Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis

N H Cheng, J K Pittman, T Shigaki, J Lachmansingh, S LeClere, Brett Lahner, David Edward Salt, K D Hirschi

Research output: Contribution to journalArticle

124 Citations (Scopus)

Abstract

Cation levels within the cytosol are coordinated by a network of transporters. Here, we examine the functional roles of calcium exchanger 1 ( CAX1), a vacuolar H+/Ca2+ transporter, and the closely related transporter CAX3. We demonstrate that like CAX1, CAX3 is also localized to the tonoplast. We show that CAX1 is predominately expressed in leaves, while CAX3 is highly expressed in roots. Previously, using a yeast assay, we demonstrated that an N-terminal truncation of CAX1 functions as an H+/Ca2+ transporter. Here, we use the same yeast assay to show that full-length CAX1 and full-length CAX3 can partially, but not fully, suppress the Ca2+ hypersensitive yeast phenotype and coexpression of full-length CAX1 and CAX3 conferred phenotypes not produced when either transporter was expressed individually. In planta, CAX3 null alleles were modestly sensitive to exogenous Ca2+ and also displayed a 22% reduction in vacuolar H+-ATPase activity. cax1/cax3 double mutants displayed a severe reduction in growth, including leaf tip and flower necrosis and pronounced sensitivity to exogenous Ca2+ and other ions. These growth defects were partially suppressed by addition of exogenous Mg2+. The double mutant displayed a 42% decrease in vacuolar H+/Ca2+ transport, and a 47% decrease in H+-ATPase activity. While the ionome of cax1 and cax3 lines were modestly perturbed, the cax1/cax3 lines displayed increased PO 32 4, Mn2+, and Zn2+ and decreased Ca2+ and Mg2+ in shoot tissue. These findings suggest synergistic function of CAX1 and CAX3 in plant growth and nutrient acquisition.

Original languageEnglish
Pages (from-to)2048-2060
Number of pages13
JournalPlant Physiology
Volume138
Issue number4
DOIs
Publication statusPublished - Aug 2005

Keywords

  • cytosolic CA2+ levels
  • Saccharomyces cerevisiae
  • protein interactions
  • H+/CA2+ antiporter
  • cation transporter
  • guard cells
  • H+-atpase
  • expression
  • thaliana
  • tobacco

Cite this

Cheng, N. H., Pittman, J. K., Shigaki, T., Lachmansingh, J., LeClere, S., Lahner, B., ... Hirschi, K. D. (2005). Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. Plant Physiology, 138(4), 2048-2060. https://doi.org/10.1104/pp.105.061218

Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. / Cheng, N H ; Pittman, J K ; Shigaki, T ; Lachmansingh, J ; LeClere, S ; Lahner, Brett; Salt, David Edward; Hirschi, K D .

In: Plant Physiology, Vol. 138, No. 4, 08.2005, p. 2048-2060.

Research output: Contribution to journalArticle

Cheng, NH, Pittman, JK, Shigaki, T, Lachmansingh, J, LeClere, S, Lahner, B, Salt, DE & Hirschi, KD 2005, 'Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis', Plant Physiology, vol. 138, no. 4, pp. 2048-2060. https://doi.org/10.1104/pp.105.061218
Cheng NH, Pittman JK, Shigaki T, Lachmansingh J, LeClere S, Lahner B et al. Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. Plant Physiology. 2005 Aug;138(4):2048-2060. https://doi.org/10.1104/pp.105.061218
Cheng, N H ; Pittman, J K ; Shigaki, T ; Lachmansingh, J ; LeClere, S ; Lahner, Brett ; Salt, David Edward ; Hirschi, K D . / Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. In: Plant Physiology. 2005 ; Vol. 138, No. 4. pp. 2048-2060.
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AU - Cheng, N H

AU - Pittman, J K

AU - Shigaki, T

AU - Lachmansingh, J

AU - LeClere, S

AU - Lahner, Brett

AU - Salt, David Edward

AU - Hirschi, K D

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N2 - Cation levels within the cytosol are coordinated by a network of transporters. Here, we examine the functional roles of calcium exchanger 1 ( CAX1), a vacuolar H+/Ca2+ transporter, and the closely related transporter CAX3. We demonstrate that like CAX1, CAX3 is also localized to the tonoplast. We show that CAX1 is predominately expressed in leaves, while CAX3 is highly expressed in roots. Previously, using a yeast assay, we demonstrated that an N-terminal truncation of CAX1 functions as an H+/Ca2+ transporter. Here, we use the same yeast assay to show that full-length CAX1 and full-length CAX3 can partially, but not fully, suppress the Ca2+ hypersensitive yeast phenotype and coexpression of full-length CAX1 and CAX3 conferred phenotypes not produced when either transporter was expressed individually. In planta, CAX3 null alleles were modestly sensitive to exogenous Ca2+ and also displayed a 22% reduction in vacuolar H+-ATPase activity. cax1/cax3 double mutants displayed a severe reduction in growth, including leaf tip and flower necrosis and pronounced sensitivity to exogenous Ca2+ and other ions. These growth defects were partially suppressed by addition of exogenous Mg2+. The double mutant displayed a 42% decrease in vacuolar H+/Ca2+ transport, and a 47% decrease in H+-ATPase activity. While the ionome of cax1 and cax3 lines were modestly perturbed, the cax1/cax3 lines displayed increased PO 32 4, Mn2+, and Zn2+ and decreased Ca2+ and Mg2+ in shoot tissue. These findings suggest synergistic function of CAX1 and CAX3 in plant growth and nutrient acquisition.

AB - Cation levels within the cytosol are coordinated by a network of transporters. Here, we examine the functional roles of calcium exchanger 1 ( CAX1), a vacuolar H+/Ca2+ transporter, and the closely related transporter CAX3. We demonstrate that like CAX1, CAX3 is also localized to the tonoplast. We show that CAX1 is predominately expressed in leaves, while CAX3 is highly expressed in roots. Previously, using a yeast assay, we demonstrated that an N-terminal truncation of CAX1 functions as an H+/Ca2+ transporter. Here, we use the same yeast assay to show that full-length CAX1 and full-length CAX3 can partially, but not fully, suppress the Ca2+ hypersensitive yeast phenotype and coexpression of full-length CAX1 and CAX3 conferred phenotypes not produced when either transporter was expressed individually. In planta, CAX3 null alleles were modestly sensitive to exogenous Ca2+ and also displayed a 22% reduction in vacuolar H+-ATPase activity. cax1/cax3 double mutants displayed a severe reduction in growth, including leaf tip and flower necrosis and pronounced sensitivity to exogenous Ca2+ and other ions. These growth defects were partially suppressed by addition of exogenous Mg2+. The double mutant displayed a 42% decrease in vacuolar H+/Ca2+ transport, and a 47% decrease in H+-ATPase activity. While the ionome of cax1 and cax3 lines were modestly perturbed, the cax1/cax3 lines displayed increased PO 32 4, Mn2+, and Zn2+ and decreased Ca2+ and Mg2+ in shoot tissue. These findings suggest synergistic function of CAX1 and CAX3 in plant growth and nutrient acquisition.

KW - cytosolic CA2+ levels

KW - Saccharomyces cerevisiae

KW - protein interactions

KW - H+/CA2+ antiporter

KW - cation transporter

KW - guard cells

KW - H+-atpase

KW - expression

KW - thaliana

KW - tobacco

U2 - 10.1104/pp.105.061218

DO - 10.1104/pp.105.061218

M3 - Article

VL - 138

SP - 2048

EP - 2060

JO - Plant Physiology

JF - Plant Physiology

SN - 0032-0889

IS - 4

ER -