Autophagy, plant senescence, and nutrient recycling

Journal of Experimental Botany

Volumn 65, Issue 14, 2014, Pages 3799-3811

  Avila Ospina, Liliana ^a   Moison, Michael ^a   Yoshimoto, Kohki ^a   Masclaux Daubresse, Céline ^a  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

Author keywords

Nitrogen remobilization; plant cell death; proteolysis; Rubisco containing bodies; vesicular trafficking

Indexed keywords

NITROGEN;

AUTOPHAGY; CHLOROPLAST; FLOWER; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT; PLANT LEAF;

AUTOPHAGY; CHLOROPLASTS; FLOWERS; NITROGEN; PLANT LEAVES; PLANTS;

EID: 84904988777     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru039     Document Type: Review

References (91)

1. Araujo WL, Ishizaki K, Nunes-Nesi A, et al. 2010. Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria. The Plant Cell 22, 1549-1563.
2. Araujo WL, Tohge T, Ishizaki K, Leaver CJ, Fernie AR. 2011. Protein degradation: An alternative respiratory substrate for stressed plants. Trends in Plant Science 16, 489-498.
3. Bassham DC, Laporte M, Marty F, Moriyasu Y, Ohsumi Y, Olsen LJ, Yoshimoto K. 2006. Autophagy in development and stress responses of plants. Autophagy 2, 2-11.
4. Breeze E, Harrison E, McHattie S, et al. 2011. High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23, 873-894.
5. Chapin LJ, Jones ML. 2009. Ethylene regulates phosphorus remobilization and expression of a phosphate transporter (PhPT1) during petunia corolla senescence. Journal of Experimental Botany 60, 2179-2190.
6. Chiba A, Ishida H, Nishizawa NK, Makino A, Mae T. 2003. Exclusion of ribulose-1,5-bisphosphate carboxylase/oxygenase from chloroplasts by specific bodies in naturally senescing leaves of wheat. Plant and Cell Physiology 44, 914-921.
7. Chung T, Suttangkakul A, Vierstra RD. 2009. The ATG autophagic conjugation system in maize: ATG transcripts and abundance of the ATG8-lipid adduct are regulated by development and nutrient availability. Plant Physiology 149, 220-234.
8. Contento AL, Xiong Y, Bassham DC. 2005. Visualization of autophagy in Arabidopsis using the fluorescent dye monodansylcadaverine and a GFP-AtATG8e fusion protein. The Plant Journal 42, 598-608.
9. De Duve C, Wattiaux R. 1966. Functions of lysosomes. Annual Review of Physiology 28, 435-492.
10. Desclos M, Etienne P, Coquet L, Jouenne T, Bonnefoy J, Segura R, Reze S, Ourry A, Avice JC. 2009. A combined 15N tracing/proteomics study in Brassica napus reveals the chronology of proteomics events associated with N remobilisation during leaf senescence induced by nitrate limitation or starvation. Proteomics 9, 3580-3608.
11. Diaz C, Lemaitre T, Christ A, Azzopardi M, Kato Y, Sato F, Morot-Gaudry JF, Le Dily F, Masclaux-Daubresse C. 2008. Nitrogen recycling and remobilization are differentially controlled by leaf senescence and development stage in Arabidopsis under low nitrogen nutrition. Plant Physiology 147, 1437-1449.
12. Diaz C, Purdy S, Christ A, Morot-Gaudry JF, Wingler A, Masclaux-Daubresse CL. 2005. Characterization of markers to determine the extent and variability of leaf senescence in Arabidopsis. A metabolic profiling approach. Plant Physiology 138, 898-908.
13. Doelling JH, Walker JM, Friedman EM, Thompson AR, Vierstra RD. 2002. The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. Journal of Biological Chemistry 277, 33105-33114.
14. Feller U, Song T, Hageman R. 1977. Leaf proteolytic activities and senescence during grain development of field-grown corn (Zea mays L.). Plant Physiology 59, 290-294.
15. Feller U, Anders I, Mae T. 2008. Rubiscolytics: Fate of Rubisco after its enzymatic function in a cell is terminated. Journal of Experimental Botany 59, 1615-1624.
