CHLORELLA, chloroplast-targeted long noncoding RNA, mediates the chloroplast functional transition during leaf lifespan through anterograde signaling pathway

The transition of chloroplast function from biogenesis to degeneration upon leaf senescence is critical for a plant's fitness, as nutrient relocation from leaves to reproductive organs is achieved through this process. The optimal timing of transition should be regulated by tight coordination between chloroplast and nucleus, but the underlying mechanisms remain elusive. Here, we describe the regulatory mechanism of this transition. Chloroplast-Related LONG NONCODING RNA 1 (CHLORELLA1) is highly co-expressed with genes coding for chloroplast functionality during leaf development. Leaves of chlorella exhibit precocious senescence symptoms and a decline in the expression of chloroplast-associated genes, indicating that CHLORELLA1 plays a role in maintaining chloroplast function. Mechanistically, nucleus-encoded CHLORELLA1 transcripts are translocated into the chloroplast and contribute to the assembly of the plastid-encoded RNA polymerase (PEP) complex. At aged leaves, decreased expression of CHLORELLA1 attenuates PEP complex assembly and transcription of photosynthesis genes, possibly triggering leaf senescence. Moreover, CHLORELLA1 is directly activated by GLK1/2, master regulators of chloroplast maintenance. Our study unravels a new layer of the regulation via chloroplast-targeted lncRNA as an anterograde signal in timely decision of leaf senescence. Overall design: To compare chlorella-1 mutant and Col transcriptome, we collected 14d,26d-old of each leaves, and performed differentially expressed gene analysis.