Significance Photoinhibitory 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 through 13 C 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. , Photoinhibitory high light stress in Arabidopsis leads to increases in markers of protein degradation and transcriptional up-regulation of proteases and proteolytic machinery, but proteostasis is largely maintained. We find significant increases in the in vivo degradation rate for specific molecular chaperones, nitrate reductase, glyceraldehyde-3 phosphate dehydrogenase, and phosphoglycerate kinase and other plastid, mitochondrial, peroxisomal, and cytosolic enzymes involved in redox shuttles. Coupled analysis of protein degradation rates, mRNA levels, and protein abundance reveal that 57% of the nuclear-encoded enzymes with higher degradation rates also had high light–induced transcriptional responses to maintain proteostasis. In contrast, plastid-encoded proteins with enhanced degradation rates showed decreased transcript abundances and must maintain protein abundance by other processes. This analysis reveals a light-induced transcriptional program for nuclear-encoded genes, beyond the regulation of the photosystem II (PSII) D1 subunit and the function of PSII, to replace key protein degradation targets in plants and ensure proteostasis under high light stress.