Dissecting the metabolic role of mitochondria during developmental leaf senescence

Plant Physiology

Volumn 172, Issue 4, 2016, Pages 2132-2153

  Chrobok, Daria ^a   Law, Simon R ^a   Brouwer, Bastiaan ^a,f   Lindén, Pernilla ^b   Ziolkowska, Agnieszka ^a   Liebsch, Daniela ^a   Narsai, Reena ^c   Szal, Bozena ^d   Moritz, Thomas ^b   Rouhier, Nicolas ^e   Whelan, James ^c   Gardeström, Per ^a   Keech, Olivier ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^c LA TROBE UNIVERSITY   (Australia)

^d UNIVERSITY OF WARSAW   (Poland)

^e UNIVERSITÉ DE LORRAINE   (France)

^f WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL PROTEIN; TRANSCRIPTOME;

ARABIDOPSIS; CELL RESPIRATION; ENERGY METABOLISM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METABOLOMICS; MITOCHONDRIAL GENE; MITOCHONDRION; PLANT GENE; PLANT LEAF; ULTRASTRUCTURE;

ARABIDOPSIS; CELL RESPIRATION; ENERGY METABOLISM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, MITOCHONDRIAL; GENES, PLANT; METABOLIC NETWORKS AND PATHWAYS; METABOLOMICS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PLANT LEAVES; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 84998775118     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.01463     Document Type: Article

References (100)

