Autophagy-related (ATG) 11, ATG9 and the Phosphatidylinositol 3-kinase Control ATG2-mediated Formation of Autophagosomes in Arabidopsis

Overview

Journal Plant Cell Rep

Publisher Springer

Date 2018 Jan 20

PMID 29350244

Citations 34

Authors

Sangwoo Kang

Kwang Deok Shin

Jeong Hun Kim

Taijoon Chung

Affiliations

Soon will be listed here.

Abstract

Using quantitative assays for autophagy, we analyzed 4 classes of atg mutants, discovered new atg2 phenotypes and ATG gene interactions, and proposed a model of autophagosome formation in plants. Plant and other eukaryotic cells use autophagy to target cytoplasmic constituents for degradation in the vacuole. Autophagy is regulated and executed by a conserved set of proteins called autophagy-related (ATG). In Arabidopsis, several groups of ATG proteins have been characterized using genetic approaches. However, the genetic interactions between ATG genes have not been established and the relationship between different ATG groups in plants remains unclear. Here we analyzed atg2, atg7, atg9, and atg11 mutants and their double mutants at the physiological, biochemical, and subcellular levels. Involvement of phosphatidylinositol 3-kinase (PI3K) in autophagy was also tested using wortmannin, a PI3K inhibitor. Our mutant analysis using autophagy markers showed that atg7 and atg2 phenotypes are more severe than those of atg11 and atg9. Unlike other mutants, atg2 cells accumulated several autophagic vesicles that could not be delivered to the vacuole. Analysis of atg double mutants, combined with wortmannin treatment, indicated that ATG11, PI3K, and ATG9 act upstream of ATG2. Our data support a model in which plant ATG1 and PI3K complexes play a role in the initiation of autophagy, whereas ATG2 is involved in a later step during the biogenesis of autophagic vesicles.

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References

Suzuki K, Kubota Y, Sekito T, Ohsumi Y . Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells. 2007; 12(2):209-18. DOI: 10.1111/j.1365-2443.2007.01050.x. View

Li F, Chung T, Vierstra R . AUTOPHAGY-RELATED11 plays a critical role in general autophagy- and senescence-induced mitophagy in Arabidopsis. Plant Cell. 2014; 26(2):788-807. PMC: 3967041. DOI: 10.1105/tpc.113.120014. View

Kim J, Lee H, Lee H, Kim S, Shin K, Chung T . Autophagy-related proteins are required for degradation of peroxisomes in Arabidopsis hypocotyls during seedling growth. Plant Cell. 2013; 25(12):4956-66. PMC: 3903998. DOI: 10.1105/tpc.113.117960. View

Shibutani S, Yoshimori T . A current perspective of autophagosome biogenesis. Cell Res. 2013; 24(1):58-68. PMC: 3879706. DOI: 10.1038/cr.2013.159. View

Oxley D, Ktistakis N, Farmaki T . Differential isolation and identification of PI(3)P and PI(3,5)P2 binding proteins from Arabidopsis thaliana using an agarose-phosphatidylinositol-phosphate affinity chromatography. J Proteomics. 2013; 91:580-94. DOI: 10.1016/j.jprot.2013.08.020. View

Yoshimoto K, Hanaoka H, Sato S, Kato T, Tabata S, Noda T . Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell. 2004; 16(11):2967-83. PMC: 527192. DOI: 10.1105/tpc.104.025395. View

Lenz H, Haller E, Melzer E, Kober K, Wurster K, Stahl M . Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens. Plant J. 2011; 66(5):818-30. DOI: 10.1111/j.1365-313X.2011.04546.x. View

Fujiki Y, Yoshimoto K, Ohsumi Y . An Arabidopsis homolog of yeast ATG6/VPS30 is essential for pollen germination. Plant Physiol. 2007; 143(3):1132-9. PMC: 1820928. DOI: 10.1104/pp.106.093864. View

Farmer L, Rinaldi M, Young P, Danan C, Burkhart S, Bartel B . Disrupting autophagy restores peroxisome function to an Arabidopsis lon2 mutant and reveals a role for the LON2 protease in peroxisomal matrix protein degradation. Plant Cell. 2013; 25(10):4085-100. PMC: 3877801. DOI: 10.1105/tpc.113.113407. View

10.

Russell R, Tian Y, Yuan H, Park H, Chang Y, Kim J . ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase. Nat Cell Biol. 2013; 15(7):741-50. PMC: 3885611. DOI: 10.1038/ncb2757. View

11.

Zhou C, Ma K, Gao R, Mu C, Chen L, Liu Q . Regulation of mATG9 trafficking by Src- and ULK1-mediated phosphorylation in basal and starvation-induced autophagy. Cell Res. 2016; 27(2):184-201. PMC: 5339848. DOI: 10.1038/cr.2016.146. View

12.

Carlsson S, Simonsen A . Membrane dynamics in autophagosome biogenesis. J Cell Sci. 2015; 128(2):193-205. DOI: 10.1242/jcs.141036. View

13.

Zhuang X, Wang H, Lam S, Gao C, Wang X, Cai Y . A BAR-domain protein SH3P2, which binds to phosphatidylinositol 3-phosphate and ATG8, regulates autophagosome formation in Arabidopsis. Plant Cell. 2013; 25(11):4596-615. PMC: 3875738. DOI: 10.1105/tpc.113.118307. View

14.

Papinski D, Schuschnig M, Reiter W, Wilhelm L, Barnes C, Maiolica A . Early steps in autophagy depend on direct phosphorylation of Atg9 by the Atg1 kinase. Mol Cell. 2014; 53(3):471-83. PMC: 3978657. DOI: 10.1016/j.molcel.2013.12.011. View

15.

Michaeli S, Galili G, Genschik P, Fernie A, Avin-Wittenberg T . Autophagy in Plants--What's New on the Menu?. Trends Plant Sci. 2015; 21(2):134-144. DOI: 10.1016/j.tplants.2015.10.008. View

16.

Yoshimoto K, Shibata M, Kondo M, Oikawa K, Sato M, Toyooka K . Organ-specific quality control of plant peroxisomes is mediated by autophagy. J Cell Sci. 2014; 127(Pt 6):1161-8. DOI: 10.1242/jcs.139709. View

17.

Merkulova E, Guiboileau A, Naya L, Masclaux-Daubresse C, Yoshimoto K . Assessment and optimization of autophagy monitoring methods in Arabidopsis roots indicate direct fusion of autophagosomes with vacuoles. Plant Cell Physiol. 2014; 55(4):715-26. DOI: 10.1093/pcp/pcu041. View

18.

Fujioka Y, Noda N, Fujii K, Yoshimoto K, Ohsumi Y, Inagaki F . In vitro reconstitution of plant Atg8 and Atg12 conjugation systems essential for autophagy. J Biol Chem. 2007; 283(4):1921-8. DOI: 10.1074/jbc.M706214200. View

19.

Thompson A, Doelling J, Suttangkakul A, Vierstra R . Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol. 2005; 138(4):2097-110. PMC: 1183398. DOI: 10.1104/pp.105.060673. View

20.

Shin K, Lee H, Chung T . A revised assay for monitoring autophagic flux in Arabidopsis thaliana reveals involvement of AUTOPHAGY-RELATED9 in autophagy. Mol Cells. 2014; 37(5):399-405. PMC: 4044311. DOI: 10.14348/molcells.2014.0042. View