title: The CTR/COPT-dependent copper uptake and SPL7-dependent copper deficiency responses are required for basal cadmium tolerance in A. thaliana.
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 that 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 three plasma membrane-localized Cu uptake transporters, COPT1, COPT2 and COPT6. Further analysis of Cd sensitivity of single and triple copt1copt2copt6 mutants, and transgenic plants ectopically expressing COPT6 suggested that Cu uptake is an essential component of Cd resistance in A. thaliana. Analysis of the contribution of the SPL7-dependent pathway to Cd-induced expression of COPT1, COPT2 and COPT6 showed that it occurs, in part, through mimicking the SPL7-dependent transcriptional Cu deficiency response. This response also involves components of the Cu reallocation system, miRNA398, FSD1, CSD1 and CSD2. Furthermore, seedlings of the spl7-1 mutant accumulate up to 2-fold less Cu in roots than the wild-type, are hypersensitive to Cd, and are more sensitive to Cd than the triple copt1copt2copt6 mutant. Together these data show that exposure to excess Cd triggers SPL7-dependent Cu deficiency responses that include Cu uptake and reallocation that are required for basal Cd tolerance in A. thaliana.
authors.affiliation: Department of Crop and Soil Sciences, Cornell University, Ithaca, NY 14853, USA.
authors.forename: Sheena R
authors.initials: SR
authors.lastname: Gayomba
authors.forename: Ha-il
authors.initials: HI
authors.lastname: Jung
authors.forename: Jiapei
authors.initials: J
authors.lastname: Yan
authors.forename: John
authors.initials: J
authors.lastname: Danku
authors.forename: Michael A
authors.initials: MA
authors.lastname: Rutzke
authors.forename: Maria
authors.initials: M
authors.lastname: Bernal
authors.forename: Ute
authors.initials: U
authors.lastname: Krämer
authors.forename: Leon V
authors.initials: LV
authors.lastname: Kochian
authors.forename: David E
authors.initials: DE
authors.lastname: Salt
authors.forename: Olena K
authors.initials: OK
authors.lastname: Vatamaniuk
mesh_terms: D000222:Adaptation, Physiological / Q000187:drug effects / Q000235:genetics; D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002104:Cadmium / Q000494:pharmacology*; D027682:Cation Transport Proteins / Q000235:genetics / Q000378:metabolism; D002462:Cell Membrane / Q000378:metabolism; D003300:Copper / Q000378:metabolism*; D000079923:Copper Transporter 1; D004268:DNA-Binding Proteins / Q000235:genetics / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D005816:Genetic Complementation Test; D006706:Homeostasis / Q000187:drug effects; D026901:Membrane Transport Proteins / Q000235:genetics / Q000378:metabolism; D035683:MicroRNAs / Q000235:genetics; D008856:Microscopy, Fluorescence; D008957:Models, Genetic; D009154:Mutation; D018517:Plant Roots / Q000235:genetics / Q000378:metabolism; D018520:Plant Shoots / Q000235:genetics / Q000378:metabolism; D030821:Plants, Genetically Modified; D020133:Reverse Transcriptase Polymerase Chain Reaction; D000080083:SLC31 Proteins; D012441:Saccharomyces cerevisiae / Q000235:genetics / Q000254:growth & development / Q000378:metabolism; D013482:Superoxide Dismutase / Q000235:genetics / Q000378:metabolism; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism*
chemical_list: D029681:Arabidopsis Proteins; C097086:COPT1 protein, Arabidopsis; C585190:COPT2 protein, Arabidopsis; C576754:COPT6 protein, Arabidopsis; D027682:Cation Transport Proteins; D000079923:Copper Transporter 1; D004268:DNA-Binding Proteins; C543882:MIRN398 microRNA, Arabidopsis; D026901:Membrane Transport Proteins; D035683:MicroRNAs; D000080083:SLC31 Proteins; C483288:SPL7 protein, Arabidopsis; D014157:Transcription Factors; D002104:Cadmium; D003300:Copper; D013482:Superoxide Dismutase; C586060:CSD1 protein, Arabidopsis; C586061:CSD2 protein, Arabidopsis