Evidence for autophagy-dependent pathways of rRNA turnover in Arabidopsis

Autophagy

Volumn 11, Issue 12, 2015, Pages 2199-2212

  Floyd, Brice E ^a   Morriss, Stephanie C ^a   MacIntosh, Gustavo C ^a   Bassham, Diane C ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

Arabidopsis thaliana; Atg5 1; Atg9 4; Autophagosome; Autophagy; Ribosome turnover; RNS2; rRNA; Vacuole

Indexed keywords

AUTOPHAGY PROTEIN 5; AUTOPHAGY PROTEIN 9; PROTEIN; RIBONUCLEASE; RIBOSOME RNA; RNS2 RIBONUCLEASE; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN;

ARABIDOPSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL VACUOLE; CONTROLLED STUDY; MUTANT; NONHUMAN; RIBOSOME; RNA DEGRADATION; TURNOVER TIME; GENETICS; METABOLISM; MUTATION; PHENOTYPE; RNA STABILITY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; AUTOPHAGY; MUTATION; PHENOTYPE; RIBOSOMES; RNA STABILITY; RNA, RIBOSOMAL; VACUOLES;

EID: 84964267365     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2015.1106664     Document Type: Article

References (95)

1. Warner JR. The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 1999; 24: 437-40; http://dx. doi.org/10.1016/S0968-0004(99)01460-7
2. Loffler A, Abel S, Jost W, Beintema JJ, Glund K. Phosphate- regulated induction of intracellular ribonucleases in cultured tomato (Lycopersicon esculentum) cells. Plant Physiol 1992; 98: 1472-8; PMID: 16668816; http://dx.doi.org/10.1104/pp.98.4.1472
3. Klemperer HG, Pilley DJ. The breakdown of tetrahymena ribosomes by lysosomal-enzymes - inhibition by cytosol. Int J Biochem 1985; 17: 399-404; http://dx. doi.org/10.1016/0020-711X(85)90217-4
4. Lardeux BR, Mortimore GE. Amino acid and hormonal control of macromolecular turnover in perfused rat liver. Evidence for selective autophagy. J Biol Chem 1987; 262: 14514-9
5. Huang H, Kawamata T, Horie T, Tsugawa H, Nakayama Y, Ohsumi Y, Fukusaki E. Bulk RNA degradation by nitrogen starvation-induced autophagy in yeast. EMBO J 2015; 34: 154-68; PMID: 25468960; http://dx.doi.org/10.15252/embj.201489083
6. Liu Y, Bassham DC. Autophagy: pathways for self-eating in plant cells. Annu Rev Plant Biol 2012; 63: 215-37; PMID: 22242963; http://dx.doi.org/10.1146/ annurev-arplant-042811-105441
7. Thompson AR, Vierstra RD. Autophagic recycling: lessons from yeast help define the process in plants. Curr Opin Plant Biol 2005; 8: 165-73; PMID: 15752997; http://dx.doi.org/10.1016/j.pbi.2005.01.013
8. Li F, Vierstra RD. Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci 2012; 17: 526-37; http://dx.doi.org/10.1016/ j.tplants.2012.05.006
9. Floyd BE, Morriss SC, Macintosh GC, Bassham DC. What to eat: Evidence for selective autophagy in plants. J Integr Plant Biol 2012; 54: 907-20; PMID: 23046163
10. Grasso D, Ropolo A, Lo Re A, Boggio V, Molejon MI, Iovanna JL, Gonzalez CD, Urrutia R, Vaccaro MI. Zymophagy, a novel selective autophagy pathway mediated by VMP1-USP9x-p62, prevents pancreatic cell death. J Biol Chem 2011; 286: 8308-24; http://dx. doi.org/10.1074/jbc.M110.197301
11. Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 2011; 7: 279-96; PMID: 21189453; http://dx.doi.org/10.4161/auto.7.3.14487
