RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis

Takashi Hirayama; Joseph J. Kieber; Noriko Hirayama; Mikhail Kogan; Plinio Guzman; Saeid Nourizadeh; Jose M. Alonso; William P. Dailey; Andrew Dancis; Joseph R. Ecker

doi:10.1016/S0092-8674(00)80747-3

RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis

Takashi Hirayama, Joseph J. Kieber, Noriko Hirayama, Mikhail Kogan, Plinio Guzman, Saeid Nourizadeh, Jose M. Alonso, William P. Dailey, Andrew Dancis, Joseph R. Ecker

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323 Citations (Scopus)

Abstract

Ethylene is an important regulator of plant growth. We identified an Arabidopsis mutant, responsive-to-antagonist1 (ran1), that shows ethylene phenotypes in response to treatment with trans-cyclooctene, a potent receptor antagonist. Genetic epistasis studies revealed an early requirement for RAN1 in the ethylene pathway. RAN1 was cloned and found to encode a protein with similarity to copper-transporting P-type ATPases, including the human Menkes/Wilson proteins and yeast Ccc2p. Expression of RAN1 complemented the defects of a ccc2Δ mutant, demonstrating its function as a copper transporter. Transgenic CaMV 35S::RAN1 plants showed constitutive expression of ethylene responses, due to cosuppression of RAN1. These results provide an in planta demonstration that ethylene signaling requires copper and reveal that RAN1 acts by delivering copper to create functional hormone receptors.

Original language	English
Pages (from-to)	383-393
Number of pages	11
Journal	Cell
Volume	97
Issue number	3
DOIs	https://doi.org/10.1016/S0092-8674(00)80747-3
Publication status	Published - Apr 30 1999
Externally published	Yes

ASJC Scopus subject areas

Biochemistry, Genetics and Molecular Biology(all)

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10.1016/S0092-8674(00)80747-3

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@article{c76ef54e9edf407e9238e68d4ce335b8,

title = "RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis",

abstract = "Ethylene is an important regulator of plant growth. We identified an Arabidopsis mutant, responsive-to-antagonist1 (ran1), that shows ethylene phenotypes in response to treatment with trans-cyclooctene, a potent receptor antagonist. Genetic epistasis studies revealed an early requirement for RAN1 in the ethylene pathway. RAN1 was cloned and found to encode a protein with similarity to copper-transporting P-type ATPases, including the human Menkes/Wilson proteins and yeast Ccc2p. Expression of RAN1 complemented the defects of a ccc2Δ mutant, demonstrating its function as a copper transporter. Transgenic CaMV 35S::RAN1 plants showed constitutive expression of ethylene responses, due to cosuppression of RAN1. These results provide an in planta demonstration that ethylene signaling requires copper and reveal that RAN1 acts by delivering copper to create functional hormone receptors.",

author = "Takashi Hirayama and Kieber, {Joseph J.} and Noriko Hirayama and Mikhail Kogan and Plinio Guzman and Saeid Nourizadeh and Alonso, {Jose M.} and Dailey, {William P.} and Andrew Dancis and Ecker, {Joseph R.}",

note = "Funding Information: We thank E. C. Sisler for kindly providing MCP; P. A. Rea for the pYES3 vector; H. Siomi for anti-HA antibody; and P. Johnson, R. Solano, A. Stepanova, and H. Yoshida for critical reading of the manuscript. T. H. acknowledges support from the Institute of Physical and Chemical Research (RIKEN) and a long-term fellowship from the Human Frontier Science Program Organization (LT-391/96). This work has been supported in part by grants from the National Science Foundation, the United States Department of Energy, and the National Institutes of Health to J. R. E. ",

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doi = "10.1016/S0092-8674(00)80747-3",

language = "English",

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T1 - RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis

AU - Hirayama, Takashi

AU - Kieber, Joseph J.

AU - Hirayama, Noriko

AU - Kogan, Mikhail

AU - Guzman, Plinio

AU - Nourizadeh, Saeid

AU - Alonso, Jose M.

AU - Dailey, William P.

AU - Dancis, Andrew

AU - Ecker, Joseph R.

N1 - Funding Information: We thank E. C. Sisler for kindly providing MCP; P. A. Rea for the pYES3 vector; H. Siomi for anti-HA antibody; and P. Johnson, R. Solano, A. Stepanova, and H. Yoshida for critical reading of the manuscript. T. H. acknowledges support from the Institute of Physical and Chemical Research (RIKEN) and a long-term fellowship from the Human Frontier Science Program Organization (LT-391/96). This work has been supported in part by grants from the National Science Foundation, the United States Department of Energy, and the National Institutes of Health to J. R. E.

PY - 1999/4/30

Y1 - 1999/4/30

N2 - Ethylene is an important regulator of plant growth. We identified an Arabidopsis mutant, responsive-to-antagonist1 (ran1), that shows ethylene phenotypes in response to treatment with trans-cyclooctene, a potent receptor antagonist. Genetic epistasis studies revealed an early requirement for RAN1 in the ethylene pathway. RAN1 was cloned and found to encode a protein with similarity to copper-transporting P-type ATPases, including the human Menkes/Wilson proteins and yeast Ccc2p. Expression of RAN1 complemented the defects of a ccc2Δ mutant, demonstrating its function as a copper transporter. Transgenic CaMV 35S::RAN1 plants showed constitutive expression of ethylene responses, due to cosuppression of RAN1. These results provide an in planta demonstration that ethylene signaling requires copper and reveal that RAN1 acts by delivering copper to create functional hormone receptors.

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RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis

Abstract

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