Expression of tobacco genes for light-harvesting chlorophyll a/b binding proteins of photosystem II is controlled by two circadian oscillators in a developmentally regulated fashion

Light-induced expression of genes encoding the light-harvesting chlorophyll a/b binding proteins of photosystem II (Cab) was shown to be controlled by a circadian oscillator coupled to the red-light-absorbing plant photoreceptor phytochrome. Here we show that a red-light-insensitive oscillator is also involved in regulating the expression of the Cab genes. We provide evidence that germination leads, in a light-independent manner, to the setting and/or synchronization of endogenous oscillators and that it induces the expression of Cab genes in a circadian fashion. This circadian oscillator is not coupled to phytochrome, as it cannot be reset by red light for at least 44 h after sowing. Short red light pulses given between 12 and 44 h after sowing, however, induce new rhythms without perturbing the already free-running red-light-independent circadian oscillation. At this stage of development, the phytochrome-coupled and uncoupled circadian rhythms coexist. Both circadian rhythms are expressed and exhibit period lengths close to 24 h but are phased differently. At later stages of development (60 h or later after sowing), red light treatments synchronized these free-running rhythms and led to the appearance of a single new circadian oscillation. These data indicate that during early development the expression of single tobacco Cab genes, particularly expression of the Cab21 and Cab40 genes, is controlled in a developmentally dependent manner by two circadian oscillators.