Autophagy Increases Zinc Bioavailability to Avoid Light-Mediated Reactive Oxygen Species Production under Zinc Deficiency

Daiki Shinozaki, Ekaterina A. Merkulova, Loreto Naya, Tetsuro Horie, Yuri Kanno, Mitsunori Seo, Yoshinori Ohsumi, Céline Masclaux-Daubresse, Kohki Yoshimoto

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Abstract

Zinc (Zn) is an essential micronutrient for plant growth. Accordingly, Zn deficiency (-Zn) in agricultural fields is a serious problem, especially in developing regions. Autophagy, a major intracellular degradation system in eukaryotes, plays important roles in nutrient recycling under nitrogen and carbon starvation. However, the relationship between autophagy and deficiencies of other essential elements remains poorly understood, especially in plants. In this study, we focused on Zn due to the property that within cells most Zn is tightly bound to proteins, which can be targets of autophagy. We found that autophagy plays a critical role during -Zn in Arabidopsis (Arabidopsis thaliana). Autophagy-defective plants (atg mutants) failed to grow and developed accelerated chlorosis under -Zn. As expected, -Zn induced autophagy in wild-type plants, whereas in atg mutants, various organelle proteins accumulated to high levels. Additionally, the amount of free Zn2+ was lower in atg mutants than in control plants. Interestingly, -Zn symptoms in atg mutants recovered under low-light, iron-limited conditions. The levels of hydroxyl radicals in chloroplasts were elevated, and the levels of superoxide were reduced in -Zn atg mutants. These results imply that the photosynthesis-mediated Fenton-like reaction, which is responsible for the chlorotic symptom of -Zn, is accelerated in atg mutants. Together, our data indicate that autophagic degradation plays important functions in maintaining Zn pools to increase Zn bioavailability and maintain reactive oxygen species homeostasis under -Zn in plants.

Original languageEnglish
Pages (from-to)1284-1296
Number of pages13
JournalPlant physiology
Volume182
Issue number3
DOIs
Publication statusPublished - 1 Mar 2020

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Shinozaki, D., Merkulova, E. A., Naya, L., Horie, T., Kanno, Y., Seo, M., Ohsumi, Y., Masclaux-Daubresse, C., & Yoshimoto, K. (2020). Autophagy Increases Zinc Bioavailability to Avoid Light-Mediated Reactive Oxygen Species Production under Zinc Deficiency. Plant physiology, 182(3), 1284-1296. https://doi.org/10.1104/pp.19.01522