Alternative oxidase pathway optimizes photosynthesis during osmotic and temperature stress by regulating cellular ROS, malate valve and antioxidative systems

The present study reveals the importance of alternative oxidase (AOX) pathway in optimizing photosynthesis under osmotic and temperature stress conditions in the mesophyll protoplasts of Pisum sativum. The responses of photosynthesis and respiration were monitored at saturating light intensity of 10...

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Main Authors: DINAKAR eCHALLABATHULA, Abhaypratap eVishwakarma, Raghavendra eAgepati, Padmasree eKollipara
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-02-01
Series:Frontiers in Plant Science
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fpls.2016.00068/full
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spelling doaj-515c461338574f4d8d6855b06c03c9712020-11-24T22:23:07ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2016-02-01710.3389/fpls.2016.00068171347Alternative oxidase pathway optimizes photosynthesis during osmotic and temperature stress by regulating cellular ROS, malate valve and antioxidative systemsDINAKAR eCHALLABATHULA0DINAKAR eCHALLABATHULA1Abhaypratap eVishwakarma2Raghavendra eAgepati3Padmasree eKollipara4Department of Life Sciences, School of Basic and Applied Sciences, Central University of Tamil Nadu, Thiruvarur, Tamil Nadu, IndiaDepartment of Plant Sciences, School of Life Sciences, University of HyderabadDepartment of Plant Sciences, School of Life Sciences, University of HyderabadDepartment of Plant Sciences, School of Life Sciences, University of HyderabadDepartment of Biotechnology and Bioinformatics, School of Life Sciences, University of HyderabadThe present study reveals the importance of alternative oxidase (AOX) pathway in optimizing photosynthesis under osmotic and temperature stress conditions in the mesophyll protoplasts of Pisum sativum. The responses of photosynthesis and respiration were monitored at saturating light intensity of 1000 µmoles m-2 s-1 at 25 oC under a range of sorbitol concentrations from 0.4 M to 1.0M to induce hyper-osmotic stress and by varying the temperature of the thermo-jacketed pre-incubation chamber from 25 oC to 10 oC to impose sub-optimal temperature stress. Compared to controls (0.4 M sorbitol and 25 OC), the mesophyll protoplasts showed remarkable decrease in NaHCO3-dependent O2 evolution (indicator of photosynthetic carbon assimilation), under both hyper-osmotic (1.0 M sorbitol) and sub-optimal temperature stress conditions (10 OC), while the decrease in rates of respiratory O2 uptake were marginal. The capacity of AOX pathway increased significantly in parallel to increase in intracellular pyruvate and reactive oxygen species (ROS) levels under both hyper-osmotic stress and sub-optimal temperature stress under the background of saturating light. The ratio of redox couple (Malate/OAA) related to malate valve increased in contrast to the ratio of redox couple (GSH/GSSG) related to antioxidative system during hyper-osmotic stress. Nevertheless, the ratio of GSH/GSSG decreased in the presence of sub-optimal temperature, while the ratio of Malate/OAA showed no visible changes. Also, the redox ratios of pyridine nucleotides increased under hyper-osmotic (NADH/NAD) and sub-optimal temperature (NADPH/NADP) stresses, respectively. However, upon restriction of AOX pathway by using salicylhydroxamic acid (SHAM), the observed changes in NaHCO3 dependent O2 evolution, cellular ROS, redox ratios of Malate/OAA, NAD(P)H/NAD(P) and GSH/GSSG were further aggravated under stress conditions with concomitant modulations in NADP-MDH and antioxidant enzymes. Taken together, the results indicated the importance of AOX pathway in optimizing photosynthesis under both hyper-osmotic stress and sub-optimal temperatures. Regulation of ROS through redox couples related to malate valve and antioxidant system by AOX pathway to optimize photosynthesis under these stresses are discussed.http://journal.frontiersin.org/Journal/10.3389/fpls.2016.00068/fullPhotosynthesisReactive Oxygen SpeciesRespirationcytochrome oxidasealternative oxidase(AOX)Salicylhydroxamic acid
collection DOAJ
language English
format Article
sources DOAJ
author DINAKAR eCHALLABATHULA
DINAKAR eCHALLABATHULA
