The chloroplast-targeted long noncoding RNA CHLORELLA mediates chloroplast functional transition across leaf ageing via anterograde signalling.

The transition from chloroplast biogenesis to degeneration during leaf senescence is critical for plants' fitness, as it facilitates the relocation of nutrients to reproductive organs1-3. However, it remains largely unknown how the timing of this transition is regulated by the coordination between chloroplasts and the nucleus4,5. Here we describe the regulatory mechanism underlying this transition in Arabidopsis thaliana. CHLOROPLAST-RELATED LONG NONCODING RNA (CHLORELLA) is highly co-expressed with genes supporting chloroplast function during leaf development. Leaves lacking CHLORELLA exhibit precocious senescence and reduced expression of chloroplast-associated genes, suggesting that CHLORELLA helps maintain chloroplast function. Mechanistically, CHLORELLA transcripts are translocated into chloroplasts and contribute to the accumulation of the plastid-encoded RNA polymerase complex. As leaves age, the expression of CHLORELLA decreases, leading to reduced plastid-encoded RNA polymerase accumulation and diminished transcription of photosynthesis-related genes, which may trigger leaf senescence. Moreover, CHLORELLA expression is activated by GOLDEN2-LIKE1 and GOLDEN2-LIKE2, master regulators of chloroplast development6-8. Our study unravels a long-noncoding-RNA-based anterograde signalling mechanism that facilitates timely leaf senescence.