12. Kageyama T, Suzuki K, Ohsumi Y. Lap3 is a selective target of autophagy in yeast, Saccharomyces cerevisiae. Biochem Biophys Res Commun 2009; 378: 551-7; PMID: 19061865; http://dx.doi.org/10.1016/j. bbrc.2008.11.084
13. Kim I, Rodriguez-Enriquez S, Lemasters JJ. Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys 2007; 462: 245-53; PMID: 17475204; http://dx.doi.org/10.1016/j.abb.2007.03.034
14. Kraft C, Peter M, Hofmann K. Selective autophagy: ubiquitin-mediated recognition and beyond. Nat Cell Biol 2010; 12: 836-41; http://dx.doi.org/10.1038/ ncb0910-836
15. Kraft C, Deplazes A, Sohrmann M, Peter M. Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat Cell Biol 2008; 10: 602-10; http://dx.doi.org/10.1038/ncb1723
16. Davey HM, Cross EJ, Davey CL, Gkargkas K, Delneri D, Hoyle DC, Oliver SG, Kell DB, Griffith GW. Genome-wide analysis of longevity in nutrientdeprived Saccharomyces cerevisiae reveals importance of recycling in maintaining cell viability. Environ Microbiol 2012; 14: 1249-60; http://dx.doi.org/10.1111/j.1462-2920.2012.02705.x
17. Cebollero E, Reggiori F, Kraft C. Reticulophagy and ribophagy: Regulated degradation of protein production factories. Int J Cell Biol 2012; 2012: 182834; PMID: 22481944; http://dx.doi.org/10.1155/2012/182834
18. Haud N, Kara F, Diekmann S, Henneke M, Willer JR, Hillwig MS, Gregg RG, MacIntosh GC, Gärtner J, Alia A, et al. rnaset2 mutant zebrafish model familial cystic leukoencephalopathy and reveal a role for RNase T2 in degrading ribosomal RNA. Proc Natl Acad Sci USA 2011; 108: 1099-103; http://dx.doi.org/10.1073/ pnas.1009811107
19. Hillwig MS, Contento AL, Meyer A, Ebany D, Bassham DC, Macintosh GC. RNS2, a conserved member of the RNase T2 family, is necessary for ribosomal RNA decay in plants. Proc Natl Acad Sci USA 2011; 108: 1093-8; http://dx.doi.org/10.1073/ pnas.1009809108
20. MacIntosh GC. RNase T2 family: Enzymatic properties, functional diversity, and evolution of ancient ribonucleases. In: AW Nicholson, ed. Berlin Heidelberg: Ribonucleases, Nucleic Acids and Molecular Biology Springer-Verlag; 2011, 2011.
21. MacIntosh GC, Bariola PA, Newbigin E, Green PJ. Characterization of Rny1, the Saccharomyces cerevisiae member of the T2 RNase family of RNases: unexpected functions for ancient enzymes Proc Natl Acad Sci USA 2001; 98: 1018-23; PMID: 11158587; http://dx.doi. org/10.1073/pnas.98.3.1018
22. Thompson DM, Parker R. The RNase Rny1p cleaves tRNAs and promotes cell death during oxidative stress in Saccharomyces cerevisiae. J Cell Biol 2009; 185: 43-50; http://dx.doi.org/10.1083/jcb.200811119
23. Andersen KL, Collins K. Several RNase T2 enzymes function in induced tRNA and rRNA turnover in the ciliate Tetrahymena. Mol Biol Cell 2012; 23: 36-44; PMID: 22049026; http://dx.doi.org/10.1091/mbc. E11-08-0689
24. Mizushima N. Methods for monitoring autophagy. Int J Biochem Cell Biol 2004; 36: 2491-502; PMID: 15325587; http://dx.doi.org/10.1016/j. biocel.2004.02.005