Abhaypratap eVishwakarma
Raghavendra eAgepati
Padmasree eKollipara
spellingShingle DINAKAR eCHALLABATHULA
DINAKAR eCHALLABATHULA
Abhaypratap eVishwakarma
Raghavendra eAgepati
Padmasree eKollipara
Alternative oxidase pathway optimizes photosynthesis during osmotic and temperature stress by regulating cellular ROS, malate valve and antioxidative systems
Frontiers in Plant Science
Photosynthesis
Reactive Oxygen Species
Respiration
cytochrome oxidase
alternative oxidase(AOX)
Salicylhydroxamic acid
author_facet DINAKAR eCHALLABATHULA
DINAKAR eCHALLABATHULA
Abhaypratap eVishwakarma
Raghavendra eAgepati
Padmasree eKollipara
author_sort DINAKAR eCHALLABATHULA
title Alternative oxidase pathway optimizes photosynthesis during osmotic and temperature stress by regulating cellular ROS, malate valve and antioxidative systems
title_short Alternative oxidase pathway optimizes photosynthesis during osmotic and temperature stress by regulating cellular ROS, malate valve and antioxidative systems
title_full Alternative oxidase pathway optimizes photosynthesis during osmotic and temperature stress by regulating cellular ROS, malate valve and antioxidative systems
title_fullStr Alternative oxidase pathway optimizes photosynthesis during osmotic and temperature stress by regulating cellular ROS, malate valve and antioxidative systems
title_full_unstemmed Alternative oxidase pathway optimizes photosynthesis during osmotic and temperature stress by regulating cellular ROS, malate valve and antioxidative systems
title_sort alternative oxidase pathway optimizes photosynthesis during osmotic and temperature stress by regulating cellular ros, malate valve and antioxidative systems
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2016-02-01
description The present study reveals the importance of alternative oxidase (AOX) pathway in optimizing photosynthesis under osmotic and temperature stress conditions in the mesophyll protoplasts of Pisum sativum. The responses of photosynthesis and respiration were monitored at saturating light intensity of 1000 µmoles m-2 s-1 at 25 oC under a range of sorbitol concentrations from 0.4 M to 1.0M to induce hyper-osmotic stress and by varying the temperature of the thermo-jacketed pre-incubation chamber from 25 oC to 10 oC to impose sub-optimal temperature stress. Compared to controls (0.4 M sorbitol and 25 OC), the mesophyll protoplasts showed remarkable decrease in NaHCO3-dependent O2 evolution (indicator of photosynthetic carbon assimilation), under both hyper-osmotic (1.0 M sorbitol) and sub-optimal temperature stress conditions (10 OC), while the decrease in rates of respiratory O2 uptake were marginal. The capacity of AOX pathway increased significantly in parallel to increase in intracellular pyruvate and reactive oxygen species (ROS) levels under both hyper-osmotic stress and sub-optimal temperature stress under the background of saturating light. The ratio of redox couple (Malate/OAA) related to malate valve increased in contrast to the ratio of redox couple (GSH/GSSG) related to antioxidative system during hyper-osmotic stress. Nevertheless, the ratio of GSH/GSSG decreased in the presence of sub-optimal temperature, while the ratio of Malate/OAA showed no visible changes. Also, the redox ratios of pyridine nucleotides increased under hyper-osmotic (NADH/NAD) and sub-optimal temperature (NADPH/NADP) stresses, respectively. However, upon restriction of AOX pathway by using salicylhydroxamic acid (SHAM), the observed changes in NaHCO3 dependent O2 evolution, cellular ROS, redox ratios of Malate/OAA, NAD(P)H/NAD(P) and GSH/GSSG were further aggravated under stress conditions with concomitant modulations in NADP-MDH and antioxidant enzymes. Taken together, the results indicated the importance of AOX pathway in optimizing photosynthesis under both hyper-osmotic stress and sub-optimal temperatures. Regulation of ROS through redox couples related to malate valve and antioxidant system by AOX pathway to optimize photosynthesis under these stresses are discussed.
topic Photosynthesis
Reactive Oxygen Species
Respiration
cytochrome oxidase
alternative oxidase(AOX)
Salicylhydroxamic acid
url http://journal.frontiersin.org/Journal/10.3389/fpls.2016.00068/full
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