Fast and global reorganization of the chloroplast protein biogenesis network during heat acclimation

Heat waves caused by global warming severely challenge photosynthesis and hence plant biomass production, but the mechanisms of its adjustment, repair and biogenesis during heat acclimation are elusive. We provide a global and time-resolved insight, how these processes are modulated during heat acclimation in chloroplasts, revealing profound modulation of protein biogenesis. Ribosome profiling with Chlamydomonas reinhardtii showed early translational downregulation during synthesis of photosynthesis core antenna proteins, a response that is conserved in Nicotiana tabacum. Our data suggest that these early effects may be caused by reduced translocation of ribosomes synthesizing thylakoid proteins, and that later heat acclimation alleviates these effects. Analysis of the proteinaceous interactome of plastid ribosomes demonstrates widespread remodeling of ribosome-associated processes that could be responsible for the early translational impacts and subsequent acclimation responses. The role of chlorophyll metabolism, protein targeting, and assembly of photosystem complexes as co-translational bottlenecks during heat acclimation are discussed.