|ZHIYANG, ZHAI - Cornell University|
|GAYOMBA, SHEENA - Cornell University|
|JUNG, HA-IL - Cornell University|
|VIMALAKUMAR, NANDITHA - Cornell University|
|RUTZKE, MIKE - Cornell University|
|DANKU, JOHN - University Of Aberdeen|
|LAHNER, BRETT - Purdue University|
|PUNSHON, TRACY - Dartmouth University|
|GUERINOT, MARY LOU - Dartmouth University|
|SALT, DAVID - University Of Aberdeen|
|VATAMANIUK, OLENA - Cornell University|
Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/22/2014
Publication Date: 5/1/2014
Citation: Zhiyang, Z., Gayomba, S.R., Jung, H., Vimalakumar, N.K., Pineros, M., Rutzke, M., Danku, J., Lahner, B., Punshon, T., Guerinot, M., Salt, D.D., Kochian, L.V., Vatamaniuk, O.K. 2014. OPT3 is a phloem-specific iron transporter that is essential for systemic iron signaling and redistribution of iron and cadmium in arabidopsis. The Plant Cell. DOI: http:dx.doi.org/10.1105/tpc.114.123737.
Interpretive Summary: Although the adverse health effects of heavy metals have been known for a long time, exposure to heavy metals continues and is increasing, due to their continued production and emission into the environment from mining, smelting, electroplating, and the use of products such as fertilizers, nickel/cadmium batteries, pigments, and plastics. Since heavy metals are not biodegradable and have a low excretion rate (e.g. cadmium has a biological half-life of 15-30 years), exposure to heavy metals leads to their accumulation in vital organs, causing neurodegenerative conditions and cancer. At the cellular level, the toxicity of heavy metals results from the displacement of naturally occurring co-factors from their cellular binding sites, resulting in damaged proteins and enzymes, and promotion of the formation of toxic reactive oxygen species. Understanding the cellular mechanisms of heavy metal transport, accumulation and detoxification is critical for the cure and prevention of heavy metal-caused diseases and for developing effective strategies for remediation of contaminated environments using plants. In this study, several model systems for human and plant heavy metal uptake and detoxification were used, including yeast and the plant model species, Arabidopsis thaliana. Novel findings were presented identifying a new transporter that is a key player in long distance transport of iron to the plant seed, which has implications for improving edible plant tissues as a source of iron for humans. Also, we found that this transporter also mediates the transport of the toxic heavy metal cadmium from the root to the shoot after its absorption into roots in heavy metal-contaminated soils. These new findings identify a novel target for genetic manipulation with regards to three important areas for humans: 1) preventing heavy metals from entering the food chain via transport to the edible portions of food crops, 2) developing plant species that can accumulate toxic metals in the shoot for the remediation of metal-contaminated soils (phytoremediation); 3) improving the iron content of staple food crops grown on normal soils not contaminated with cadmium or other heavy metals.
Technical Abstract: Iron is essential for both plant growth and human health and nutrition. Cadmium, on the other hand, is a non-essential and highly toxic element that competes with iron for uptake and partitioning in plant tissues, posing a threat to crop productivity and human health. Knowledge of signaling mechanisms that communicate iron demand from shoots to roots to regulate iron uptake and partitioning, and molecular events underlying crosstalk between iron signaling and cadmium uptake are critical for the development of biofortification strategies and “cadmium-safe” crops. We show here that the Arabidopsis thaliana oligopeptide transporter, OPT3, previously implicated in iron homeostasis, is transcriptionally induced by cadmium and contributes to cadmium root-to-shoot partitioning and toxicity. Comprehensive analysis of the role of OPT3 in cadmium redistribution and its relationship to iron homeostasis revealed that OPT3 is expressed in the phloem and is a plasma membrane transporter capable of transporting cadmium and iron ions in vitro. Studies in Arabidopsis showed that OPT3 loads iron into the phloem and controls both shoot-to-root iron signaling and iron redistribution from mature to developing tissues. Although OPT3 transports cadmium, its role in root-to-shoot cadmium partitioning is an indirect effect of its main role in orchestrating shoot-to-root iron signaling: disruption of OPT3 function alters expression of genes encoding multispecific transition ion transporters, which mediate vacuolar cadmium sequestration, resulting in retention of cadmium in the root. The reported results also highlight the role of iron in the phloem in systemic signaling and uncover a novel function for the oligopeptide transporter family member in transport of transition elements.