16. Ferguson C, Simon E. 1973. membrane lipids in senescing green tissue. Journal of Experimental Botany 24, 307-316.
17. Fischer AM. 2012. The complex regulation of senescence. Critical Reviews in Plant Sciences 31, 124-147.
18. García-Ferris C, Moreno J. 1993. Redox regulation of enzymatic activity and proteolytic and susceptibility of ribulose-1,5-bisphosphate carboxylase/oxygenase from Euglena gracilis. Photosynthesis Research 35, 55-66.
19. García-Ferris C, Moreno J. 1994. Oxidative modification and breakdown of ribulose-1,5-bisphosphate carboxylase/oxygenase induced in Euglena gracilis by nitrogen starvation. Planta 193, 208-215.
20. Ghiglione HO, Gonzalez FG, Serrago R, Maldonado SB, Chilcott C, Cura JA, Miralles DJ, Zhu T, Casal JJ. 2008. Autophagy regulated by day length determines the number of fertile florets in wheat. The Plant Journal 55, 1010-1024.
21. Gregersen P, Culetic A, Boschian L, Krupinska K. 2013. Plant senescence and crop productivity. Plant Molecular Biology 82, 603-622.
22. Guiboileau A, Avila-Ospina L, Yoshimoto K, Soulay F, Azzopardi M, Marmagne A, Lothier J, Masclaux-Daubresse C. 2013. Physiological and metabolic consequences of autophagy defisciency for the management of nitrogen and protein resources in Arabidopsis leaves depending on nitrate availability. New Phytologist 199, 683-694.
23. Guiboileau A, Sormani R, Meyer C, Masclaux-Daubresse C. 2010. Senescence and death of plant organs: Nutrient recycling and developmental regulation. Comptes Rendus Biologies 333, 382-391.
24. Guiboileau A, Yoshimoto K, Soulay F, Bataille M-P, Avice J-C, Masclaux-Daubresse C. 2012. Autophagy machinery controls nitrogen remobilization at the whole-plant level under both limiting and ample nitrate conditions in Arabidopsis. New Phytologist 194, 732-740.
25. Hanaoka H, Noda T, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Ohsumi Y. 2002. Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiology 129, 1181-1193.
26. Hew CS, Tan SC, Chin TY, Ong TK. 1989. Influence of ethylene on enzyme activities and mobilization of materials in pollinated Arachnis orchid flowers. Journal of Plant Growth Regulation 8, 121-130.
27. Ishida H, Yoshimoto K. 2008. Chloroplasts are partially mobilized to the vacuole by autophagy. Autophagy 4, 961-962.
28. Ishida H, Yoshimoto K, Izumi M, Reisen D, Yano Y, Makino A, Ohsumi Y, Hanson MR, Mae T. 2008. Mobilization of rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process. Plant Physiology 148, 142-155.
29. Jain V, Kaiser W, Huber SC. 2008. Cytokinin inhibits the proteasomemediated degradation of carbonylated proteins in Arabidopsis leaves. Plant and Cell Physiology 49, 843-852.
30. Jones M. 2013. Mineral nutrient remobilization during corolla senescence in ethylene-sensitive and-insensitive flowers. AoB Plants. DOI: 010.1093/aobpla/plt023
31. Kabbage M, Williams B, Dickman MB. 2013. Cell death control: The interplay of apoptosis and autophagy in the pathogenicity of sclerotinia sclerotiorum. PloS Pathogens 9, e1003287. doi:1003210.1001371/journal.ppat. 1003287.
32. Kaltaler REL, Steponkus PL. 1976. Factors affecting respiration in cut roses. Journal of the American Society for Horticultural Science 101, 353-354.
33. Kato Y, Murakami S, Yamamoto Y, Chatani H, Kondo Y, Nakano T, Yokota A, Sato F. 2004. The DNA-binding protease, CND41, and the degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase in senescent leaves of tobacco. Planta 220, 97-104.
34. Kaup MT, Froese CD, Thompson JE. 2002. A role for diacylglycerol acyltransferase during leaf senescence. Plant Physiology 129, 1616-1626.
