carboxylase small chain; TIP: tonoplast intrinsic protein; TBL: TRICHOME BIREFRINGENCE-LIKE (xylan acetylation); ZIP: zinc transporter.