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Ascorbic acid is a key participant during the interactions between chloroplasts and mitochondria to optimize photosynthesis and protect against photoinhibition

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Abstract

The possible role of L-ascorbate (AsA) as a biochemical signal during the interactions between photosynthesis and respiration was examined in leaf discs of Arabidopsis thaliana. AsA content was either decreased as in AsA-deficient vtc1 mutants or increased by treatment with L-galactono-1, 4-lactone (L-GalL, a precursor of AsA; EC 1.3.2.3). In mutants, photosynthesis was extremely sensitive to both antimycin A (inhibitor of the cytochrome c oxidase pathway [COX pathway]) and salicylhydroxamic acid (SHAM, inhibitor of the alternative pathway [AOX pathway]), particularly at high light conditions. Mitochondrial inhibitors lowered the ratio of reduced AsA to total AsA, at high light, indicating oxidative stress in leaf discs. Elevation of AsA by L-GalL decreased the sensitivity of photosynthesis at high light to antimycin A or SHAM, sustained photosynthesis at supraoptimal light and relieved the extent of photoinhibition. High ratios of reduced AsA to total AsA in L-GalL-treated leaf discs suggests that L-GalL lowers oxidative stress. The protection by L-GalL of photosynthesis against the mitochondrial inhibitors and photoinhibition was quite pronounced in vtc1 mutants. Our results suggest that the levels and redox state of AsA modify the pattern of modulation of photosynthesis by mitochondrial metabolism. The extent of the AOX pathway as a percentage of the total respiration in Arabidopsis mesophyll protoplasts was much higher in vtc1 than in wild type. We suggest that the role of AsA becomes pronounced at high light and/or when the AOX pathway is inhibited. While acknowledging the importance of the COX pathway, we hypothesize that AsA and the AOX pathway may complement each other to protect photosynthesis against photoinhibition.

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Abbreviations

AOX:

alternative oxidase

AsA:

ascorbate

CCCP:

carbonyl cyanide m-chlorophenylhydrazone

COX:

cytochrome c oxidase

l-GalL:

l-galactono-1, 4-lactone

DHA:

dehydroascorbate

l-GalLDH:

l-galactono-1, 4-lactone dehydrogenase

H2O2 :

hydrogen peroxide

ROS:

reactive oxygen species

SHAM:

salicylhydroxamic acid

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Acknowledgements

This work was supported by grants to ASR from Council of Scientific and Industrial Research (No. 38(1063)/03/EMR), and a JC Bose National Fellowship (No. SR/S2/JCB-06/2006). Senior Research fellowships from CSIR to KR and LP, University Grants Commission-Special Assistance Program fellowship for meritorious students to (TSK and BS) and Junior Research fellowship from UGC (PR). Special grants from the Department of Science and Technology (DST-FIST) and University Grants Commission (UGC-SAP–CAS-I) were provided to the Department of Plant Sciences. We thank Dr Nick Smirnoff for providing us with an initial supply of seeds of wild-type and vtc1 mutant of A. thaliana and also a small sample of L-galactono-1,4-lactone.

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Authors and Affiliations

  1. Department of Plant Sciences, School of Life Sciences, University of Hyderabad, Hyderabad, 500 046, India

    Saikrishna Talla, Khateef Riazunnisa, Lolla Padmavathi, Bobba Sunil, Pidakala Rajsheel & Agepati S Raghavendra

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  1. Saikrishna Talla
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  2. Khateef Riazunnisa
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  3. Lolla Padmavathi
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  4. Bobba Sunil
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  5. Pidakala Rajsheel
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  6. Agepati S Raghavendra
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Correspondence to Agepati S Raghavendra.

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Corresponding editor: Jitendra P Khurana

[Talla S, Riazunnisa K, Padmavathi L, Sunil B, Rajsheel P and Raghavendra AS 2011 Ascorbic acid is a key participant during the interactions between chloroplasts and mitochondria to optimize photosynthesis and protect against photoinhibition. J. Biosci. 36 XXX–XXX] DOI

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Talla, S., Riazunnisa, K., Padmavathi, L. et al. Ascorbic acid is a key participant during the interactions between chloroplasts and mitochondria to optimize photosynthesis and protect against photoinhibition. J Biosci 36, 163–173 (2011). https://doi.org/10.1007/s12038-011-9000-x

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