25. Xie Z, Nair U, Klionsky DJ. Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell 2008; 19: 3290-8; PMID: 18508918; http://dx.doi. org/10.1091/mbc.E07-12-1292
26. Contento AL, Xiong Y, Bassham DC. Visualization of autophagy in Arabidopsis using the fluorescent dye monodansylcadaverine and a GFP-AtATG8e fusion protein. Plant J 2005; 42: 598-608; PMID: 15860017; http://dx.doi.org/10.1111/j.1365-313X.2005.02396.x
27. Yoshimoto K, Hanaoka H, Sato S, Kato T, Tabata S, Noda T, Ohsumi Y. Processing of ATG8s, ubiquitinlike proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell 2004; 16: 2967-83; PMID: 15494556; http://dx.doi.org/10.1105/tpc.104.025395
28. Thompson AR, Doelling JH, Suttangkakul A, Vierstra RD. Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol 2005; 138: 2097-110; PMID: 16040659; http://dx.doi.org/10.1104/ pp.105.060673
29. Drose S, Bindseil KU, Bowman EJ, Siebers A, Zeeck A, Altendorf K. Inhibitory effect of modified bafilomycins and concanamycins on P- and V-type adenosinetriphosphatases. Biochemistry 1993; 32: 3902-6; PMID: 8385991; http://dx.doi.org/10.1021/ bi00066a008
30. Dettmer J, Hong-Hermesdorf A, Stierhof YD, Schumacher K. Vacuolar H+-ATPase activity is required for Endocytic and secretory trafficking in Arabidopsis. Plant Cell 2006; 18: 715-30; PMID: 16461582; http:// dx.doi.org/10.1105/tpc.105.037978
31. Merkulova EA, 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: 715-26; PMID: 24566535; http://dx.doi.org/10.1093/pcp/pcu041
32. Yen Y, Green PJ. Identification and properties of the Major Ribonucleases of Arabidopsis thaliana. Plant Physiol 1991; 97: 1487-93; PMID: 16668575; http:// dx.doi.org/10.1104/pp.97.4.1487
33. Noda T, Kim J, Huang WP, Baba M, Tokunaga C, Ohsumi Y, Klionsky DJ. Apg9p/Cvt7p is an integral membrane protein required for transport vesicle formation in the Cvt and autophagy pathways. J Cell Biol 2000; 148: 465-80; PMID: 10662773; http://dx.doi. org/10.1083/jcb.148.3.465
34. Yamamoto H, Kakuta S, Watanabe TM, Kitamura A, Sekito T, Kondo-Kakuta C, Ichikawa R, Kinjo M, Ohsumi Y. Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J Cell Biol 2012; 198: 219-33; PMID: 22826123; http://dx.doi.org/10.1083/jcb.201202061
35. Webber JL, Tooze SA. New insights into the function of Atg9. FEBS Letts 2010; 584: 1319-26; http://dx.doi. org/10.1016/j.febslet.2010.01.020
36. Hanaoka H, Noda T, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Ohsumi Y. Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol 2002; 129: 1181-93; PMID: 12114572; http://dx. doi.org/10.1104/pp.011024
37. Le Bars R, Marion J, Le Borgne R, Satiat-Jeunemaitre B, Bianchi MW. ATG5 defines a phagophore domain connected to the endoplasmic reticulum during autophagosome formation in plants. Nat Commun 2014; 5: 4121; PMID: 24947672
38. Wang T, Lao U, Edgar BA. TOR-mediated autophagy regulates cell death in Drosophila neurodegenerative disease. J Cell Biol 2009; 186: 703-11; PMID: 19720874; http://dx.doi.org/10.1083/ jcb.200904090
39. Vazquez P, Arroba AI, Cecconi F, de la Rosa EJ, Boya P, de Pablo F. Atg5 and Ambra1 differentially modulate neurogenesis in neural stem cells. Autophagy 2012; 8: 187-99; PMID: 22240590; http://dx.doi.org/10.4161/auto.8.2.18535