35. Korolchuk VI, Menzies FM, Rubinsztein DC. 2010. Mechanisms of cross-talk between the ubiquitin-proteasome and autophagy-lysosome systems. FEBS Letters 584, 1393-1398.
36. Koyama T, Nii H, Mitsuda N, Ohta M, Kitajima S, Ohme-Takagi M, Sato F. 2013. A regulatory cascade involving class II ETHYLENE RESPONSE factor transcriptional repressors operates in the progression of leaf senescence. Plant Physiology 162, 991-1005.
37. Kuzuoglu-Ozturk D, Yalcinkaya OC, Akpinar BA, Mitou G, Korkmaz G, Gozuacik D, Budak H. 2012. Autophagy-related gene, TdAtg8, in wild emmer wheat plays a role in drought and osmotic stress response. Planta 236, 1081-1092.
38. Lee TA, Vande Wetering SW, Brusslan JA. 2013. Stromal protein degradation is incomplete in Arabidopsis thaliana autophagy mutants undergoing natural senescence. BMC Research Notes 6, 17-17.
39. Lemaitre T, Gaufichon L, Boutet-Mercey S, Christ A, Masclaux-Daubresse C. 2008. Enzymatic and metabolic diagnostic of nitrogen deficiency in Arabidopsis thaliana Wassileskija accession. Plant and Cell Physiology 49, 1056-1065.
40. Mae T, Makino A, Ohira K. 1983. Changes in the amounts of ribulose biphosphate carboxylase synthesized and degraded during the life span of rice leaf (Oryza sativa L.). Plant and Cell Physiology 24, 1079-1086.
41. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. 2007. Self-eating and self-killing: Crosstalk between autophagy and apoptosis. Nature Reviews Molecular Cell Biology 8, 741-752.
42. Martinez DE, Bartoli CG, Grbic V, Guiamet JJ. 2007. Vacuolar cysteine proteases of wheat (Triticum aestivum L.) are common to leaf senescence induced by different factors. Journal of Experimental Botany 58, 1099-1107.
43. Martinez DE, Costa ML, Gomez FM, Otegui MS, Guiamet JJ. 2008a. 'Senescence-associated vacuoles' are involved in the degradation of chloroplast proteins in tobacco leaves. The Plant Journal 56, 196-206.
44. Martinez DE, Costa ML, Guiamet JJ. 2008b. Senescence-associated degradation of chloroplast proteins inside and outside the organelle. Plant Biology (Stuttgart) 10, Supplement 1, 15-22.
45. Masclaux C, Quillere I, Gallais A, Hirel B. 2001. The challenge of remobilisation in plant nitrogen economy. A survey of physio-agronomic and molecular approaches. Annals of Applied Biology 138, 69-81.
46. Masclaux C, Valadier MH, Brugiere N, Morot-Gaudry JF, Hirel B. 2000. Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. Planta 211, 510-518.
47. Masclaux-Daubresse C, Chardon F. 2011. Exploring nitrogen remobilization for seed filling using natural variation in Arabidopsis thaliana. Journal of Experimental Botany 62, 2131-2142.
48. Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gaufichon L, Suzuki A. 2010. Nitrogen uptake, assimilation, and remobilization in plants: Challenges for sustainable and productive agriculture. Annals of Botany 105, 1141-1157.
49. Masclaux-Daubresse C, Reisdorf-Cren M, Pageau K, Lelandais M, Grandjean O, Kronenberger J, Valadier MH, Feraud M, Jouglet T, Suzuki A. 2006. Glutamine synthetase-glutamate synthase pathway and glutamate dehydrogenase play distinct roles in the sink-source nitrogen cycle in tobacco. Plant Physiology 140, 444-456.
50. Matile P. 1992. Chloroplast senescence. In: Baker NR, Thomas H, eds. Crop photosynthesis: Spatial and temporal determinants. Amsterdam: Elsevier, 413-440.
51. Matile P, Winkenbach F. 1971. Function of lysosomes and lysosomal enzymes in the senescing corolla of the morning glory (Ipomoea purpurea). Journal of Experimental Botany 22, 759-771.
52. Mizushima N, Yamamoto A, Yoshimori T, Ohsumi Y. 2002. Mice with a fluorescent marker for autophagy. Molecular Biology of the Cell 13, 750.
