Salt tolerance, salt accumulation, and ionic homeostasis in an epidermal bladder-cell-less mutant of the common ice plant Mesembryanthemum crystallinum

Sakae Agarie, Toshifumi Shimoda, Yumi Shimizu, Kathleen Baumann, Haruki Sunagawa, Ayumu Kondo, Ueno Osamu, Teruhisa Nakahara, Akihiro Nose, John C. Cushman

Research output: Contribution to journalArticle

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Abstract

The aerial surfaces of the common or crystalline ice plant Mesembryanthemum crystallinum L., a halophytic, facultative crassulacean acid metabolism species, are covered with specialized trichome cells called epidermal bladder cells (EBCs). EBCs are thought to serve as a peripheral salinity and/or water storage organ to improve survival under high salinity or water deficit stress conditions. However, the exact contribution of EBCs to salt tolerance in the ice plant remains poorly understood. An M. crystallinum mutant lacking EBCs was isolated from plant collections mutagenized by fast neutron irradiation. Light and electron microscopy revealed that mutant plants lacked EBCs on all surfaces of leaves and stems. Dry weight gain of aerial parts of the mutant was almost half that of wild-type plants after 3 weeks of growth at 400 mM NaCl. The EBC mutant also showed reduced leaf succulence and leaf and stem water contents compared with wild-type plants. Aerial tissues of wild-type plants had approximately 1.5-fold higher Na+ and Cl- content than the mutant grown under 400 mM NaCl for 2 weeks. Na+ and Cl- partitioning into EBCs of wild-type plants resulted in lower concentrations of these ions in photosynthetically active leaf tissues than in leaves of the EBC-less mutant, particularly under conditions of high salt stress. Potassium, nitrate, and phosphate ion content decreased with incorporation of NaCl into tissues in both the wild type and the mutant, but the ratios of Na +/K+ and Cl-/NO3- content were maintained only in the leaf and stem tissues of wild-type plants. The EBC mutant showed significant impairment in plant productivity under salt stress as evaluated by seed pod and seed number and average seed weight. These results clearly show that EBCs contribute to succulence by serving as a water storage reservoir and to salt tolerance by maintaining ion sequestration and homeostasis within photosynthetically active tissues of M. crystallinum.

Original languageEnglish
Pages (from-to)1957-1967
Number of pages11
JournalJournal of Experimental Botany
Volume58
Issue number8
DOIs
Publication statusPublished - Apr 1 2007

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Mesembryanthemum
Mesembryanthemum crystallinum
Salt-Tolerance
bladder
salt tolerance
homeostasis
Urinary Bladder
Homeostasis
Salts
salts
mutants
cells
Seeds
leaves
Salinity
Ions
ions
Water
stems
salt stress

All Science Journal Classification (ASJC) codes

  • Physiology
  • Plant Science

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Salt tolerance, salt accumulation, and ionic homeostasis in an epidermal bladder-cell-less mutant of the common ice plant Mesembryanthemum crystallinum. / Agarie, Sakae; Shimoda, Toshifumi; Shimizu, Yumi; Baumann, Kathleen; Sunagawa, Haruki; Kondo, Ayumu; Osamu, Ueno; Nakahara, Teruhisa; Nose, Akihiro; Cushman, John C.

In: Journal of Experimental Botany, Vol. 58, No. 8, 01.04.2007, p. 1957-1967.

Research output: Contribution to journalArticle

Agarie, S, Shimoda, T, Shimizu, Y, Baumann, K, Sunagawa, H, Kondo, A, Osamu, U, Nakahara, T, Nose, A & Cushman, JC 2007, 'Salt tolerance, salt accumulation, and ionic homeostasis in an epidermal bladder-cell-less mutant of the common ice plant Mesembryanthemum crystallinum', Journal of Experimental Botany, vol. 58, no. 8, pp. 1957-1967. https://doi.org/10.1093/jxb/erm057
Agarie, Sakae ; Shimoda, Toshifumi ; Shimizu, Yumi ; Baumann, Kathleen ; Sunagawa, Haruki ; Kondo, Ayumu ; Osamu, Ueno ; Nakahara, Teruhisa ; Nose, Akihiro ; Cushman, John C. / Salt tolerance, salt accumulation, and ionic homeostasis in an epidermal bladder-cell-less mutant of the common ice plant Mesembryanthemum crystallinum. In: Journal of Experimental Botany. 2007 ; Vol. 58, No. 8. pp. 1957-1967.
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abstract = "The aerial surfaces of the common or crystalline ice plant Mesembryanthemum crystallinum L., a halophytic, facultative crassulacean acid metabolism species, are covered with specialized trichome cells called epidermal bladder cells (EBCs). EBCs are thought to serve as a peripheral salinity and/or water storage organ to improve survival under high salinity or water deficit stress conditions. However, the exact contribution of EBCs to salt tolerance in the ice plant remains poorly understood. An M. crystallinum mutant lacking EBCs was isolated from plant collections mutagenized by fast neutron irradiation. Light and electron microscopy revealed that mutant plants lacked EBCs on all surfaces of leaves and stems. Dry weight gain of aerial parts of the mutant was almost half that of wild-type plants after 3 weeks of growth at 400 mM NaCl. The EBC mutant also showed reduced leaf succulence and leaf and stem water contents compared with wild-type plants. Aerial tissues of wild-type plants had approximately 1.5-fold higher Na+ and Cl- content than the mutant grown under 400 mM NaCl for 2 weeks. Na+ and Cl- partitioning into EBCs of wild-type plants resulted in lower concentrations of these ions in photosynthetically active leaf tissues than in leaves of the EBC-less mutant, particularly under conditions of high salt stress. Potassium, nitrate, and phosphate ion content decreased with incorporation of NaCl into tissues in both the wild type and the mutant, but the ratios of Na +/K+ and Cl-/NO3- content were maintained only in the leaf and stem tissues of wild-type plants. The EBC mutant showed significant impairment in plant productivity under salt stress as evaluated by seed pod and seed number and average seed weight. These results clearly show that EBCs contribute to succulence by serving as a water storage reservoir and to salt tolerance by maintaining ion sequestration and homeostasis within photosynthetically active tissues of M. crystallinum.",
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AU - Baumann, Kathleen

AU - Sunagawa, Haruki

AU - Kondo, Ayumu

AU - Osamu, Ueno

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