Photosystem I (PSI) is present as trimeric complexes in most characterized cyanobacteria and as monomers in plants and algae. Recent reports of tetrameric PSI have raised questions regarding its structural basis, physiological role, phylogenetic distribution and evolutionary significance. Here, we examined PSI in 61 cyanobacteria, showing that tetrameric PSI, which correlates with the psaL gene and a distinct genomic structure, is widespread among heterocyst-forming cyanobacteria and their close relatives. Physiological studies revealed that expression of tetrameric PSI is favoured under high light, with an increased content of novel PSI-bound carotenoids (myxoxanthophyll, canthaxanthan and echinenone). In sum, this work suggests that tetrameric PSI is an adaptation to high light intensity, and that change in PsaL leads to monomerization of trimeric PSI, supporting the hypothesis of tetrameric PSI being the evolutionary intermediate in the transition from cyanobacterial trimeric PSI to monomeric PSI in plants and algae.
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The cloned cyanobacterial psaL sequences have been deposited in GenBank with the accession numbers KY575410, KY575411, KY575412, KY575413, KY575414, KY575415, KY575416, KY575417, KY575418, KY575419, KY575420, KY575421, KY575422, KY575423 and KY575424. The TS-821 whole-genome shotgun project has been deposited at DNA Data Bank of Japan/European Nucleotide Archive/GenBank under the accession MVDI00000000. The version described in this paper is version MVDI01000000.
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Support to B.D.B., M.L. and J.T.N. was provided by the Gibson Family Foundation, the Bredesen Center for Interdisciplinary Research and Education, the Tennessee Plant Research Center, a UTK Professional Development Award, the Dr. Donald L. Akers Faculty Enrichment Fellowship to B.D.B. and National Science Foundation support to B.D.B. (DGE-0801470 and EPS-1004083). M.L. has been supported as a CIRE Fellow at University of Tennessee, Knoxville. A Professional Development Award from the Graduate School at UTK supported travel of B.D.B. to the Netherlands and to the Institut Pasteur. NWO Chemical Sciences supported work at University of Groningen. J.P.W. has been supported by NIH P30 DK063491. The Institut Pasteur supported Pasteur Culture Collection of cyanobacteria. We thank Y. I. Park for the use of the cyanobacterial genome of PCC 7124, and N.G. Brady and T. Cardona for helpful comments on the manuscript.
The authors declare no competing interests.
Peer review information Nature Plants thanks Conrad Mullineaux, Ann Magnuson and the other, anonymous, reviewer for their contribution to the peer review of this work.
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Li, M., Calteau, A., Semchonok, D.A. et al. Physiological and evolutionary implications of tetrameric photosystem I in cyanobacteria. Nat. Plants 5, 1309–1319 (2019). https://doi.org/10.1038/s41477-019-0566-x
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