53. Moriyasu Y, Ohsumi Y. 1996. Autophagy in tobacco suspensioncultured cells in response to sucrose starvation. Plant Physiology 111, 1233-1241.
54. Otegui MS, Noh YS, Martinez DE, Vila Petroff MG, Andrew Staehelin L, Amasino RM, Guiamet JJ. 2005. Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. The Plant Journal 41, 831-844.
55. Partier B. 1988. Gerontoplasts: The yellow end in the ontogenesis of chloroplasts. Endocytobiosis and Cell Research 5, 163-190.
56. Peoples M, Dalling M. 1988. The interplay between proteolysis and amino acid metabolism during senescence and nitrogen reallocation. In: Noodén L, Leopold A, eds. Senescence and aging in plants. San Diego: Academic Press, 181-217.
57. Peterson LW, Huffaker RC. 1975. Loss of ribulose 1,5-diphosphate carboxylase in proteolytic activity during senescence of detached primary barley leaves. Plant Physiology 55, 1009-1015.
58. Phillips AR, Suttangkakul A, Vierstra RD. 2008. The ATG12-conjugating enzyme ATG10 is essential for autophagic vesicle formation in Arabidopsis thaliana. Genetics 178, 1339-1353.
59. Polge C, Jaquinod M, Holzer F, Bourguignon J, Walling L, Brouquisse R. 2009. Evidence for the existence in Arabidopsis thaliana of the proteasome proteolytic pathway ACTIVATION IN RESPONSE TO CADMIUM. Journal of Biological Chemistry 284, 35412-35424.
60. Prins A, van Heerden PDR, Olmos E, Kunert KJ, Foyer CH. 2008. Cysteine proteinases regulate chloroplast protein content and composition in tobacco leaves: A model for dynamic interactions with ribulose-1,5-biphosphate carboxylase/oxygenase (Rubisco) vesicular bodies. Journal of Experimental Botany 59, 1935-1950.
61. Raab S, Drechsel G, Zarepour M, Hartung W, Koshiba T, Bittner F, Hoth S. 2009. Identification of a novel E3 ubiquitin ligase that is required for suppression of premature senescence in Arabidopsis. The Plant Journal 59, 39-51.
62. Roberts IN, Caputo C, Criado MV, Funk C. 2012. Senescenceassociated proteases in plants. Physiologia Plantarum 145, 130-139.
63. Sakamoto W. 2006. Protein degradation machineries in plastids. Annual Review of Plant Biology 57, 599-621.
64. Schippers JHM, Nunes-Nesi A, Apetrei R, Hille J, Fernie AR, Dijkwel PP. 2008. The Arabidopsis onset of leaf death5 mutation of quinolinate synthase affects nicotinamide adenine dinucleotide biosynthesis and causes early ageing. The Plant Cell 20, 2909-2925.
65. Svenning S, Lamark T, Krause K, Johansen T. 2011. Plant NBR1 is a selective autophagy substrate and a functional hybrid of the mammalian autophagic adapters NBR1 and p62/SQSTM1. Autophagy 7, 993-1010.
66. Shibuya K, Niki T, Ichimura K. 2013. Pollination induces autophagy in petunia petals via ethylene. Journal of Experimental Botany 64, 1111-1120.
67. Shibuya K, Shimizu K, Yamada T, Ichimura K. 2011. Expression of autophagy-associated ATG8 genes during petal senescence in Japanese morning glory. Journal of the Japanese Society for Horticultural Science 80, 89-95.
68. Shin J-H, Yoshimoto K, Ohsumi Y, Jeon J-s, An G. 2009. OsATG10b, an autophagosome component, is needed for cell survival against oxidative stresses in rice. Molecules and Cells 27, 67-74.
69. Sitte P. 1977. Chromoplasten-bunte Objekte der modernen Zellbiologie. Biologie in unserer Zeit 7, 65-74.
70. Skubatz H, Meeuse BJD, Bendich AJ. 1989. Oxidation of proline and glutamate by mitochondria of the inflorescence of voodoo lily (Sauromatum guttatum). Plant Physiology 91, 530-535.
71. Su W, Ma H, Liu C, Wu J, Yang J. 2006. Identification and characterization of two rice autophagy associated genes, OsAtg8 and OsAtg4. Molecular Biology Reports 33, 273-278.
72. Tegeder M, Rentsch D. 2010. Uptake and partitioning of amino acids and peptides. Molecular Plant 3, 997-1011.
