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Differential activity of plasma and vacuolar membrane transporters contributes to genotypic differences in salinity tolerance in a Halophyte Species, Chenopodium quinoa.

Bonales-Alatorre E, Pottosin I, Shabala L, Chen ZH, Zeng F, Jacobsen SE, Shabala S - Int J Mol Sci (2013)

Bottom Line: Our results suggest that multiple mechanisms contribute towards genotypic differences in salinity tolerance in quinoa.These include: (i) a higher rate of Na+ exclusion from leaf mesophyll; (ii) maintenance of low cytosolic Na+ levels; (iii) better K+ retention in the leaf mesophyll; (iv) a high rate of H+ pumping, which increases the ability of mesophyll cells to restore their membrane potential; and (v) the ability to reduce the activity of SV and FV channels under saline conditions.These mechanisms appear to be highly orchestrated, thus enabling the remarkable overall salinity tolerance of quinoa species.

View Article: PubMed Central - PubMed

Affiliation: School of Agricultural Science and Tasmanian Institute for Agriculture, University of Tasmania, Private Bag 54, Hobart, TAS 7001, Australia. Sergey.Shabala@utas.edu.au.

ABSTRACT
Halophytes species can be used as a highly convenient model system to reveal key ionic and molecular mechanisms that confer salinity tolerance in plants. Earlier, we reported that quinoa (Chenopodium quinoa Willd.), a facultative C3 halophyte species, can efficiently control the activity of slow (SV) and fast (FV) tonoplast channels to match specific growth conditions by ensuring that most of accumulated Na+ is safely locked in the vacuole (Bonales-Alatorre et al. (2013) Plant Physiology). This work extends these finding by comparing the properties of tonoplast FV and SV channels in two quinoa genotypes contrasting in their salinity tolerance. The work is complemented by studies of the kinetics of net ion fluxes across the plasma membrane of quinoa leaf mesophyll tissue. Our results suggest that multiple mechanisms contribute towards genotypic differences in salinity tolerance in quinoa. These include: (i) a higher rate of Na+ exclusion from leaf mesophyll; (ii) maintenance of low cytosolic Na+ levels; (iii) better K+ retention in the leaf mesophyll; (iv) a high rate of H+ pumping, which increases the ability of mesophyll cells to restore their membrane potential; and (v) the ability to reduce the activity of SV and FV channels under saline conditions. These mechanisms appear to be highly orchestrated, thus enabling the remarkable overall salinity tolerance of quinoa species.

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Typical whole vacuole recordings of fast-activating vacuolar (FV) currents from the Q5206 genotype, illustrating a run-up phenomenon in patch-clamp measurements. (A,B) typical FV current recordings in a symmetrical 100 mM KCl solution from small (C ~3 pF) quinoa tonoplast vesicles, isolated from a large central vacuole, shortly (1 min; defined as initial; panel A) and 30 min after obtaining a whole vacuole configuration (defined as final; panel B); (C,D) as above, for 100 mM NaCl in the pipette. One (of six to 10 vacuoles) typical recording is shown for each case.
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f4-ijms-14-09267: Typical whole vacuole recordings of fast-activating vacuolar (FV) currents from the Q5206 genotype, illustrating a run-up phenomenon in patch-clamp measurements. (A,B) typical FV current recordings in a symmetrical 100 mM KCl solution from small (C ~3 pF) quinoa tonoplast vesicles, isolated from a large central vacuole, shortly (1 min; defined as initial; panel A) and 30 min after obtaining a whole vacuole configuration (defined as final; panel B); (C,D) as above, for 100 mM NaCl in the pipette. One (of six to 10 vacuoles) typical recording is shown for each case.

Mentions: Tonoplast conductance is dominated by instantaneously activated FV currents at zero free concentrations of divalent cations (Ca2+ and Mg2+) on both sides of the membrane. Recordings immediately after breaking into the whole vacuole configuration revealed instantaneous currents with a marked outward rectification (larger currents evoked by cytosol-positive voltages, Figure 4). This current remained stable over a period of time (typically up to 15–20 min), before suddenly growing to reach a new stable state (illustrated by comparing panels A and B). This phenomenon is known as a run-up and has previously been described for FV currents in other plant systems [34]. Regardless of the nature of the cation used in a pipette (e.g., K+vs. Na+), FV currents were about the same (Figure 4) and showed the same run-up patterns. This is consistent with previous reports of FV channels being almost equally selective for Na+ and K+ [25,35] and suggests that either ion can be used to study the properties of FV channels in quinoa.


