The N-degron pathways of ubiquitin mediated proteolysis target proteins for degradation dependent on the amino terminal residue, often produced after endopeptidase activity. Very few substrates have been identified in plants even though enzymes of these pathways are highly conserved in eukaryotes. Here we identify ELONGATED HYPOCOTYL5 (HY5), a master transcriptional regulator involved in many aspects of plant development, as a target for the endopeptidase METACASPASE (MC)9, producing the carboxy-terminal protein fragment (proteoform) E59-HY5. E59-HY5 is shown to be a substrate of the arginyl transferase (ATE) N-degron pathway, and influences physiological processes known to be controlled by HY5, including photomorphogenesis and the unfolded protein response. Conditional stability of E59-HY5 was shown to result from environmentally controlled ATE function, which may highlight a general mechanism for N-degron pathway regulation of proteoform and proteome function during growth and development.