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The slow S to M rise of chlorophyll a fluorescence reflects transition from state 2 to state 1 in the green alga Chlamydomonas reinhardtii

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Abstract

The green alga Chlamydomonas (C.) reinhardtii is a model organism for photosynthesis research. State transitions regulate redistribution of excitation energy between photosystem I (PS I) and photosystem II (PS II) to provide balanced photosynthesis. Chlorophyll (Chl) a fluorescence induction (the so-called OJIPSMT transient) is a signature of several photosynthetic reactions. Here, we show that the slow (seconds to minutes) S to M fluorescence rise is reduced or absent in the stt7 mutant (which is locked in state 1) in C. reinhardtii. This suggests that the SM rise in wild type C. reinhardtii may be due to state 2 (low fluorescence state; larger antenna in PS I) to state 1 (high fluorescence state; larger antenna in PS II) transition, and thus, it can be used as an efficient and quick method to monitor state transitions in algae, as has already been shown in cyanobacteria (Papageorgiou et al. 1999, 2007; Kaňa et al. 2012). We also discuss our results on the effects of (1) 3-(3,4-dichlorophenyl)-1,4-dimethyl urea, an inhibitor of electron transport; (2) n-propyl gallate, an inhibitor of alternative oxidase (AOX) in mitochondria and of plastid terminal oxidase in chloroplasts; (3) salicylhydroxamic acid, an inhibitor of AOX in mitochondria; and (4) carbonyl cyanide p-trifluoromethoxyphenylhydrazone, an uncoupler of phosphorylation, which dissipates proton gradient across membranes. Based on the data presented in this paper, we conclude that the slow PSMT fluorescence transient in C. reinhardtii is due to the superimposition of, at least, two phenomena: qE dependent non-photochemical quenching of the excited state of Chl, and state transitions.

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Notes

  1. In the Supplementary Material, which is not a part of the main text, we have provided our preliminary results on the effect of using a compatible osmolyte (N,N,N-trimethyl-glycine (C5H11NO2); also called glycine betaine) for the benefit of those who may be asking if its use would have helped us in answering the question of relation between state changes and the SM rise, as it had in cyanobacteria (see e.g., Papageorgiou and Stamatakis 2004). Although our results are complex, and, further studies are necessary to examine these issues, we have made it available to researchers interested in it.

Abbreviations

AOX:

Alternative oxidase

CEF:

Cyclic electron flow

Chl:

Chlorophyll

Cyt:

Cytochrome

DCMU:

3-(3,4-Dichlorophenyl)-1,4-dimethyl urea; also known as Diuron

FCCP:

Carbonyl cyanide p-trifluoromethoxyphenylhydrazone

LEF:

Linear electron flow

NADP:

Nicotinamide adenine dinucleotide phosphate

Ndh:

NAD(P)H dehydrogenase

NDA2:

Type II NADPH dehydrogenase

OJIPSMT:

Chl a fluorescence transient, where “O” refers to the minimum fluorescence, J and I for inflections, P for peak, S for semi-steady state, M for maximum and T for terminal steady state

PC:

Plastocyanin

PG:

n-Propyl gallate

pmf :

Proton-motive force

PQ, PQH2 :

Plastoquinone, plastoquinol

PS:

Photosystem

PTOX:

Plastid (or plastoquinol) terminal oxidase

SHAM:

Salicylhydroxamic acid

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Acknowledgments

Rajagopal Subramanyam was supported by the Department of Biotechnology (BT/PR15132/BRB/10/909/2011) and the Council of Scientific and Industrial Research (38(1381)/14/EMR-II), India, and Sireesha Kodru by the Department of Biotechnology for a research associate fellowship (DBT-RA), India. Govindjee was supported by the US Fulbright foundation during his stay at the University of Hyderabad, India. We are grateful to Reto J. Strasser and to the late Prasanna Mohanty for providing the Handy PEA instrument used in our studies. We thank Vandana Chakravartty of the University of Illinois at Urbana-Champaign for her valuable comments during the preparation of this manuscript.

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Authors and Affiliations

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

    Sireesha Kodru, Tirupathi Malavath, Elsinraju Devadasu & Rajagopal Subramanyam

  2. Department of Biochemistry, School of Life Sciences, University of Hyderabad, Hyderabad, 500 046, India

    Sreedhar Nellaepalli

  3. 204 Anne Burras Lane, Newport News, VA, 23606, USA

    Alexandrina Stirbet

  4. Departments of Biochemistry and Plant Biology, and Center of Biophysics & Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801-3707, USA

    Govindjee

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  1. Sireesha Kodru
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  2. Tirupathi Malavath
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  3. Elsinraju Devadasu
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  4. Sreedhar Nellaepalli
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  5. Alexandrina Stirbet
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  6. Rajagopal Subramanyam
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  7. Govindjee
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Correspondence to Rajagopal Subramanyam or Govindjee.

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In earlier publications, Sireesha Kodru and Sreedhar Nellaepalli have used their names as Kodru Sireesha and Nellaepalli Sreedhar, respectively.

Rajagopal Subramanyam—in earlier publications, has used his name as Subramanyam Rajagopal.

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Kodru, S., Malavath, T., Devadasu, E. et al. The slow S to M rise of chlorophyll a fluorescence reflects transition from state 2 to state 1 in the green alga Chlamydomonas reinhardtii . Photosynth Res 125, 219–231 (2015). https://doi.org/10.1007/s11120-015-0084-2

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