Assessment and optimization of autophagy monitoring methods in arabidopsis roots indicate direct fusion of autophagosomes with vacuoles

Plant and Cell Physiology

Volumn 55, Issue 4, 2014, Pages 715-726

  Merkulova, Ekaterina A ^a   Guiboileau, Anne ^a   Naya, Loreto ^a   Masclaux Daubresse, Céline ^a   Yoshimoto, Kohki ^a  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

Author keywords

Acidotropic dye; Arabidopsis thaliana; ATG8; Autophagosome; Autophagy; Monitoring

Indexed keywords

(3-ETHOXYCARBONYLOXIRANE-2-CARBONYL)LEUCINE (3-METHYLBUTYL) AMIDE; AMINE; ANDROSTANE DERIVATIVE; ARABIDOPSIS PROTEIN; CADAVERINE; DANSYLCADAVERINE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; LEUCINE; RED DND-99; WORTMANNIN;

ANALOGS AND DERIVATIVES; ARABIDOPSIS; AUTOPHAGY; CELL VACUOLE; CYTOLOGY; DRUG EFFECTS; KINETICS; LYSOSOME; MEMBRANE FUSION; METABOLISM; PHAGOSOME; PLANT CELL; PLANT ROOT; PROCEDURES; STAINING; TOBACCO; TRANSGENIC PLANT;

AMINES; ANDROSTADIENES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; AUTOPHAGY; CADAVERINE; CYTOLOGICAL TECHNIQUES; GREEN FLUORESCENT PROTEINS; KINETICS; LEUCINE; LYSOSOMES; MEMBRANE FUSION; PHAGOSOMES; PLANT CELLS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; RECOMBINANT FUSION PROTEINS; STAINING AND LABELING; TOBACCO; VACUOLES;

EID: 84898885017     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcu041     Document Type: Article

References (43)

