Physiological and metabolic consequences of autophagy deficiency for the management of nitrogen and protein resources in Arabidopsis leaves depending on nitrate availability

New Phytologist

Volumn 199, Issue 3, 2013, Pages 683-694

  Guiboileau, Anne ^a   Avila Ospina, Liliana ^a   Yoshimoto, Kohki ^a   Soulay, Fabienne ^a   Azzopardi, Marianne ^a   Marmagne, Anne ^a   Lothier, Jérémy ^a   Masclaux Daubresse, Céline ^a  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

Author keywords

Aminopeptidase; Carboxypeptidase; Leaf senescence; Nitrate availability; Nitrogen remobilization; Selective autophagy

Indexed keywords

AMINOPEPTIDASE; ARABIDOPSIS PROTEIN; CARBON; CARBOXYPEPTIDASE; GLUTAMATE AMMONIA LIGASE; NITRATE; NITROGEN; PEPTIDE HYDROLASE;

AMINO ACID; AMMONIUM; CARBON; CHLOROPLAST; CONCENTRATION (COMPOSITION); ENZYME ACTIVITY; HERB; MANAGEMENT PRACTICE; METABOLISM; NITROGEN; PHYSIOLOGY; PROTEIN; SENESCENCE;

ARABIDOPSIS; ARTICLE; AUTOPHAGY; BIOMASS; CARBOHYDRATE METABOLISM; CYTOLOGY; DRUG EFFECT; ENZYMOLOGY; GENETICS; LEAF SENESCENCE; METABOLISM; MUTATION; NITRATE AVAILABILITY; NITROGEN REMOBILIZATION; PHYSIOLOGY; PLANT LEAF; PROTEIN DEGRADATION; RNA INTERFERENCE; SELECTIVE AUTOPHAGY; WESTERN BLOTTING;

AMINOPEPTIDASE; CARBOXYPEPTIDASE; LEAF SENESCENCE; NITRATE AVAILABILITY; NITROGEN REMOBILIZATION; SELECTIVE AUTOPHAGY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; AUTOPHAGY; BIOMASS; BLOTTING, WESTERN; CARBOHYDRATE METABOLISM; CARBON; GLUTAMATE-AMMONIA LIGASE; MUTATION; NITRATES; NITROGEN; PEPTIDE HYDROLASES; PLANT LEAVES; PROTEOLYSIS; RNA INTERFERENCE;

ARABIDOPSIS;

EID: 84880259390     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12307     Document Type: Article

References (44)

