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J. Biol. Chem., Vol. 269, Issue 44, 27303-27309, Nov, 1994

Multiple mechanisms for the targeting of photosystem I subunits F, H, K, L, and N into and across the thylakoid membrane

A Mant, VS Nielsen, TG Knott, BL Moller and C Robinson
Department of Biological Sciences, University of Warwick, Coventry, United Kingdom.

The photosystem I (PSI) complex in higher plants contains eight nuclear- encoded subunits, of which two (PSI-F and -N) are synthesized with bipartite presequences containing cleavable thylakoid transfer sequences. Previous studies on four other chloroplast proteins bearing bipartite presequences have shown that they are transported across the thylakoid membrane by two distinct mechanisms. One mechanism is delta pH-dependent and hence sensitive to uncouplers, whereas the other is inhibited by azide. We show that PSI-F is targeted by the latter pathway, since its translocation across the thylakoid membrane is inhibited by azide but not by nigericin. Translocation is furthermore unaffected by the presence of high concentrations of the lumenal 23-kDa photosystem II (PSII) protein, which is known to be transported by the delta pH-dependent pathway. In contrast, translocation of PSI-N across the thylakoid membrane is completely blocked by saturating concentrations of pre-23-kDa protein. Three proteins are now known to be synthesized with thylakoid transfer signals in both higher plants and cyanobacteria (PSI-F, plastocyanin, and the 33-kDa PSII protein), and all three are transported by the azide-sensitive, possibly sec- dependent pathway. In contrast, PSI-N and the 23-kDa and 16-kDa PSII proteins (transported by the delta pH-driven pathway in higher plants) are all absent in cyanobacteria. These data suggest that the delta pH- dependent translocation mechanism for these proteins may also have arisen relatively recently during the evolution of the chloroplast. Three additional PSI proteins (PSI-H, -K, and -L) are synthesized in the cytosol with stroma-targeting presequences and hence integrate into the thylakoid membrane by means of information in the mature proteins. We show that the integration mechanisms are insensitive to azide in each case, and nigericin causes only a slight inhibition of integration in each case. We therefore suggest that these proteins are targeted into the thylakoid membrane by a separate pathway(s).
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