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Functional division of f-type and m-type thioredoxins to regulate the Calvin cycle and cyclic electron transport around photosystem I

  • JPR Symposium
  • Regulation of Cyclic Electron Flow, A to Z
  • Published:
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Abstract

Redox regulation of chloroplast proteins is necessary to adjust photosynthetic performance with changes in light. The thioredoxin (Trx) system plays a central role in this process. Chloroplast-localized classical Trx is a small redox-active protein that regulates many target proteins by reducing their disulfide bonds in a light-dependent manner. Arabidopsis thaliana mutants lacking f-type Trx (trx f1f2) or m-type Trx (trx m124-2) have been reported to show delayed reduction of Calvin cycle enzymes. As a result, the trx m124-2 mutant exhibits growth defects. Here, we characterized a quintuple mutant lacking both Trx f and Trx m to investigate the functional complementarity of Trx f and Trx m. The trx f1f2 m124-2 quintuple mutant was newly obtained by crossing, and is analyzed here for the first time. The growth defects of the trx m124-2 mutant were not enhanced by the lack of Trx f. In contrast, deficiencies of both Trxs additively suppressed the reduction of Calvin cycle enzymes, resulting in a further delay in the initiation of photosynthesis. Trx f appeared to be necessary for the rapid activation of the Calvin cycle during the early induction of photosynthesis. To perform effective photosynthesis, plants seem to use both Trxs in a coordinated manner to activate carbon fixation reactions. In contrast, the PROTON GRADIENT REGULATION 5 (PGR5)-dependent cyclic electron transport around photosystem I was regulated by Trx m, but not by Trx f. Lack of Trx f did not affect the activity and regulation of the PGR5-dependent pathway. Trx f may have a higher specificity for target proteins, whereas Trx m has a variety of target proteins to regulate overall photosynthesis and other metabolic reactions in the chloroplasts.

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Acknowledgements

We thank Dr. Krishna K Niyogi (University of California) for providing the npq4 mutant seeds.

Funding

This study was supported by the Japan Society for the Promotion of Science (JSPS) KAKENHI Grant (grant numbers JP19H04733, 20H02961, and JP21K06219 to Y.O.). We also thank the Oohara Foundation for financial support of our research group.

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Authors and Affiliations

  1. Institute of Plant Science and Resources, Okayama University, Chuo 2-20-1, Kurashiki, 710-0046, Japan

    Yuki Okegawa & Wataru Sakamoto

  2. Faculty of Life Sciences, Kyoto Sangyo University, Kamigamo Motoyama, Kita-ku, Kyoto, 603-8047, Japan

    Yuki Okegawa & Ken Motohashi

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  1. Yuki Okegawa
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  2. Wataru Sakamoto
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  3. Ken Motohashi
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by YO. The first draft of the manuscript was written by YO and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Yuki Okegawa.

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Okegawa, Y., Sakamoto, W. & Motohashi, K. Functional division of f-type and m-type thioredoxins to regulate the Calvin cycle and cyclic electron transport around photosystem I. J Plant Res 135, 543–553 (2022). https://doi.org/10.1007/s10265-022-01388-7

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