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A CAM- and starch-deficient mutant of the facultative CAM species Mesembryanthemum crystallinum reconciles sink demands by repartitioning carbon during acclimation to salinity.

Haider MS, Barnes JD, Cushman JC, Borland AM - J. Exp. Bot. (2012)

Bottom Line: Under salinity, CAM deficiency reduced 24 h photosynthetic carbon gain by >50%.Dark respiration of leaves and roots was a stronger sink for carbohydrate in the mutant compared with the wild type and implied higher maintenance costs for the metabolic processes underpinning acclimation to salinity when CAM was curtailed.The data suggest a key role for the vacuole in regulating the supply and demand for carbohydrate over the day/night cycle in the starch-/CAM-deficient mutant.

View Article: PubMed Central - PubMed

Affiliation: Newcastle Institute for Research on Sustainability, Newcastle University, Newcastle upon Tyne, UK.

ABSTRACT
In the halophytic species Mesembryanthemum crystallinum, the induction of crassulacean acid metabolism (CAM) by salinity requires a substantial investment of resources in storage carbohydrates to provide substrate for nocturnal CO(2) uptake. Acclimation to salinity also requires the synthesis and accumulation of cyclitols as compatible solutes, maintenance of root respiration, and nitrate assimilation. This study assessed the hierarchy and coordination of sinks for carbohydrate in leaves and roots during acclimation to salinity in M. crystallinum. By comparing wild type and a CAM-/starch-deficient mutant of this species, it was sought to determine if other metabolic sinks could compensate for a curtailment in CAM and enable acclimation to salinity. Under salinity, CAM deficiency reduced 24 h photosynthetic carbon gain by >50%. Cyclitols were accumulated to comparable levels in leaves and roots of both the wild type and mutant, but represented only 5% of 24 h carbon balance. Dark respiration of leaves and roots was a stronger sink for carbohydrate in the mutant compared with the wild type and implied higher maintenance costs for the metabolic processes underpinning acclimation to salinity when CAM was curtailed. CAM required the nocturnal mobilization of >70% of primary carbohydrate in the wild type and >85% of carbohydrate in the mutant. The substantial allocation of carbohydrate to CAM limited the export of sugars to roots, and the root:shoot ratio declined under salinity. The data suggest a key role for the vacuole in regulating the supply and demand for carbohydrate over the day/night cycle in the starch-/CAM-deficient mutant.

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The 24 h net carbon budgets for leaves of wild-type and CAM-deficient mutants of M. crystallinum showing partitioning of carbon skeletons derived from C3 and C4 carboxylation between different carbohydrate pools, export, dark respiration, and CAM in control plants and after exposure to 300 mM NaCl for 14 d. The source of carbon in the leaf during the day is C3 (daytime photosynthesis) or C4 (from breakdown of malate over a 12 h photoperiod with 1 mol malate=4 mol C). Export includes growth/maintenance, and fluxes shown in the white (open) arrows are daytime processes, while those in black (solid) arrows are night-time processes. All numbers presented on the budgets are mmol C m−2 d−1.
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fig7: The 24 h net carbon budgets for leaves of wild-type and CAM-deficient mutants of M. crystallinum showing partitioning of carbon skeletons derived from C3 and C4 carboxylation between different carbohydrate pools, export, dark respiration, and CAM in control plants and after exposure to 300 mM NaCl for 14 d. The source of carbon in the leaf during the day is C3 (daytime photosynthesis) or C4 (from breakdown of malate over a 12 h photoperiod with 1 mol malate=4 mol C). Export includes growth/maintenance, and fluxes shown in the white (open) arrows are daytime processes, while those in black (solid) arrows are night-time processes. All numbers presented on the budgets are mmol C m−2 d−1.

Mentions: The net 24 h carbon budgets presented in Fig. 7 provide a quantitative illustration of the sources (C3 or C4) of carbon in the leaf, how this carbon was partitioned between starch and soluble sugars, and how much of each fraction was used to generate the substrate for CAM, respiratory CO2, or cyclitol synthesis. Export was calculated as the sum of carbon in excess of that accumulated in starch and soluble sugars during the day, plus carbon degraded at night that is not accounted for by the requirement to produce the 3-C substrate (PEP) for nocturnal carboxylation or the generation of respiratory CO2. Under control conditions, wild-type plants took up ∼20% more carbon compared with the mutants, with ∼25% of this carbon stored as starch; the remaining 75% entered the soluble sugar pool, with some 40% of these soluble sugars exported over the course of the day. At night, the amount of sugars exported from control leaves was >2-fold higher than those exported during the day. In the starch-deficient mutants, all carbon entered the soluble sugar pool, with daytime export ∼70% of that noted in control plants. At night, export from leaves of control mutants was ∼80% of that calculated for the wild type.


