|GAYUMBA, SHEENA - Cornell University|
|JUNG, HA-IL - Cornell University|
|YAN, JIAPEI - Cornell University|
|DANKU, JOHN - University Of Aberdeen|
|RUTZKE, MICHAEL - Cornell University|
|BERNAL, MARIA - University Of Bochum|
|KRAMER, UTE - University Of Bochum|
|SALT, DAVID - University Of Aberdeen|
|VATAMANIUK, OLENA - Cornell University|
Submitted to: Metallomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/12/2013
Publication Date: 7/30/2013
Citation: Gayumba, S., Jung, H., Yan, J., Danku, J., Rutzke, M.A., Bernal, M., Kramer, U., Kochian, L.V., Salt, D.E., Vatamaniuk, O.K. 2013. The CTR/COPT-dependent copper uptake and SPL7-dependent copper deficiency responses are required for basal cadmium tolerance in A. thaliana. Metallomics. 5:1262-1275. DOI: 10.1039/c3mt00111c
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, batteries, pigments, and plastics. Heavy metals enter the food chain via uptake into plants and heavy metals such as cadmium, (Cd), which is the focus of this study, cause cellular toxicity due to 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. Therefore for toxic heavy metals such as Cd, understanding the cellular mechanisms 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, the plant model species, Arabidopsis thaliana, was used to study Cd toxicity and tolerance. It was found that Cd turns on the molecular systems involved in regulating copper (Cu) nutrition, including several Cu transporters and how Cu is allocated throughout the plant. Cu is an essential micronutrient and Cu ions are similar in size and charge to Cd ions. Hence it appears that Cd enters the plant via Cu transporters and an important aspect of Cd toxicity is disruption of the control of Cu nutrition. These findings indicate that maintaining plant Cu nutrition is an essential aspect of how plants tolerate Cd. These new findings identify a novel target for genetic manipulation with regards to preventing heavy metals from entering the food chain via transport to the edible portions of food crops, and also may be useful in designing plants to use for the cleanup of soils contaminated with toxic metals.
Technical Abstract: Copper (Cu) homeostasis in plants is maintained by at least two mechanisms: 1) the miRNA-dependent reallocation of intracellular Cu among major Cu-enzymes and important energy-related functions; 2) the regulation of the expression of Cu transporters including members of the CTR/COPT family. These events are controlled by the transcription factor SPL7 in Arabidopsis thaliana. Cadmium (Cd), on the other hand, is a non-essential and a highly toxic metal, which interferes with homeostasis of essential elements by competing for cellular binding sites. Whether Cd affects Cu homeostasis in plants is unknown. We found that Cd stimulates Cu accumulation in roots of A. thaliana and increases mRNA expression of two CTR/COPT transporters, COPT2 and COPT6. Subsequent characterization of COPT2 revealed that it is a plasma membrane Cu uptake transporter, which expression is restricted mainly to roots where it is induced in both, Cu-deficient and Cd-toxic, environments. The heterologous expression of COPT2 or COPT6 in the S. cerevisiae Cu uptake mutant rescues its Cd sensitivity through Cu uptake. Analyses of the contribution of the SPL7-dependent pathway to Cd-induced expression of COPT2 and COPT6 showed that it occurs through mimicking the SPL7-dependent transcriptional Cu deficiency response. This response involves, in addition to COPT2 and COPT6, components of the Cu reallocation system, miRNA398, FSD1, CSD1 and CSD2. Furthermore, seedlings of the spl7-1 mutant are hypersensitive to Cd and accumulate up to 2-fold less Cu in roots then the wild-type. Together these data suggest that maintaining SPL7-dependent Cu homeostasis through at a minimum Cu uptake and intracellular Cu reallocation are essential for Cd resistance in A. thaliana.