40. Filimonenko M, Isakson P, Finley KD, Anderson M, Jeong H, Melia TJ, Bartlett BJ, Myers KM, Birkeland HC, Lamark T, et al. The selective macroautophagic degradation of aggregated proteins requires the PI3Pbinding protein Alfy. Mol Cell 2010; 38: 265-79; PMID: 20417604; http://dx.doi.org/10.1016/j. molcel.2010.04.007
41. Guiboileau A, Yoshimoto K, Soulay F, Bataille MP, Avice JC, Masclaux-Daubresse C. Autophagy machinery controls nitrogen remobilization at the whole-plant level under both limiting and ample nitrate conditions in Arabidopsis. New Phytol 2012; 194: 732-40; PMID: 22404536; http://dx.doi.org/10.1111/j.1469-8137.2012.04084.x
42. Patel S, Dinesh-Kumar SP. Arabidopsis ATG6 is required to limit the pathogen-associated cell death response. Autophagy 2008; 4: 20-7; PMID: 17932459; http://dx.doi.org/10.4161/auto.5056
43. De Vylder J, Vandenbussche F, Hu Y, Philips W, Van Der Straeten D. Rosette tracker: an open source image analysis tool for automatic quantification of genotype effects. Plant Physiol 2012; 160: 1149-59; PMID: 22942389; http://dx. doi.org/10.1104/pp.112.202762
44. Shin KD, Lee HN, Chung T. A revised assay for monitoring autophagic flux in Arabidopsis thaliana reveals involvement of AUTOPHAGY-RELATED9 in autophagy. Mol Cells 2014; 37: 399-405; PMID: 24805779; http://dx.doi.org/10.14348/ molcells.2014.0042
45. Suttangkakul A, Li FQ, Chung T, Vierstra RD. The ATG1/ATG13 Protein Kinase Complex Is Both a Regulator and a Target of Autophagic Recycling in Arabidopsis. Plant Cell 2011; 23: 3761-79; PMID: 21984698; http://dx.doi.org/10.1105/tpc.111.090993
46. Phillips AR, Suttangkakul A, Vierstra RD. The ATG12-conjugating enzyme ATG10 is essential for autophagic vesicle formation in Arabidopsis thaliana. Genetics 2008; 178: 1339-53; http://dx.doi.org/10.1534/genetics.107.086199
47. Chung T, Phillips AR, Vierstra RD. ATG8 lipidation and ATG8-mediated autophagy in Arabidopsis require ATG12 expressed from the differentially controlled ATG12A AND ATG12B loci. Plant J 2010; 62: 483-93; PMID: 20136727; http://dx.doi.org/10.1111/ j.1365-313X.2010.04166.x
48. Toyooka K, Okamoto T, Minamikawa T. Cotyledon cells of Vigna mungo seedlings use at least two distinct autophagic machineries for degradation of starch granules and cellular components. J Cell Biol 2001; 154: 973-82; PMID: 11524437; http://dx.doi.org/10.1083/jcb.200105096
49. Yano K, Hattori M, Moriyasu Y. A novel type of autophagy occurs together with vacuole genesis in miniprotoplasts prepared from tobacco culture cells. Autophagy 2007; 3: 215-21; PMID: 17224627; http:// dx.doi.org/10.4161/auto.3739
50. Levanony H, Rubin R, Altschuler Y, Galili G. Evidence for a Novel Route of Wheat Storage Proteins to Vacuoles. J Cell Biol 1992; 119: 1117-28; PMID: 1447291; http://dx.doi.org/10.1083/ jcb.119.5.1117
51. Slavikova S, Shy G, Yao YL, Giozman R, Levanony H, Pietrokovski S, Elazar Z, Galili G. The autophagy-associated Atg8 gene family operates both under favourable growth conditions and under starvation stresses in Arabidopsis plants. J Exp Bot 2005; 56: 2839-49; PMID: 16157655; http://dx.doi.org/10.1093/jxb/ eri276