A CAM- and starch-deficient mutant of the facultative CAM species Mesembryanthemum crystallinum reconciles sink demands by repartitioning carbon during acclimation to salinity.

Haider MS, Barnes JD, Cushman JC, Borland AM - J. Exp. Bot. (2012)

The 24 h net carbon budgets for leaves of wild-type and CAM-deficient mutants of M. crystallinum showing partitioning of carbon skeletons derived from C3 and C4 carboxylation between different carbohydrate pools, export, dark respiration, and CAM in control plants and after exposure to 300 mM NaCl for 14 d. The source of carbon in the leaf during the day is C3 (daytime photosynthesis) or C4 (from breakdown of malate over a 12 h photoperiod with 1 mol malate=4 mol C). Export includes growth/maintenance, and fluxes shown in the white (open) arrows are daytime processes, while those in black (solid) arrows are night-time processes. All numbers presented on the budgets are mmol C m−2 d−1.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC3295396&req=5

fig7: The 24 h net carbon budgets for leaves of wild-type and CAM-deficient mutants of M. crystallinum showing partitioning of carbon skeletons derived from C3 and C4 carboxylation between different carbohydrate pools, export, dark respiration, and CAM in control plants and after exposure to 300 mM NaCl for 14 d. The source of carbon in the leaf during the day is C3 (daytime photosynthesis) or C4 (from breakdown of malate over a 12 h photoperiod with 1 mol malate=4 mol C). Export includes growth/maintenance, and fluxes shown in the white (open) arrows are daytime processes, while those in black (solid) arrows are night-time processes. All numbers presented on the budgets are mmol C m−2 d−1.
Mentions: The net 24 h carbon budgets presented in Fig. 7 provide a quantitative illustration of the sources (C3 or C4) of carbon in the leaf, how this carbon was partitioned between starch and soluble sugars, and how much of each fraction was used to generate the substrate for CAM, respiratory CO2, or cyclitol synthesis. Export was calculated as the sum of carbon in excess of that accumulated in starch and soluble sugars during the day, plus carbon degraded at night that is not accounted for by the requirement to produce the 3-C substrate (PEP) for nocturnal carboxylation or the generation of respiratory CO2. Under control conditions, wild-type plants took up ∼20% more carbon compared with the mutants, with ∼25% of this carbon stored as starch; the remaining 75% entered the soluble sugar pool, with some 40% of these soluble sugars exported over the course of the day. At night, the amount of sugars exported from control leaves was >2-fold higher than those exported during the day. In the starch-deficient mutants, all carbon entered the soluble sugar pool, with daytime export ∼70% of that noted in control plants. At night, export from leaves of control mutants was ∼80% of that calculated for the wild type.

Bottom Line: Under salinity, CAM deficiency reduced 24 h photosynthetic carbon gain by >50%.Dark respiration of leaves and roots was a stronger sink for carbohydrate in the mutant compared with the wild type and implied higher maintenance costs for the metabolic processes underpinning acclimation to salinity when CAM was curtailed.The data suggest a key role for the vacuole in regulating the supply and demand for carbohydrate over the day/night cycle in the starch-/CAM-deficient mutant.

View Article: PubMed Central - PubMed

Affiliation: Newcastle Institute for Research on Sustainability, Newcastle University, Newcastle upon Tyne, UK.

ABSTRACT
In the halophytic species Mesembryanthemum crystallinum, the induction of crassulacean acid metabolism (CAM) by salinity requires a substantial investment of resources in storage carbohydrates to provide substrate for nocturnal CO(2) uptake. Acclimation to salinity also requires the synthesis and accumulation of cyclitols as compatible solutes, maintenance of root respiration, and nitrate assimilation. This study assessed the hierarchy and coordination of sinks for carbohydrate in leaves and roots during acclimation to salinity in M. crystallinum. By comparing wild type and a CAM-/starch-deficient mutant of this species, it was sought to determine if other metabolic sinks could compensate for a curtailment in CAM and enable acclimation to salinity. Under salinity, CAM deficiency reduced 24 h photosynthetic carbon gain by >50%. Cyclitols were accumulated to comparable levels in leaves and roots of both the wild type and mutant, but represented only 5% of 24 h carbon balance. Dark respiration of leaves and roots was a stronger sink for carbohydrate in the mutant compared with the wild type and implied higher maintenance costs for the metabolic processes underpinning acclimation to salinity when CAM was curtailed. CAM required the nocturnal mobilization of >70% of primary carbohydrate in the wild type and >85% of carbohydrate in the mutant. The substantial allocation of carbohydrate to CAM limited the export of sugars to roots, and the root:shoot ratio declined under salinity. The data suggest a key role for the vacuole in regulating the supply and demand for carbohydrate over the day/night cycle in the starch-/CAM-deficient mutant.

Show MeSH
Related in: MedlinePlus