The autophagy receptor NBR1 directs the clearance of photodamaged chloroplasts

Lee, Han Nim; Chacko, Jenu Varghese; Gonzalez Solís, Ariadna; Chen, Kuo-En; Barros, Jessica AS; Signorelli, Santiago; Millar, A. Harvey; Vierstra, Richard David; Eliceiri, Kevin W.; Otegui, Marisa S.

doi:10.7554/elife.86030

Title: The autophagy receptor NBR1 directs the clearance of photodamaged chloroplasts

Journal Article · 18 April 2023 · eLife

DOI: https://doi.org/10.7554/elife.86030 · OSTI ID:1970384

^[1];

^[1]; Gonzalez Solís, Ariadna ^[1]; Chen, Kuo-En ^[2]; Barros, Jessica AS ^[2]; Signorelli, Santiago ^[3]; Millar, A. Harvey ^[4];

^[2];

^[5];

^[1]

Univ. of Wisconsin, Madison, WI (United States)
Washington Univ., St. Louis, MO (United States)
Univ. of Western Australia, Perth, WA (Australia); Universidad de la República (Uruguay)
Univ. of Western Australia, Perth, WA (Australia)
Univ. of Wisconsin, Madison, WI (United States); Morgridge Institute for Research, Madison, WI (United States)

The ubiquitin-binding NBR1 autophagy receptor plays a prominent role in recognizing ubiquitylated protein aggregates for vacuolar degradation by macroautophagy. Here, we show that upon exposing Arabidopsis plants to intense light, NBR1 associates with photodamaged chloroplasts independently of ATG7, a core component of the canonical autophagy machinery. NBR1 coats both the surface and interior of chloroplasts, which is then followed by direct engulfment of the organelles into the central vacuole via a microautophagy-type process. The relocalization of NBR1 into chloroplasts does not require the chloroplast translocon complexes embedded in the envelope but is instead greatly enhanced by removing the self-oligomerization mPB1 domain of NBR1. The delivery of NBR1-decorated chloroplasts into vacuoles depends on the ubiquitin-binding UBA2 domain of NBR1 but is independent of the ubiquitin E3 ligases SP1 and PUB4, known to direct the ubiquitylation of chloroplast surface proteins. Compared to wild-type plants, nbr1 mutants have altered levels of a subset of chloroplast proteins and display abnormal chloroplast density and sizes upon high light exposure. We postulate that, as photodamaged chloroplasts lose envelope integrity, cytosolic ligases reach the chloroplast interior to ubiquitylate thylakoid and stroma proteins which are then recognized by NBR1 for autophagic clearance. This study uncovers a new function of NBR1 in the degradation of damaged chloroplasts by microautophagy.

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Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC); USDOE

Grant/Contract Number:: SC0019013

OSTI ID:: 1970384

Alternate ID(s):: OSTI ID: 1970386; OSTI ID: 2420899

Journal Information:: eLife, Vol. 12; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

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autophagy receptor

Title: The autophagy receptor NBR1 directs the clearance of photodamaged chloroplasts

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