Loss of OPT3 function decreases phloem copper levels and impairs crosstalk between copper and iron homeostasis and shoot-to-root signaling in Arabidopsis thaliana

Authors: CHIA, JU-CHEN - Cornell University; YAN, JIAPEI - Cornell University; ISHKA, MARYAM - Cornell University; FAULKNER, MARTA - Cornell University; HUANG, RONG - Cornell University; SMIESKA, LOUISA - Cornell University; WOLL, ARTHUR - Cornell University; TAPPERO, RYAN - Brookhaven National Laboratory; KISS, ANDREW - Brookhaven National Laboratory; JIAO, CHEN - Boyce Thompson Institute; FEI, ZHANGJUN - Boyce Thompson Institute; Pineros, Miguel; KOCHIAN, LEON - University Of Saskatchewan; WALKER, ELSBETH - University Of Massachusetts; VATAMANIUK, OLENA - Cornell University

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/17/2023
Publication Date: 2/22/2023
Citation: Chia, J., Yan, J., Ishka, M.R., Faulkner, M.M., Huang, R., Smieska, L., Woll, A., Tappero, R., Kiss, A., Jiao, C., Fei, Z., Pineros, M., Kochian, L., Walker, E., Vatamaniuk, O.K. 2023. Loss of OPT3 function decreases phloem copper levels and impairs crosstalk between copper and iron homeostasis and shoot-to-root signaling in Arabidopsis thaliana. The Plant Cell. 35(6):2157-2185. https://doi.org/10.1093/plcell/koad053.
DOI: https://doi.org/10.1093/plcell/koad053

Interpretive Summary: In plants, copper (Cu) and iron (Fe) are essential micronutrients key to many plant processes. However, since excessive accumulation of these nutrients results in toxicity, the crosstalk among the pathways determining the status of each nutrient is needed to coordinate and synchronize the transport processes. The AtOPT3 transport protein is known to mediate the movement of Fe in the phloem, with Fe concentrations determining and regulating the magnitude of iron uptake to the root. In this work, we show that in addition to Fe, AtOPT3 also loads Cu into the phloem to deliver it to sink regions of the plant for storage. We demonstrate that disrupting the function of the AtOPT3 protein results in a reduction of Cu in the phloem, roots, developing leaves, and embryos. The mechanistic findings increase understanding of Fe-Cu interactions and will assist in devising sustainable approaches for improving plant mineral nutrition in marginal soils where mineral deficiencies are a major obstacle for crop production.

Technical Abstract: Copper and iron are micronutrients but are toxic when they accumulate in cells in excess. Crosstalk between copper and iron homeostasis in Arabidopsis thaliana has been documented and includes iron accumulation under copper deficiency and vice versa. However, molecular components of this crosstalk are not well understood. Iron concentration in the phloem has been suggested to act systemically, negatively regulating iron uptake to the root. Consistently, systemic iron signaling is disrupted in A. thaliana mutants lacking the phloem companion cell-localized iron transporter, AtOPT3, and opt3 mutants hyperaccumulate iron. Here, we report that in addition to iron, AtOPT3 transports copper and mediates copper loading to the phloem for delivery from sources to sinks. As a result of this function, the opt3-3 mutant accumulates less copper in the phloem, roots, developing leaves and embryos compared to wild type, is sensitive to copper deficiency, and mounts transcriptional copper deficiency response. Because copper deficiency has been shown to stimulate iron accumulation, we propose that reduced copper concentration in the phloem of the opt3-3 mutant and its constitutive copper deficiency contribute to iron overaccumulation in its tissues. Our data assign new transport capabilities to AtOPT3 and increase understanding of copper - iron interactions and signaling.