Singlet Oxygen Leads to Structural Changes to Chloroplasts during their Degradation in the Arabidopsis thaliana plastid ferrochelatase two Mutant

Journal Article · Wed Nov 24 04:00:00 EST 2021 · Plant and Cell Physiology

DOI:https://doi.org/10.1093/pcp/pcab167· OSTI ID:1845154

Fisher, Karen E.; Krishnamoorthy, Praveen; Joens, Matthew S.; Chory, Joanne; Fitzpatrick, James A. J.; Woodson, Jesse D.

Abstract

During stress, chloroplasts produce large amounts of reactive oxygen species (ROS). Chloroplasts also contain many nutrients, including 80% of a leaf’s nitrogen supply. Therefore, to protect cells from photo-oxidative damage and to redistribute nutrients to sink tissues, chloroplasts are prime targets for degradation. Multiple chloroplast degradation pathways are induced by photo-oxidative stress or nutrient starvation, but the mechanisms by which damaged or senescing chloroplasts are identified, transported to the central vacuole and degraded are poorly defined. Here, we investigated the structures involved with degrading chloroplasts induced by the ROS singlet oxygen (1O2) in the Arabidopsis thaliana plastid ferrochelatase two (fc2) mutant. Under mild 1O2 stress, most fc2 chloroplasts appeared normal, but had reduced starch content. A subset of chloroplasts was degrading, and some protruded into the central vacuole via ‘blebbing’ structures. A 3D electron microscopy analysis demonstrated that up to 35% of degrading chloroplasts contained such structures. While the location of a chloroplast within a cell did not affect the likelihood of its degradation, chloroplasts in spongy mesophyll cells were degraded at a higher rate than those in palisade mesophyll cells. To determine if degrading chloroplasts have unique structural characteristics, allowing them to be distinguished from healthy chloroplasts, we analyzed fc2 seedlings grown under different levels of photo-oxidative stress. A correlation was observed among chloroplast swelling, 1O2 signaling and the state of degradation. Finally, plastoglobule (PG) enzymes involved in chloroplast disassembly were upregulated while PGs increased their association with the thylakoid grana, implicating an interaction between 1O2-induced chloroplast degradation and senescence pathways.

• Sponsoring Organization: USDOE
• Grant/Contract Number: FG02-04ER15540; SC0019573
• OSTI ID: 1845154
• Alternate ID(s): OSTI ID: 1833423; OSTI ID: 1880339; OSTI ID: 2503485
• Journal Information: Plant and Cell Physiology, Journal Name: Plant and Cell Physiology Journal Issue: 2 Vol. 63; ISSN 0032-0781
• Publisher: Oxford University Press
• Country of Publication: Japan
• Language: English