Autophagy of Chloroplasts During Leaf Senescence
During leaf senescence, chloroplasts undergo the programmed breakdown of both stromal and thylakoid components of the photosynthetic apparatus. This strategy has evolved to remobilize nutrients from old leaves into newly developing tissues and sustain maximal growth rates. After the remobilization of chloroplast components, some shrunken chloroplasts called gerontoplasts, which are plastid structures formed by the loss of the thylakoid membrane network, remain in the cytoplasm. Concomitantly, the population of chloroplasts is decreased in mesophyll cells. The morphological traits of senescing cells, including the capture of whole chloroplasts in the vacuole has been observed by electron microscopy since the early 1980s. Chloroplast degradation in the vacuole has been observed.
Recent genome-wide analysis has shed light on autophagy, a bulk protein degradation system well-conserved in eukaryotes ranging from yeast to mammals, in plants. The improvement of techniques for imaging living cells has enabled researchers to describe the characteristic substrate trafficking across membranes from the cytoplasm into the vacuole. By applying our understanding of the degradation mechanism of autophagy characterized in yeasts to plants, chloroplasts were shown to be degraded by autophagy during leaf senescence.
Chloroplast autophagy occurs by two different pathways. The first is partial degradation via vesicle trafficking. Chloroplasts produce vesicles, named Rubisco-containing bodies (RCBs), which contain only the stromal fraction. RCB formation is affected by the carbon status of the cell, and is specifically linked to photosynthesis inside chloroplasts. RCBs are finally transported and degraded in the vacuole by autophagy. The second pathway is the autophagy of whole chloroplasts, and their degradation inside the vacuole. These pathways of chloroplast autophagy exist as one of the degradation mechanisms of chloroplast components during leaf senescence, causing a decrease in chloroplast size and number.
KeywordsLeaf Senescence Autophagosome Membrane Selective Autophagy Stromal Protein Nitrogen Remobilization
- ATG genes;
Autophagy related genes;
Green fluorescent protein;
Individually darkened leaves;
We dedicate this review to Prof. Dr. Tadahiko Mae who originated this work in our laboratory, and thank Prof. Dr. Amane Makino and Dr. Yuji Suzuki for helpful advice to guide our investigations. We thank Dr. Louis Irving for critical reading of the manuscript. We also thank all lab members and collaborators, especially Dr. Masanori Izumi, Dr. Kohki Yoshimoto, Prof. Dr. Yoshinori Ohsumi, and Prof. Dr. Maureen R. Hanson. The authors’ work was supported by KAKENHI (grant nos. 18780042, 19039004, 20200061, 20780044, and 22780054).
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