Autophagic degradation of the chloroplastic 2-phosphoglycolate phosphatase TaPGLP1 in wheat

• Published in: Plant cell reports Vol. 41; no. 2; pp. 473 - 487
• Main Authors: Ni, Jiayao, Li, Yuru, Xiang, Yue, Yang, Xiangyun, Jia, Lei, Yue, Jieyu, Wang, Huazhong
• Format: Journal Article
• Language: English
• Published: Berlin/Heidelberg Springer Berlin Heidelberg 01.02.2022; Springer Nature B.V
• Subjects: Autophagy; Autophagy - physiology; Autophagy-Related Proteins - genetics; Autophagy-Related Proteins - metabolism; Biomedical and Life Sciences; Biotechnology; Cell Biology; Chloroplasts; Chloroplasts - metabolism; Degradation; Gene silencing; Life Sciences; Luminescent Proteins - genetics; Luminescent Proteins - metabolism; Mesophyll; Mesophyll Cells - metabolism; Nutrition; Original Article; Phosphatase; Phosphoglycolate phosphatase; Phosphoric Monoester Hydrolases - genetics; Phosphoric Monoester Hydrolases - metabolism; Plant Biochemistry; Plant Proteins - genetics; Plant Proteins - metabolism; Plant Sciences; Plants, Genetically Modified; Protein Transport; Proteins; Protoplasts; Red Fluorescent Protein; Stroma; Triticum - cytology; Triticum - genetics; Triticum - metabolism; Vacuoles; Wheat; L.; 2-Phosphoglycolate phosphatase (PGLP); Autophagy; Wheat; Chloroplast; Wheat (Triticum aestivum L.)
• ISSN: 0721-7714; 1432-203X
• DOI: 10.1007/s00299-021-02820-3

Key message TaPGLP1, a chloroplast stromal 2-phosphoglycolate phosphatase of wheat, is an ATG8-interacting protein and undergoes autophagic degradation in starvation-treated wheat mesophyll protoplasts. Selective autophagy in plants has been shown to target diverse cellular cargoes including whole chloroplasts (Chlorophagy) and several chloroplast components (Piecemeal chlorophagy). Most cargoes of selective autophagy are captured by the autophagic machinery through their direct or indirect interactions with the autophagy-essential factor ATG8. Here, we reported a new ATG8-interacting cargo of piecemeal chlorophagy, the wheat photorespiratory 2-phosphoglycolate phosphatase TaPGLP1. The TaPGLP1-mCherry fusions expressed in wheat protoplasts located in the chloroplast stroma. Strikingly, these fusions are translocated into newly formed chloroplast surface protrusions after a long time incubation of protoplasts in a nutrition-free solution. Visualization of co-expressed TaPGLP1-mCherry and the autophagy marker GFP-TaATG8a revealed physical associations of TaPGLP1-mCherry-accumulating chloroplast protrusions with autophagic structures, implying the delivery of TaPGLP1-mCherry fusions from chloroplasts to the autophagic machinery. TaPGLP1-mCherry fusions were also detected in the GFP-TaATG8a-labelled autophagic bodies undergoing degradation in the vacuoles, which suggested the autophagic degradation of TaPGLP1. This autophagic degradation of TaPGLP1 was further demonstrated by the enhanced stability of TaPGLP1-mCherry in protoplasts with impaired autophagy. Expression of TaPGLP1-mCherry in protoplasts stimulated an enhanced autophagy level probably adopted by cells to degrade the over-produced TaPGLP1-mCherry fusions. Results from gene silencing assays showed the requirement of ATG2s and ATG7s in the autophagic degradation of TaPGLP1. Additionally, TaPGLP1 was shown to interact with ATG8 family members. Collectively, our data suggest that autophagy mediates the degradation of the chloroplast stromal protein TaPGLP1 in starvation-treated mesophyll protoplasts.