1. 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.
2. Breeze E, Harrison E, McHattie S, Hughes L, Hickman R, Hill C, Kiddle S, Kim Y-S, Penfold CA, Jenkins D 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.
3. Brouquisse R, Masclaux C, Feller U, Raymond P. 2001. Protein hydrolysis and nitrogen remobilisation in plant life and senescence. In: Lea P, Morot-Gaudry JF, eds. Plant nitrogen. Berlin, Germany: Springer-Verlag, 275-293.
4. 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.
5. Cren M, Hirel B. 1999. Glutamine synthetase in higher plants: regulation of gene and protein expression from the organ to the cell. Plant Cell Physiology 40: 1187-1193.
6. Desclos M, Dubousset L, Etienne P, Le Caherec F, Satoh H, Bonnefoy J, Ourry A, Avice JC. 2008. A proteomic profiling approach to reveal a novel role of Brassica napus drought 22 kD/water-soluble chlorophyll-binding protein in young leaves during nitrogen remobilization induced by stressful conditions. Plant Physiology 147: 1830-1844.
7. 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.
8. 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.
9. 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.
10. Etienne P, Desclos M, Le Gou L, Gombert J, Bonnefoy J, Maurel K, Le Dily F, Ourry A, Avice J-C. 2007. N-protein mobilisation associated with the leaf senescence process in oilseed rape is concomitant with the disappearance of trypsin inhibitor activity. Functional Plant Biology 34: 895-906.
11. 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.
12. Feller U, Fischer A. 1994. Nitrogen-metabolism in senescing leaves. Critical Reviews in Plant Sciences 13: 241-273.
13. 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.
14. 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.
15. 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.
16. 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.
17. Inoue Y, Klionsky DJ. 2010. Regulation of macroautophagy in Saccharomyces cerevisiae. Seminars in Cell & Developmental Biology 21: 664-670.
18. 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.
19. Izumi M, Wada S, Makino A, 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 Physiology 154: 1196-1209.
20. 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.
21. Li F, Vierstra RD. 2012. Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends in Plant Science 17: 526-537.
22. Liu Y, Bassham DC. 2012. Autophagy: pathways for self-eating in plant cells. Annual review of plant biology 63: 215-237.
23. Liu Y, Xiong Y, Bassham DC. 2009. Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 5: 954-963.
24. Lothier J, Gaufichon L, Sormani R, Lemaitre T, Azzopardi M, Morin H, Chardon F, Reisdorf-Cren M, Avice JC, Masclaux-Daubresse C. 2011. The cytosolic glutamine synthetase GLN1;2 plays a role in the control of plant growth and ammonium homeostasis in Arabidopsis rosettes when nitrate supply is not limiting. Journal of Experimental Botany 62: 1375-1390.
25. MacIntosh GC, Bassham DC. 2011. The connection between ribophagy, autophagy and ribosomal RNA decay. Autophagy 7: 662-663.
26. Martinez DE, Costa ML, Guiamet JJ. 2008. Senescence-associated degradation of chloroplast proteins inside and outside the organelle. Plant Biology (Stuttgart) 10(Suppl 1): 15-22.
27. 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.
28. 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.
29. 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.
30. Masclaux-Daubresse C, Valadier MH, Carrayol E, Reisdorf-Cren M, Hirel B. 2002. Diurnal changes in the expression of glutamate dehydrogenase and nitrate reductase are involved in the C/N balance of tobacco source leaves. Plant, Cell & Environment 25: 1451-1462.
31. Nakano R, Ishida H, Makino A, Mae T. 2006. In vivo fragmentation of the large subunit of ribulose-1, 5-bisphosphate carboxylase by reactive oxygen species in an intact leaf of cucumber under chilling-light conditions. Plant and Cell Physiology 47: 270-276.
32. Noda NN, Ohsumi Y, Inagaki F. 2010. Atg8-family interacting motif crucial for selective autophagy. FEBS Letters 584: 1379-1385.
33. Ono Y, Wada S, Izumi M, Makino A, Ishida H. 2013. Evidence for contribution of autophagy to Rubisco degradation during leaf senescence in Arabidopsis thaliana. Plant, Cell & Environment 36: 1147-1159.
34. Palatnik JF, Carrillo N, Valle EM. 1999. The role of photosynthetic electron transport in the oxidative degradation of chloroplastic glutamine synthetase. Plant Physiology 121: 471-478.
35. 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, CA, USA: Academic Press, 181-217.
36. 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-bisphosphate carboxylase/oxygenase (Rubisco) vesicular bodies. Journal of Experimental Botany 59: 1935-1950.
37. Roberts IN, Caputo C, Criado MV, Funk C. 2012. Senescence-associated proteases in plants. Physiologia Plantarum 145: 130-139.
38. Rosen H. 1957. A modified ninhydrin colorimetric analysis for amino acids. Archives of Biochemistry and Biophysics 67: 10-15.
39. Tegeder M, Rentsch D. 2010. Uptake and partitioning of amino acids and peptides. Molecular Plant 3: 997-1011.
40. 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.
41. Wada S, Ishida H, Izumi M, Yoshimoto K, Ohsumi Y, Mae T, Makino A. 2009. Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiology 149: 885-893.
42. Xiong Y, Contento AL, Bassham DC. 2005. AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana. Plant Journal 42: 535-546.
43. Yoshimoto K. 2012. Beginning to understand autophagy, an intracellular self-degradation system in plants. Plant and Cell Physiology 53: 1355-1365.
44. 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. Plant Cell 21: 2914-2927.