SignificancePhotoinhibitory high light stress in plants leads to increases in markers of protein degradation and transcriptional up-regulation of proteases and proteolytic machinery, but protein homeostasis (proteostasis) of most enzymes is largely maintained under high light, so we know little about the metabolic consequences of it beyond photosystem damage. We developed a technique to look for rapid protein turnover events in response to high light through¹³C partial labeling and detailed peptide mass spectrometry. This analysis reveals a light-induced transcriptional program for nuclear-encoded genes, beyond the regulation of photosystem II, to replace key protein degradation targets in plants and ensure proteostasis under high light stress.