New Insights into the Evolution of the Electron Transfer from Cytochrome f to Photosystem I in the Green and Red Branches of Photosynthetic Eukaryotes

In cyanobacteria and most green algae of the eukaryotic green lineage, the copper-protein plastocyanin (Pc) alternatively replaces the heme-protein cytochrome c6 (Cc6) as the soluble electron carrier from cytochrome f (Cf) to photosystem I (PSI). The functional and structural equivalence of ‘green’ Pc and Cc6 has been well established, representing an example of convergent evolution of two unrelated proteins. However, plants only produce Pc, despite having evolved from green algae. On the other hand, Cc6 is the only soluble donor available in most species of the red lineage of photosynthetic organisms, which includes, among others, red algae and diatoms. Interestingly, Pc genes have been identified in oceanic diatoms, probably acquired by horizontal gene transfer from green algae. However, the mechanisms that regulate the expression of a functional Pc in diatoms are still unclear. In the green eukaryotic lineage, the transfer of electrons from Cf to PSI has been characterized in depth. The conclusion is that in the green lineage, this process involves strong electrostatic interactions between partners, which ensure a high affinity and an efficient electron transfer (ET) at the cost of limiting the turnover of the process. In the red lineage, recent kinetic and structural modeling data suggest a different strategy, based on weaker electrostatic interactions between partners, with lower affinity and less efficient ET, but favoring instead the protein exchange and the turnover of the process. Finally, in diatoms the interaction of the acquired green-type Pc with both Cf and PSI may not yet be optimized.The Spanish Ministry of Economy, Industry and Competitiveness (BIO2015-64169-P and BIO2016-79930-R) and the Andalusian Government (PAIDI BIO-022). These grants were partially financed by the EU FEDER Program. C.C. is the recipient of a FPU Program fellowship (FPU16/04040; Spanish Ministry of Education, Culture and Sports). We acknowledge the support of the publication fee by the CSIC Open Access Publication Support Initiative through its Unit of Information Resources for Research (URICI).Peer reviewe