Differential activity of plasma and vacuolar membrane transporters contributes to genotypic differences in salinity tolerance in a Halophyte Species, Chenopodium quinoa.

Bonales-Alatorre E, Pottosin I, Shabala L, Chen ZH, Zeng F, Jacobsen SE, Shabala S - Int J Mol Sci (2013)

Typical whole vacuole recordings of fast-activating vacuolar (FV) currents from the Q5206 genotype, illustrating a run-up phenomenon in patch-clamp measurements. (A,B) typical FV current recordings in a symmetrical 100 mM KCl solution from small (C ~3 pF) quinoa tonoplast vesicles, isolated from a large central vacuole, shortly (1 min; defined as initial; panel A) and 30 min after obtaining a whole vacuole configuration (defined as final; panel B); (C,D) as above, for 100 mM NaCl in the pipette. One (of six to 10 vacuoles) typical recording is shown for each case.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC3676782&req=5

f4-ijms-14-09267: Typical whole vacuole recordings of fast-activating vacuolar (FV) currents from the Q5206 genotype, illustrating a run-up phenomenon in patch-clamp measurements. (A,B) typical FV current recordings in a symmetrical 100 mM KCl solution from small (C ~3 pF) quinoa tonoplast vesicles, isolated from a large central vacuole, shortly (1 min; defined as initial; panel A) and 30 min after obtaining a whole vacuole configuration (defined as final; panel B); (C,D) as above, for 100 mM NaCl in the pipette. One (of six to 10 vacuoles) typical recording is shown for each case.
Mentions: Tonoplast conductance is dominated by instantaneously activated FV currents at zero free concentrations of divalent cations (Ca2+ and Mg2+) on both sides of the membrane. Recordings immediately after breaking into the whole vacuole configuration revealed instantaneous currents with a marked outward rectification (larger currents evoked by cytosol-positive voltages, Figure 4). This current remained stable over a period of time (typically up to 15–20 min), before suddenly growing to reach a new stable state (illustrated by comparing panels A and B). This phenomenon is known as a run-up and has previously been described for FV currents in other plant systems [34]. Regardless of the nature of the cation used in a pipette (e.g., K+vs. Na+), FV currents were about the same (Figure 4) and showed the same run-up patterns. This is consistent with previous reports of FV channels being almost equally selective for Na+ and K+ [25,35] and suggests that either ion can be used to study the properties of FV channels in quinoa.

Bottom Line: Our results suggest that multiple mechanisms contribute towards genotypic differences in salinity tolerance in quinoa.These include: (i) a higher rate of Na+ exclusion from leaf mesophyll; (ii) maintenance of low cytosolic Na+ levels; (iii) better K+ retention in the leaf mesophyll; (iv) a high rate of H+ pumping, which increases the ability of mesophyll cells to restore their membrane potential; and (v) the ability to reduce the activity of SV and FV channels under saline conditions.These mechanisms appear to be highly orchestrated, thus enabling the remarkable overall salinity tolerance of quinoa species.

View Article: PubMed Central - PubMed

Affiliation: School of Agricultural Science and Tasmanian Institute for Agriculture, University of Tasmania, Private Bag 54, Hobart, TAS 7001, Australia. Sergey.Shabala@utas.edu.au.

ABSTRACT
Halophytes species can be used as a highly convenient model system to reveal key ionic and molecular mechanisms that confer salinity tolerance in plants. Earlier, we reported that quinoa (Chenopodium quinoa Willd.), a facultative C3 halophyte species, can efficiently control the activity of slow (SV) and fast (FV) tonoplast channels to match specific growth conditions by ensuring that most of accumulated Na+ is safely locked in the vacuole (Bonales-Alatorre et al. (2013) Plant Physiology). This work extends these finding by comparing the properties of tonoplast FV and SV channels in two quinoa genotypes contrasting in their salinity tolerance. The work is complemented by studies of the kinetics of net ion fluxes across the plasma membrane of quinoa leaf mesophyll tissue. Our results suggest that multiple mechanisms contribute towards genotypic differences in salinity tolerance in quinoa. These include: (i) a higher rate of Na+ exclusion from leaf mesophyll; (ii) maintenance of low cytosolic Na+ levels; (iii) better K+ retention in the leaf mesophyll; (iv) a high rate of H+ pumping, which increases the ability of mesophyll cells to restore their membrane potential; and (v) the ability to reduce the activity of SV and FV channels under saline conditions. These mechanisms appear to be highly orchestrated, thus enabling the remarkable overall salinity tolerance of quinoa species.

Show MeSH
Related in: MedlinePlus