Dynamic association of the plastid localized cysteine synthase complex is vital for efficient cysteine production, photosynthesis, and grana thylakoid formation in transgenic tobacco.

Cysteine biosynthesis is essential for translation and represents the entry point of reduced sulfur into plant metabolism. The two consecutively acting enzymes serine-acetyltransferase (SAT) and O-acetylserine-thiol-lyase catalyze cysteine production and form the cysteine synthase complex (CSC), in which SAT is activated. Here we show that expression of active SAT in plastids of tobacco (PSA) causes substantial cysteine accumulation. Remarkably, enhanced cysteine production in plastids entirely abolished grana stack formation, impaired photosynthesis capacity, and decreased the number of chloroplasts in mesophyll cells of PSA lines. Transgenic tobacco lines expressing active SAT in the cytosol (CSA) accumulated comparable amounts of thiols but displayed no phenotype. To dissect the consequences of CSC formation from enhanced SAT activity in tobacco plastids, we expressed an enzymatically inactive SAT that can still form the CSC in tobacco plastids (PSI). The PSI lines were indistinguishable from PSA lines, although the PSI lines displayed no increase in plastid-localized SAT activity. Neither PSA lines nor PSI lines suffered from an oxidized redox environment in plastids that could have been causative for the disturbed photosynthesis. From these findings, we infer that the association of the plastid CSC itself triggers a signaling cascade controlling sulfur assimilation and photosynthetic capacity in leaves.