52. Inoue Y, Suzuki T, Hattori M, Yoshimoto K, Ohsumi Y, Moriyasu Y. AtATG genes, homologs of yeast autophagy genes, are involved in constitutive autophagy in Arabidopsis root tip cells. Plant Cell Physiol 2006; 47: 1641-52; PMID: 17085765; http://dx.doi.org/10.1093/pcp/pcl031
53. Fujiwara Y, Furuta A, Kikuchi H, Aizawa S, Hatanaka Y, Konya C, Uchida K, Yoshimura A, Tamai Y, Wada K, et al. Discovery of a novel type of autophagy targeting RNA. Autophagy 2013; 9: 403-9; PMID: 23291500; http://dx.doi.org/10.4161/auto.23002
54. Ahmed SU, Rojo E, Kovaleva V, Venkataraman S, Dombrowski JE, Matsuoka K, Raikhel NV. The plant vacuolar sorting receptor AtELP is involved in transport of NH2-terminal propeptide-containing vacuolar proteins in Arabidopsis thaliana. J Cell Biol 2000; 149: 1335-44; PMID: 10871276; http://dx.doi.org/10.1083/jcb.149.7.1335
55. Leigh RA, Walker RR. Atpase and acid-phosphatase activities associated with vacuoles isolated from storage roots of red beet (Beta-Vulgaris L). Planta 1980; 150: 222-9; PMID: 24306686; http://dx.doi.org/10.1007/BF00390830
56. Lafontaine DLJ. A ‘garbage can’ for ribosomes: how eukaryotes degrade their ribosomes. Trends Biochem Sci 2010; 35: 267-77; PMID: 20097077; http://dx.doi. org/10.1016/j.tibs.2009.12.006
57. Houseley J, Tollervey D. The Many Pathways of RNA Degradation. Cell 2009; 136: 763-76; PMID: 19239894; http://dx.doi.org/10.1016/j.cell.2009.01.019
58. Hillwig MS, Rizhsky L, Wang Y, Umanskaya A, Essner JJ, MacIntosh GC. Zebrafish RNase T2 genes and the evolution of secretory ribonucleases in animals. BMC Evol Biol 2009; 9: 170; PMID: 19619322; http://dx. doi.org/10.1186/1471-2148-9-170
59. Irie M. Structure-function relationships of acid ribonucleases: Lysosomal, vacuolar, and periplasmic enzymes. Pharmacol Therapeut 1999; 81: 77-89; http://dx.doi. org/10.1016/S0163-7258(98)00035-7
60. MacIntosh GC, Hillwig MS, Meyer A, Flagel L. RNase T2 genes from rice and the evolution of secretory ribonucleases in plants; PMID: 20182746; http://dx.doi. org/10.1007/s00438-010-0524-9
61. Ambrosio L, Morriss S, Riaz A, Bailey R, Ding J, Mac-Intosh GC. Phylogenetic analyses and characterization of RNase X25 from Drosophila melanogaster suggest a conserved housekeeping role and additional functions for RNase T2 enzymes in protostomes. PLoS One 2014; 9: e105444; PMID: 25133712; http://dx.doi.org/10.1371/journal.pone.0105444
62. Igic B, Kohn JR. Evolutionary relationships among selfincompatibility RNases. Proc Natl Acad Sci USA 2001; 98: 13167-71; PMID: 11698683; http://dx.doi.org/10.1073/pnas.231386798
63. Luhtala N, Parker R. T2 Family ribonucleases: ancient enzymes with diverse roles. Trends Biochem Sci 2010; 35: 253-9; PMID: 20189811; http://dx.doi.org/10.1016/j.tibs.2010.02.002
64. Decker CJ, Parker R. P-bodies and stress granules: possible roles in the control of translation and mRNA degradation. Cold Spring Harbor Perspectives in Biology 2012; 4: a012286; PMID: 22763747; http://dx.doi.org/10.1101/cshperspect.a012286