1. Blommaart, E.F.C., Krause, U., Schellens, J.P.M., Vreeling- Sindelárová, H. and Meijer, A.J. (1997) The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hep-atocytes. Eur. J. Biochem. 243: 240-246.
2. Chikte, S., Panchal, N. and Warnes, G. (2014) Use of LysoTracker dyes: a flow cytometric study of autophagy. Cytometry A 85: 169-178.
3. Chung, T., Phillips, A.R. and Vierstra, R. (2010) ATG8 lipidation and ATG8-mediated autophagy in Arabidopsis require ATG12 expressed from the differentially controlled ATG12A and ATG12B loci. Plant J. 62: 483-493.
4. Contento, A.L., Xiong, Y. and Bassham, D.C. (2005) Visualization of autophagy in Arabidopsis using the fluorescent dye monodansylca-daverine and a GFP-AtATG8e fusion protein. Plant J. 42: 598-608.
5. Deprost, D., Yao, L., Sormani, R., Moreau, M., Leterreux, G., Nicolai, M. et al. (2007) The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Rep. 8: 864-870.
6. Doelling, J.H., Walker, J.M., Friedman, E.M., Thompson, A.R. and Vierstra, R.D. (2002) The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J. Biol. Chem. 277: 33105-33114.
7. Fujiwara, T., Hirai, M.Y., Chino, M., Komeda, Y. and Naito, S. (1992) Effects of sulfur nutrition on expression of the soybean seed storage protein genes in transgenic petunia. Plant Physiol. 99: 263-268.
8. Guiboileau, A., Avila-Ospina, L., Yoshimoto, K., Soulay, F., Azzopardi, M., Marmagne, A. et al. (2013) Physiological and metabolic consequences of autophagy deficiency for the management of nitrogen and protein resources in Arabidopsis leaves depending on nitrate availability. New Phytol. 199: 683-694.
9. Guiboileau, A., Yoshimoto, K., Soulay, F., Bataille, M.-P., Avice, J.-C. and Masclaux-Daubresse, C. (2012) Autophagy machinery controls nitrogen remobilization at the whole-plant level under both limiting and ample nitrate conditions in Arabidopsis. New Phytol. 194: 732-740.
10. Hanaoka, H., Noda, T., Shirano, Y., Kato, T., Hayashi, H., Shibata, D. et al. (2002) Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol. 129: 1181-1193.
11. Hofius, D., Schultz-Larsen, T., Joensen, J., Tsitsigiannis, D.I., Petersen, N.H.T., Mattsson, O. et al. (2009) Autophagic components contribute to hypersensitive cell death in Arabidopsis. Cell 137: 773-783.
12. Inoue, Y., Suzuki, T., Hattori, M., Yoshimoto, K., Ohsumi, Y. and Moriyasu, Y. (2006) AtATG genes, homologs of yeast autophagy genes, are involved in constitutive autophagy in Arabidopsis root tip cells. Plant Cell Physiol. 47: 1641-1652.
13. Izumi, M., Wada, S., Makino, A. and Ishida, H. (2010) The autophagic degradation of chloroplasts via rubisco-containing bodies is specifically linked to leaf carbon status but not nitrogen status in Arabidopsis. Plant Physiol. 154: 1196-1209.
14. Klionsky, D.J. (2007) Autophagy: from phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 8: 931-937.
15. Kwon, S.I., Cho, H.J., Kim, S.R. and Park, O.K. (2013) The Rab GTPase RabG3b positively regulates autophagy and immunity-associated hypersensitive cell death in Arabidopsis. Plant Physiol. 161: 1722-1736.
16. Liu, Y., Schiff, M., Czymmek, K., Tallóczy, Z., Levine, B. and Dinesh-Kumar, S.P. (2005) Autophagy regulates programmed cell death during the plant innate immune response. Cell 121: 567-577.
17. Liu, Y. and Bassham, D.C. (2010) TOR is a negative regulator of autop-hagy in Arabidopsis thaliana. PLoS One 5: e11883.
18. Mizushima, N. (2007) Autophagy: process and function. Genes Dev. 21: 2861-2873.
19. Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T. and Ohsumi, Y. (2004) In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol. Biol. Cell 15: 1101-1111.
20. Moriyasu, Y., Hattori, M., Jauh, G.-Y. and Rogers, J.C. (2003) Alpha tonoplast intrinsic protein is specifically associated with vacuole membrane involved in an autophagic process. Plant Cell Physiol. 44: 795-802.
21. Moriyasu, Y. and Inoue, Y. (2008) Use of protease inhibitors for detecting autophagy in plants. Methods Enzymol. 451: 557-580.
22. Munafó, D.B. and Colombo, M.I. (2001) A novel assay to study autop-hagy: regulation of autophagosome vacuole size by amino acid deprivation. J. Cell Sci. 114: 3619-3629.
23. Otegui, M.S., Noh, Y.-S., Mart́inez, D.E., Vila Petroff, M.G., Staehelin, L.A., Amasino, R.M. et al. (2005) Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. Plant J. 41: 831-844.
24. Reumann, S., Voitsekhovskaja, O. and Lillo, C. (2010) From signal trans-duction to autophagy plant cell organelles: lessons from yeast and mammals and plant-specific features. Protoplasma 247: 233-256.
25. Rodriguez-Enriquez, S., Kim, I., Currin, R.T. and Lemasters, J.J. (2006) Tracker dyes to probe mitochondrial autophagy (mitophagy) in rat hepatocytes. Autophagy 2: 39-46.
26. Sabnis, R.W. (2010) Handbook of Biological Dyes and Stains: Synthesis and Industrial Applications. John Wiley & Sons, Inc., Hoboken, NJ.
27. Saito, C., Uemura, T., Awai, C., Tominaga, M., Ebine, K., Ito, J. et al. (2011) The occurrence of 'bulbs', a complex configuration of the vacuolar membrane, is affected by mutations of vacuolar SNARE and phospholipase in Arabidopsis. Plant J. 68: 64-73.
28. Sláviková, S., Shy, G., Yao, Y., Glozman, R., Levanony, H., Pietrokovski, S. et al. (2005) The autophagy-associated Atg8 gene family operates both under favourable growth conditions and under starvation stresses in Arabidopsis plants. J. Exp. Bot. 56: 2839-2849.
29. Suzuki, K., Kubota, Y., Sekito, T. and Ohsumi, Y. (2007) Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 12: 209-218.
30. Takatsuka, C., Inoue, Y., Higuchi, T., Hillmer, S., Robinson, D.G. and Moriyasu, Y. (2011) Autophagy in tobacco BY-2 cells cultured under sucrose starvation conditions: isolation of the autolysosome and its characterization. Plant Cell Physiol. 52: 2074-2087.
31. Takatsuka, C., Inoue, Y., Matsuoka, K. and Moriyasu, Y. (2004) 3-Methyladenine inhibits autophagy in tobacco culture cells under sucrose starvation conditions. Plant Cell Physiol. 45: 265-274.
32. Tanida, I. (2011) Autophagosome formation and molecular mechanism of autophagy. Antioxid. Redox Signal. 14: 2201-2214.
33. Thompson, A.R., Doelling, J.H., Suttangkakul, A. and Vierstra, R.D. (2005) Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol. 138: 2097-2110.
34. Uemura, T., Morita, M.T., Ebine, K., Okatani, Y., Yano, D., Saito, C. et al. (2010) Vacuolar/pre-vacuolar compartment Qa-SNAREs VAM3/SYP22 and PEP12/SYP21 have interchangeable functions in Arabidopsis. Plant J. 64: 864-873.
35. Viotti, C., Krüger, F., Krebs, M., Neubert, C., Fink, F., Lupanga, U. et al. (2013) The endoplasmic reticulum is the main membrane source for biogenesis of the lytic vacuole in Arabidopsis. Plant Cell 25: 3434-3449.
36. Xie, Z. and Klionsky, D.J. (2007) Autophagosome formation: core machinery and adaptations. Nat. Cell Biol. 9: 1102-1109.
37. Xie, Z., Nair, U. and Klionsky, D.J. (2008) Atg8 controls phagophore expansion during autophagosome formation. Mol. Biol. Cell 19: 3290-3298.
38. Xiong, Y., Contento, A.L., Nguyen, P.Q. and Bassham, D.C. (2007) Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol. 143: 291-299.
39. Yamada, K., Fuji, K., Shimada, T., Nishimura, M. and Hara-Nishimura, I. (2005) Endosomal processes facilitate the fusion of endosomes with vacuoles at the final step of the endocytotic pathway. Plant J. 41: 888-898.
40. Yano, K., Matsui, S., Tsuchiya, T., Maeshima, M., Kutsuna, N., Hasezawa, S. et al. (2004) Contribution of the plasma membrane and central vacuole in the formation of autolysosomes in cultured tobacco cells. Plant Cell Physiol. 45: 951-957.
41. Yoshimoto, K., Hanaoka, H., Sato, S., Kato, T., Tabata, S., Noda, T. et al. (2004) Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell 16: 2967-2983.
42. Yoshimoto, K. (2012) Beginning to understand autophagy, an intra-cellular self degradation system in plants. Plant Cell Physiol. 53: 1355-1365.
43. Yoshimoto, K., Jikumaru, Y., Kamiya, Y., Kusano, M., Consonni, C., Panstruga, R. et al. (2009) Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell 21: 2914-2927.