Overexpression of protein import machinery subunit <i>ycf1</i> / <i>Tic214</i> represses photosynthetic complex biogenesis by inhibiting the synthesis of plastid-encoded core subunits in tobacco

ycf1 is a chloroplast-encoded large ORF. Recently, the Ycf1 protein was identified as a component (Tic214) of the translocon complex at the inner envelope membrane of chloroplasts (TIC). However, the effects of altered Ycf1 protein levels on chloroplast biogenesis and development in higher plants have not yet been studied. In this study, by constructing transplastomic ycf1 overexpression (OE) lines in tobacco, we showed that slight overaccumulation of Ycf1 protein leads to a strong reduction of chloroplast-encoded core subunits of photosynthetic complexes, thus causing massive repression of photosystem biogenesis and photosynthetic capacity. The polysome loading of several chloroplast-encoded photosynthesis-related genes was reduced in ycf1 OE lines, suggesting putative translational repression of these genes. In contrast, the nucleus-encoded subunits of photosystems, especially light-harvesting complex (LHC) proteins, are much less affected, promoting the formation of hyperstacked unfunctional grana thylakoids in transplastomic ycf1 OE lines. Our data suggested that the protein level of Ycf1 is tightly regulated in chloroplasts and indicates a possible function for Ycf1 in chloroplast gene expression.