Ubiquitin-dependent chloroplast-associated protein degradation in plants

• Published in: Science (American Association for the Advancement of Science) Vol. 363; no. 6429; p. 836
• Main Authors: Ling, Qihua, Broad, William, Trösch, Raphael, Töpel, Mats, Sert, Tijen Demiral, Lymperopoulos, Panagiotis, Baldwin, Amy, Jarvis, R. Paul
• Format: Journal Article
• Language: English
• Published: United States American Association for the Advancement of Science 22.02.2019; The American Association for the Advancement of Science
• Subjects: Adenosine triphosphatase; Arabidopsis; Arabidopsis - enzymology; Arabidopsis - genetics; Arabidopsis Proteins - metabolism; ATPases Associated with Diverse Cellular Activities - metabolism; Biodegradation; Biosynthesis; Cell Cycle Proteins - metabolism; Chloroplast Proteins; Chloroplasts; Chloroplasts - enzymology; Conductance; Cooperation; Cyanobacteria; Cytosol; Deactivation; Degradation; Endoplasmic reticulum; Genetic analysis; Genetics; Homeostasis; Inactivation; Intracellular Signaling Peptides and Proteins - metabolism; Mathematical models; Membrane Proteins; Membranes; Organelles; Outer membrane proteins; Photosynthesis; Plant growth; Primary production; Proteasome 26S; Proteasome Endopeptidase Complex - metabolism; Proteasomes; Protein transport; Proteins; Proteolysis; Proteomics; RESEARCH ARTICLE SUMMARY; Resistance; Secretion; Sp1 protein; Substrates; Translocase; Ubiquitin - metabolism; Ubiquitin-protein ligase; Ubiquitin-Protein Ligases - metabolism; Ubiquitination; Viability; Viral envelope proteins
• ISSN: 0036-8075; 1095-9203; 1095-9203
• DOI: 10.1126/science.aav4467

Protein degradation is vital for cellular functions, and it operates selectively with distinct mechanisms in different organelles. Some organellar proteins are targeted by the ubiquitin-proteasome system (UPS)—a major proteolytic network in the eukaryotic cytosol. In such cases, the organelle membrane presents a substantial barrier to protein degradation. Working in the model plant Arabidopsis , Ling et al. identified mechanisms underlying the UPS-mediated degradation of proteins in the outer membrane of chloroplasts (the organelles responsible for photosynthesis). They identified an Omp85-type β-barrel outer membrane channel and a cytosolic AAA + chaperone that fulfill conductance and motor functions in the retrotranslocation of target proteins from chloroplasts. This process thus enabled outer membrane protein processing by the cytosolic proteasome. Such chloroplast-associated protein degradation was initiated by ubiquitination of the targets by the chloroplast-localized E3 ubiquitin ligase SP1. Science , this issue p. eaav4467 A retrotranslocation system in the chloroplast envelope allows cytosolic degradation of chloroplast outer-envelope proteins by the proteasome Chloroplasts contain thousands of nucleus-encoded proteins that are imported from the cytosol by translocases in the chloroplast envelope membranes. Proteolytic regulation of the translocases is critically important, but little is known about the underlying mechanisms. We applied forward genetics and proteomics in Arabidopsis to identify factors required for chloroplast outer envelope membrane (OEM) protein degradation. We identified SP2, an Omp85-type β-barrel channel of the OEM, and CDC48, a cytosolic AAA+ (ATPase associated with diverse cellular activities) chaperone. Both proteins acted in the same pathway as the ubiquitin E3 ligase SP1, which regulates OEM translocase components. SP2 and CDC48 cooperated to bring about retrotranslocation of ubiquitinated substrates from the OEM (fulfilling conductance and motor functions, respectively), enabling degradation of the substrates by the 26S proteasome in the cytosol. Such chloroplast-associated protein degradation (CHLORAD) is vital for organellar functions and plant development.