65. Schoenberg DR, Maquat LE. Regulation of cytoplasmic mRNA decay. Nat Rev Genet 2012; 13: 246-59; PMID: 22392217; http://dx.doi.org/10.1038/ nrg3254
66. Henneke M, Diekmann S, Ohlenbusch A, Kaiser J, Engelbrecht V, Kohlschutter A, Kratzner R, Madruga-Garrido M, Mayer M, Opitz L, et al. RNASET2-deficient cystic leukoencephalopathy resembles congenital cytomegalovirus brain infection. Nat Genet 2009; 41: 773-5; PMID: 19525954; http://dx.doi.org/10.1038/ng.398
67. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 2005; 139: 5-17; PMID: 16166256; http://dx.doi.org/10.1104/ pp.105.063743
68. Xu J, Chua NH. Processing bodies and plant development. Curr Opin Plant Biol 2011; 14: 88-93; PMID: 21075046; http://dx.doi.org/10.1016/j. pbi.2010.10.003
69. Eulalio A, Behm-Ansmant I, Izaurralde E. P bodies: at the crossroads of post-transcriptional pathways. Nat Rev Mol Cell Biol 2007; 8: 9-22; PMID: 17183357; http://dx.doi.org/10.1038/nrm2080
70. Buchan JR, Kolaitis RM, Taylor JP, Parker R. Eukaryotic stress granules are cleared by autophagy and Cdc48/VCP function. Cell 2013; 153: 1461-74; PMID: 23791177; http://dx.doi.org/10.1016/j. cell.2013.05.037
71. Noda NN, Inagaki F. Mechanisms of autophagy. Annu Rev Biophys 2015; 44: 101-22; PMID: 25747593
72. Mijaljica D, Prescott M, Devenish RJ. Microautophagy in mammalian cells: revisiting a 40-year-old conundrum. Autophagy 2011; 7: 673-82; PMID: 21646866; http://dx.doi.org/10.4161/auto.7.7.14733
73. Inada N, Sakai A, Kuroiwa H, Kuroiwa T. Threedimensional analysis of the senescence program in rice (Oryza sativa L.) coleoptiles. Investigations of tissues and cells by fluorescence microscopy. Planta 1998; 205: 153-64; PMID: 9637068; http://dx.doi.org/10.1007/s004250050307
74. Smith MT, Saks Y, Vanstaden J. Ultrastructural-Changes in the Petals of Senescing Flowers of Dianthus-Caryophyllus L. Ann Bot 1992; 69: 277-85
75. Thompson JE, Froese CD, Hong Y, Hudak KA, Smith MD. Membrane deterioration during senescence. Can J Bot 1997; 75: 867-79; http://dx.doi.org/10.1139/ b97-096
76. Gupta HS. Vacuolar autophagy - apparent dilution and elimination of cytoplasmic organelles in acridine orange-treated plant-cells. Caryologia 1988; 41: 347-59; http://dx.doi.org/10.1080/00087114.1988.10797875
77. Chen MH, Liu LF, Chen YR, Wu HK, Yu SM. Expression of alpha-amylases, carbohydrate-metabolism, and autophagy in cultured rice cells is coordinately regulated by sugar nutrient. Plant J 1994; 6: 625-36; PMID: 8000424; http://dx.doi.org/10.1046/j.1365-313X.1994.6050625.x
78. Beers EP. Programmed cell death during plant growth and development. Cell Death Differ 1997; 4: 649-61; PMID: 16465277; http://dx.doi.org/10.1038/sj. cdd.4400297
79. Kwon SI, Cho HJ, Jung JH, Yoshimoto K, Shirasu K, Park OK. The Rab GTPase RabG3b functions in autophagy and contributes to tracheary element differentiation in Arabidopsis. Plant J 2010; 64: 151-64; PMID: 20659276
