The cytochrome-b6f complex, a key component of the photosynthetic electron transport chain, contains a number of very small protein subunits whose functions are not well defined. Here we have investigated the function of the 31-amino acid PetL subunit encoded in the chloroplast genome in all higher plants. Chloroplast-transformed petL knock-out tobacco plants display no obvious phenotype, suggesting that PetL is not essential for cytochrome b6f complex biogenesis and function (Fiebig, A., Stegemann, S., and Bock, R. (2004) Nucleic Acids Res. 32, 3615-3622). We show here that, whereas young mutant leaves accumulate comparable amounts of cytochrome b6f complex and have an identical assimilation capacity as wild type leaves, both cytochrome b6f complex contents and assimilation capacities of mature and old leaves are strongly reduced in the mutant, indicating that the cytochrome b6f complex is less stable than in the wild type. Reduced complex stability was also confirmed by in vitro treatments of isolated thylakoids with chaotropic reagents. Adaptive responses observed in the knockout mutants, such as delayed down-regulation of plastocyanin contents, indicate that plants can sense the restricted electron flux to photosystem I yet cannot compensate the reduced stability of the cytochrome b6f complex by adaptive up-regulation of complex synthesis. We propose that efficient cytochrome b6f complex biogenesis occurs only in young leaves and that the capacity for de novo synthesis of the complex is very low in mature and aging leaves. Gene expression analysis indicates that the ontogenetic down-regulation of cytochrome b6f complex biogenesis occurs at the post-transcriptional level.