Singlet oxygen initiates a plastid signal controlling photosynthetic gene expression

Retrograde signals from the plastid regulate photosynthesis-associated nuclear genes and are essential to successful chloroplast biogenesis. One model is that a positive haem-related signal promotes photosynthetic gene expression in a pathway that is abolished by the herbicide norflurazon. Far-red light (FR) pretreatment and transfer to white light also results in plastid damage and loss of photosynthetic gene expression. Here, we investigated whether norflurazon and FR pretreatment affect the same retrograde signal. We used transcriptome analysis and real-time reverse transcription-polymerase chain reaction (RT-PCR) to analyse the effects of these treatments on nuclear gene expression in various Arabidopsis (Arabidopsis thaliana) retrograde signalling mutants. Results showed that the two treatments inhibited largely different nuclear gene sets, suggesting that they affected different retrograde signals. Moreover, FR pretreatment resulted in singlet oxygen (¹ O₂ ) production and a rapid inhibition of photosynthetic gene expression. This inhibition was partially blocked in the executer1executer2 mutant, which is impaired in ¹ O₂ signalling. Our data support a new model in which a ¹ O₂ retrograde signal, generated by chlorophyll precursors, inhibits expression of key photosynthetic and chlorophyll synthesis genes to prevent photo-oxidative damage during de-etiolation. Such a signal would provide a counterbalance to the positive haem-related signal to fine tune regulation of chloroplast biogenesis.