80. Liu Y, Schiff M, Czymmek K, Talloczy Z, Levine B, Dinesh-Kumar SP. Autophagy regulates programmed cell death during the plant innate immune response. Cell 2005; 121: 567-77; PMID: 15907470; http://dx. doi.org/10.1016/j.cell.2005.03.007
81. Moriyasu Y, Ohsumi Y. Autophagy in tobacco suspension- cultured cells in response to sucrose starvation. Plant Physiol 1996; 111: 1233-41; PMID: 12226358
82. Fujiwara Y, Kikuchi H, Aizawa S, Furuta A, Hatanaka Y, Konya C, Uchida K, Wada K, Kabuta T. Direct uptake and degradation of DNA by lysosomes. Autophagy 2013; 9: 1167-71; PMID: 23839276; http:// dx.doi.org/10.4161/auto.24880
83. Tanaka Y, Guhde G, Suter A, Eskelinen EL, Hartmann D, Lullmann-Rauch R, Janssen PML, Blanz J, von Figura K, Saftig P. Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature 2000; 406: 902-6; PMID: 10972293; http://dx. doi.org/10.1038/35022595
84. Liu YM, Burgos JS, Deng Y, Srivastava R, Howell SH, Bassham DC. Degradation of the endoplasmic reticulum by autophagy during endoplasmic reticulum stress in arabidopsis. Plant Cell 2012; 24: 4635-51; PMID: 23175745; http://dx.doi.org/10.1105/ tpc.112.101535
85. Liu YM, Xiong Y, Bassham DC. Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 2009; 5: 954-63; PMID: 19587533; http:// dx.doi.org/10.4161/auto.5.7.9290
86. Doelling JH, Walker JM, Friedman EM, Thompson AR, Vierstra RD. The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J Biol Chem 2002; 277: 33105-14; PMID: 12070171; http://dx.doi.org/10.1074/jbc.M204630200
87. Weigel D, Glazebrook J. Arabidopsis: A laboratory manual. Cold spring harbor. New York: Cold Spring Harbor Laboratory Press; 2002.
88. Xiong Y, Contento AL, Nguyen PQ, Bassham DC. Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol 2007; 143: 291-9; PMID: 17098847; http://dx.doi.org/10.1104/pp.106.092106
89. Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 1998; 16: 735-43; PMID: 10069079; http://dx.doi.org/10.1046/j.1365-313x.1998.00343.x
90. Sheen J. A transient expression assay using Arabidopsis meshophyll protoplasts. http://geneticsmghharvardedu/ sheenweb/2002.
91. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods 2012; 9: 676-82; PMID: 22743772; http://dx.doi.org/10.1038/ nmeth.2019
92. Robert S, Zouhar J, Carter C, Raikhel N. Isolation of intact vacuoles from Arabidopsis rosette leaf-derived protoplasts. Nat Protoc 2007; 2: 259-62; PMID: 17406583; http://dx.doi.org/10.1038/ nprot.2007.26
93. Ahmed SU, Rojo E, Kovaleva V, Venkataraman S, Dombrowski JE, Matsuoka K, Raikhel NV. The plant vacuolar sorting receptor AtELP is involved in transport of NH(2)-terminal propeptide-containing vacuolar proteins in Arabidopsis thaliana. J Cell Biol 2000; 149: 1335-44; PMID: 10871276; http://dx.doi.org/10.1083/jcb.149.7.1335
94. Pfaffl MW. Quantification strategies in real-time PCR. A-Z of quantitative PCR. Ed. SA Bustin. La Jolla, CA, USA: International University Line; 2004: 87-112.
95. Reilly TJ, Baron GS, Nano FE, Kuhlenschmidt MS. Characterization and sequencing of a respiratory burstinhibiting acid phosphatase from Francisella tularensis. J Biol Chem 1996; 271: 10973-83; PMID: 8631917; http://dx.doi.org/10.1074/jbc.271.18.10973