OPT3 Transports Copper to the Phloem, Mediates Shoot-to-Root Copper Signaling andCrosstalk Between Copper and Iron Homeostasis in A. thaliana

Copper and iron are essential micronutrients but are toxic when accumulating in cells in excess. Thus, their uptake by roots is tightly regulated. While plants sense and respond to local copper availability, the systemic regulation of copper uptake has not been documented. By contrast, both local and systemic control for iron uptake has been reported. Iron abundance in the phloem has been suggested to act systemically, regulating the expression of iron uptake genes in the root. Consistently, shoot-to-root iron signaling is disrupted in A. thaliana mutants lacking the phloem companion cell-localized iron transporter, AtOPT3: opt3 mutants overaccumulate iron in leaves while constitutively upregulating iron deficiency-responsive genes in roots. We report that AtOPT3 transports copper and mediates its delivery from source leaves to sinks including young leaves and developing embryos. Consequently, the opt3 mutant accumulates less copper in the phloem, is sensitive to copper deficiency, and mounts transcriptional copper deficiency response in roots. Copper rescues these defects. Notably, feeding the opt3 mutant with copper or iron via the phloem in leaves downregulates the expression of both copper and iron-deficiency marker genes in roots, suggesting that copper and iron can substitute each others function in the phloem in shoot-to-root communication. One-sentence summaryAtOPT3 loads copper and iron into the phloem companion cells, for subsequent distribution to sink tissues and systemic signaling of copper and iron deficiency.