The CTR/COPT-dependent copper uptake and SPL7-dependent copper deficiency responses are required for basal cadmium tolerance in A. thaliana

Sheena R Gayomba, Ha-Il Jung, Jiapei Yan, John Danku, Michael A Rutzke, Maria Bernal, Ute Krämer, Leon V Kochian, David E Salt, Olena K Vatamaniuk

Research output: Contribution to journalArticle

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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.
Original languageEnglish
Pages (from-to)1262-1275
Number of pages14
JournalMetallomics
Volume5
Issue number9
Early online date12 Jun 2013
DOIs
Publication statusPublished - 1 Sep 2013

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Cadmium
Copper
Arabidopsis
Homeostasis
Transcription factors
Poisons
Genetically Modified Plants
Binding sites
Cell membranes
MicroRNAs
Seedlings
Chemical elements
Transcription Factors
Enzymes
Metals
Binding Sites
Cell Membrane
Messenger RNA

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Gayomba, S. R., Jung, H-I., Yan, J., Danku, J., Rutzke, M. A., Bernal, M., ... 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(9), 1262-1275. https://doi.org/10.1039/c3mt00111c

The CTR/COPT-dependent copper uptake and SPL7-dependent copper deficiency responses are required for basal cadmium tolerance in A. thaliana. / Gayomba, Sheena R; Jung, Ha-Il; Yan, Jiapei; Danku, John; Rutzke, Michael A; Bernal, Maria; Krämer, Ute; Kochian, Leon V; Salt, David E; Vatamaniuk, Olena K.

In: Metallomics, Vol. 5, No. 9, 01.09.2013, p. 1262-1275.

Research output: Contribution to journalArticle

Gayomba, SR, Jung, H-I, Yan, J, Danku, J, Rutzke, MA, Bernal, M, Krämer, U, Kochian, LV, Salt, DE & Vatamaniuk, OK 2013, 'The CTR/COPT-dependent copper uptake and SPL7-dependent copper deficiency responses are required for basal cadmium tolerance in A. thaliana', Metallomics, vol. 5, no. 9, pp. 1262-1275. https://doi.org/10.1039/c3mt00111c
Gayomba, Sheena R ; Jung, Ha-Il ; Yan, Jiapei ; Danku, John ; Rutzke, Michael A ; Bernal, Maria ; Krämer, Ute ; Kochian, Leon V ; Salt, David E ; Vatamaniuk, Olena K. / The CTR/COPT-dependent copper uptake and SPL7-dependent copper deficiency responses are required for basal cadmium tolerance in A. thaliana. In: Metallomics. 2013 ; Vol. 5, No. 9. pp. 1262-1275.
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AU - Gayomba, Sheena R

AU - Jung, Ha-Il

AU - Yan, Jiapei

AU - Danku, John

AU - Rutzke, Michael A

AU - Bernal, Maria

AU - Krämer, Ute

AU - Kochian, Leon V

AU - Salt, David E

AU - Vatamaniuk, Olena K

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N2 - 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.

AB - 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.

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