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Importance of ROS and antioxidant system during the beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation

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Abstract

The present study suggests the importance of reactive oxygen species (ROS) and antioxidant metabolites as biochemical signals during the beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation at saturating light and optimal CO2. Changes in steady-state photosynthesis of pea mesophyll protoplasts monitored in the presence of antimycin A [AA, inhibitor of cytochrome oxidase (COX) pathway] and salicylhydroxamic acid [SHAM, inhibitor of alternative oxidase (AOX) pathway] were correlated with total cellular ROS and its scavenging system. Along with superoxide dismutase (SOD) and catalase (CAT), responses of enzymatic components—ascorbate peroxidase (APX), monodehydroascorbate reductase (MDAR), glutathione reductase (GR) and non-enzymatic redox components of ascorbate–glutathione (Asc–GSH) cycle, which play a significant role in scavenging cellular ROS, were examined in the presence of mitochondrial inhibitors. Both AA and SHAM caused marked reduction in photosynthetic carbon assimilation with concomitant rise in total cellular ROS. Restriction of electron transport through COX or AOX pathway had differential effect on ROS generating (SOD), ROS scavenging (CAT and APX) and antioxidant (Asc and GSH) regenerating (MDAR and GR) enzymes. Further, restriction of mitochondrial electron transport decreased redox ratios of both Asc and GSH. However, while decrease in redox ratio of Asc was more prominent in the presence of SHAM in light compared with dark, decrease in redox ratio of GSH was similar in both dark and light. These results suggest that the maintenance of cellular ROS at optimal levels is a prerequisite to sustain high photosynthetic rates which in turn is regulated by respiratory capacities of COX and AOX pathways.

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Abbreviations

AA:

Antimycin A

AOX:

Alternative oxidase

APX:

Ascorbate peroxidase

Asc:

Ascorbate reduced

CAT:

Catalase

COX:

Cytochrome oxidase

DHA:

Dehydroascorbate

GR:

Glutathione reductase

GSH:

Glutathione (reduced)

GSSG:

Glutathione (oxidized)

MDAR:

Monodehydroascorbate reductase

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

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Acknowledgments

This work was supported by grants to K.P.S. from Department of Science and Technology (No. SR/FTP/LS-226/2000). The support of funds to the Department of Plant Sciences and School of Life Sciences from DST-FIST level II (SR/FST/LSII-010/2007) and UGC-CAS-I (F-5-8/2008, SAP-II) is gratefully acknowledged. The authors are grateful to Dr. G. Padmaja, and CIL, UoHyd, for their help in statistical analysis and confocal microscopic studies. Ch.D. is a recipient of Senior Research Fellowship from Council of Scientific and Industrial Research. We thank Prof. Greg Vanlerberghe and Dr. T. Saradadevi for helpful discussion and suggestions related to the manuscript.

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  1. Department of Plant Sciences, School of Life Sciences, University of Hyderabad, Hyderabad, 500046, India

    Challabathula Dinakar, Vishwakarma Abhaypratap, Srinivasa Rao Yearla, Agepati S. Raghavendra & Kollipara Padmasree

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  1. Challabathula Dinakar
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  2. Vishwakarma Abhaypratap
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  3. Srinivasa Rao Yearla
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Correspondence to Kollipara Padmasree.

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Supplementary Table 1 (DOC 34 kb)

425_2009_1067_MOESM2_ESM.tif

Supplementary Fig. 1 Identification of SOD isoforms from the mesophyll protoplasts of pea (Pisum sativum). Activity staining was performed without any inhibitor (control), in the presence of 5 mM KCN that inhibits Cu/Zn-SOD, or in the presence of 5 mM H2O2, which inhibits both Cu/Zn- and Fe-SOD (TIFF 3,283 kb)

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Dinakar, C., Abhaypratap, V., Yearla, S.R. et al. Importance of ROS and antioxidant system during the beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Planta 231, 461–474 (2010). https://doi.org/10.1007/s00425-009-1067-3

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