73. Thomas H. 2013. Senescence, ageing and death of the whole plant. New Phytologist 197, 696-711.
74. Thompson AR, Doelling JH, Suttangkakul A, Vierstra RD. 2005. Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiology 138, 2097-2110.
75. van der Graaff E, Schwacke R, Schneider A, Desimone M, Flugge UI, Kunze R. 2006. Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiology 141, 776-792.
76. Verlinden S. 2003. Changes in mineral nutrient concentrations in petunia corollas during development and senescence. HortScience 38, 71-74.
77. Wagner R, Aigner H, Pružinská A, Jänkänpä ä H, Jansson S, Funk C. 2011. Fitness analyses of Arabidopsis thaliana mutants depleted of FtsH metalloproteases and characterization of three FtsH6 deletion mutants exposed to high light stress, senescence and chilling. New Phytologist 191, 449-458.
78. Watanabe M, Balazadeh S, Tohge T, Erban A, Giavalisco P, Kopka J, Mueller-Roeber B, Fernie A, Hoefgen R. 2013. Comprehensive dissection of spatio-temporal metabolic shifts in primary, secondary and lipid metabolism during developmental senescence in arabidopsis. Plant Physiology 162, 1290-1310.
79. Wittenbach VA. 1978. Breakdown of ribulose biphosphate carboxylase and change in proteolytic activity during dark-induced senescence of wheat seedlings. Plant Physiology 62, 604-608.
80. Wittenbach VA, Lin W, Hebert RR. 1982. Vacuolar localization of proteases and degradation of chloroplasts in mesophyll protoplasts from senescing primary wheat leaves. Plant Physiology 69, 98-102.
81. Wulster GJ, Sacalis JN, Janes HW. 1984. Development of cyanideresistant respiration in carnation flower petals. Journal of the American Society for Horticultural Science 109, 202-206.
82. Xia T, Xiao D, Liu D, Chai W, Gong Q, Wang NN. 2012. Heterologous expression of ATG8c from soybean confers tolerance to nitrogen deficiency and increases yield in Arabidopsis. PLoS ONE 7, e37217.
83. Xiong Y, Contento AL, Bassham DC. 2005. AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana. The Plant Journal 42, 535-546.
84. Xiong Y, Contento AL, Bassham DC. 2007a. Disruption of autophagy results in constitutive oxidative stress in Arabidopsis. Autophagy 3, 257-258.
85. Xiong Y, Contento AL, Nguyen PQ, Bassham DC. 2007b. Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiology 143, 291-299.
86. Yamada T, Ichimura K, Kanekatsu M, van Doorn WG. 2009. Homologs of genes associated with programmed cell death in animal cells are differentially expressed during senescence of Ipomoea nil petals. Plant and Cell Physiology 50, 610-625.
87. Yoshimoto K, Hanaoka H, Sato S, Tomohiko K, Tabata S, Noda T, Ohsumi Y. 2004. Analysis of Arabidopsis ATG8 family proteins involved in autophagy, a vacuolar degradation process. Plant and Cell Physiology 45, S110-S110.
88. Yoshimoto K, Jikumaru Y, Kamiya Y, Kusano M, Consonni C, Panstruga R, Ohsumi Y. Shirasu K. 2009. Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. The Plant Cell 21, 2914-2927.
89. Zelisko A, Garcia-Lorenzo M, Jackowski G, Jansson S, Funk C. 2005. AtFtsH6 is involved in the degradation of the light-harvesting complex II during high-light acclimation and senescence. Proceedings of the National Academy of Sciences, USA 102, 13699-13704.
90. Zelisko A, Jackowski G. 2004. Senescence-dependent degradation of Lhcb3 is mediated by a thylakoid membrane-bound protease. Journal of Plant Physiology 161, 1157-1170.
91. Zientara-Rytter K, Lukomska J, Moniuszko G, Gwozdecki R, Surowiecki P, Lewandowska M, Liszewska F, Wawrzynska A, Sirko A. 2011. Identification and functional analysis of Joka2, a tobacco member of the family of selective autophagy cargo receptors. Autophagy 7, 1145-1158.