OsRNase ZS2 degrades the transcripts of NdhD and NdhF subunits of the NDH complex to modulate the balance between cyclic and linear photosynthetic electron transport at different developmental stages

Photosynthetic electron transport occurs via linear (LET) and cyclic (CET) pathways. The balance between LET and CET is essential for sustaining photosynthetic efficiency because these pathways regulate ATP and NADPH production. In rice, the NDH complex mediates CET, but how the NDH complex participates in regulating the proportion of CET is currently unknown. Here, we found that rice RNase ZS2, which localizes to the chloroplast, degrades mRNAs encoding NdhD and NdhF subunits of the NDH complex, thereby negatively regulating the accumulation of NDH-PSI supercomplexes, which impacts CET:LET ratios. In plants with transgenic RNase ZS2 down-regulation, increased NDH accumulation causes chloroplast ultrastructural alterations and changes in photosynthetic electron transport, with a higher proportion of CET. We demonstrate physical interactions between NdhD and Cyt f that may recruit more Cyt b₆f complexes for CET, which ultimately regulates CET:LET ratios to meet different metabolic needs at various developmental stages. These results reveal a regulatory mechanism in which a nuclear-encoded RNase ZS2 degrades chloroplast-encoded NDH mRNAs to regulate CET:LET ratios.