1. Araujo WL, Ishizaki K, Nunes-Nesi A, Larson TR, Tohge T, Krahnert I, Witt S, Obata T, Schauer N, Graham IA, 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. Plant Cell 22: 1549-1563
2. Aubert S, Bligny R, Douce R, Gout E, Ratcliffe RG, Roberts JKM (2001) Contribution of glutamate dehydrogenase to mitochondrial glutamate metabolism studied by C-13 and P-31 nuclear magnetic resonance. J Exp Bot 52: 37-45
3. Avila-Ospina L, Marmagne A, Talbotec J, Krupinska K, Masclaux-Daubresse C (2015) The identification of new cytosolic glutamine synthetase and asparagine synthetase genes in barley (Hordeum vulgare L.), and their expression during leaf senescence. J Exp Bot 66: 2013-2026
4. Balk J, Schaedler TA (2014) Iron cofactor assembly in plants. Annu Rev Plant Biol 65: 125-153
5. Barreto P, Okura VK, Neshich IA, Maia Ide G, Arruda P (2014) Overexpression of UCP1 in tobacco induces mitochondrial biogenesis and amplifies a broad stress response. BMC Plant Biol 14: 144
6. Besagni C, Kessler F (2013) A mechanism implicating plastoglobules in thylakoid disassembly during senescence and nitrogen starvation. Planta 237: 463-470
7. Bhalerao R, Keskitalo J, Sterky F, Erlandsson R, Bjorkbacka H, Birve SJ, Karlsson J, Gardestrom P, Gustafsson P, Lundeberg J, et al (2003) Gene expression in autumn leaves. Plant Physiol 131: 430-442
8. Binder S (2010) Branched-chain amino acid metabolism in Arabidopsis thaliana. The Arabidopsis Book 8: e0137, doi/10.1199/tab.0137
9. Bohner A, Kojima S, Hajirezaei M, Melzer M, von Wiren N (2015) Urea retranslocation from senescing Arabidopsis leaves is promoted by DUR3-mediated urea retrieval from leaf apoplast. Plant J 81: 377-387
10. Breeze E, Harrison E, McHattie S, Hughes L, Hickman R, Hill C, Kiddle S, Kim YS, 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
11. Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin JF, Wu SH, Swidzinski J, Ishizaki K, et al (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvationinduced senescence in Arabidopsis. Plant J 42: 567-585
12. Carlsson J, Leino M, Sohlberg J, Sundstrom JF, Glimelius K (2008) Mitochondrial regulation of flower development. Mitochondrion 8: 74-86
13. Catoni E, Desimone M, HilpertM,Wipf D, Kunze R, Schneider A, Flugge UI, Schumacher K, Frommer WB (2003) Expression pattern of a nuclear encoded mitochondrial arginine-ornithine translocator gene from Arabidopsis. BMC Plant Biol 3: 1
14. Clifton R, Millar AH, Whelan J (2006) Alternative oxidases in Arabidopsis: a comparative analysis of differential expression in the gene family provides new insights into function of non-phosphorylating bypasses. Biochim Biophys Acta 1757: 730-741
15. Collier DE, Thibodeau BA (1995) Changes in respiration and chemical content during autumnal senescence of Populus tremuloides and Quercus rubra leaves. Tree Physiol 15: 759-764
16. Couturier J, Doidy J, Guinet F, Wipf D, Blaudez D, Chalot M (2010) Glutamine, arginine and the amino acid transporter Pt-CAT11 play important roles during senescence in poplar. Ann Bot (Lond) 105: 1159-1169
17. Couturier J, Touraine B, Briat JF, Gaymard F, Rouhier N (2013) The ironsulfur cluster assembly machineries in plants: current knowledge and open questions. Front Plant Sci 4: 259
18. Daschner K, Couee I, Binder S (2001) The mitochondrial isovalerylcoenzyme A dehydrogenase of Arabidopsis oxidizes intermediates of leucine and valine catabolism. Plant Physiol 126: 601-612
19. Debellis L, Nishimura M (1991) Development of enzymes of the glyoxylate cycle during senescence of pumpkin cotyledons. Plant Cell Physiol 32: 555-561
20. Dekker PJ, Martin F, Maarse AC, Bomer U, Muller H, Guiard B, Meijer M, Rassow J, Pfanner N (1997) The Tim core complex defines the number of mitochondrial translocation contact sites and can hold arrested preproteins in the absence of matrix Hsp70-Tim44. EMBO J 16: 5408-5419
21. Dekkers BJ, Pearce S, van Bolderen-Veldkamp RP,Marshall A, Widera P, Gilbert J, Drost HG, Bassel GW, Muller K, King JR, et al (2013) Transcriptional dynamics of two seed compartments with opposing roles in Arabidopsis seed germination. Plant Physiol 163: 205-215
22. Douce R, Bourguignon J, Neuburger M, Rebeille F (2001) The glycine decarboxylase system: a fascinating complex. Trends Plant Sci 6: 167-176
23. 2-induced production of nitric oxide (NO) by NO synthase differentially affects nitrate reductase activity in Arabidopsis plants under different nitrate supplies. J Exp Bot 67: 893-904
24. Dubois F, Tercé-Laforgue T, Gonzalez-Moro MB, Estavillo MB, Sangwan R, Gallais A, Hirel B (2003) Glutamate dehydrogenase in plants: is there a new story for an old enzyme?. Plant Physiol Biochem 41: 565-576
25. 2 levels. Plant J 73: 836-849
26. Engel N, van den Daele K, Kolukisaoglu U, Morgenthal K, Weckwerth W, Parnik T, Keerberg O, Bauwe H (2007) Deletion of glycine decarboxylase in Arabidopsis is lethal under nonphotorespiratory conditions. Plant Physiol 144: 1328-1335
27. Engqvist M, Drincovich MF, Flugge UI, Maurino VG (2009) Two D-2- hydroxy-acid dehydrogenases in Arabidopsis thaliana with catalytic capacities to participate in the last reactions of the methylglyoxal and beta-oxidation pathways. J Biol Chem 284: 25026-25037
28. Engqvist MK, Esser C, Maier A, Lercher MJ, Maurino VG (2014) Mitochondrial 2-hydroxyglutarate metabolism. Mitochondrion 19 Pt B: 275-281
29. Engqvist MK, Kuhn A, Wienstroer J, Weber K, Jansen EE, Jakobs C, Weber AP, Maurino VG (2011) Plant D-2-hydroxyglutarate dehydrogenase participates in the catabolism of lysine especially during senescence. J Biol Chem 286: 11382-11390
30. Faes P, Deleu C, Ainouche A, Le Caherec F, Montes E, Clouet V, Gouraud AM, Albert B, Orsel M, Lassalle G, et al (2015) Molecular evolution and transcriptional regulation of the oilseed rape proline dehydrogenase genes suggest distinct roles of proline catabolism during development. Planta 241: 403-419
31. Fiermonte G, Palmieri L, Todisco S, Agrimi G, Palmieri F, Walker JE (2002) Identification of the mitochondrial glutamate transporter: bacterial expression, reconstitution, functional characterization, and tissue distribution of two human isoforms. J Biol Chem 277: 19289-19294
32. Gardeström P, Igamberdiev AU (2016) The origin of cytosolic ATP in photosynthetic cells. Physiol Plant 157: 367-379
33. Godbole A, Dubey AK, Reddy PS, Udayakumar M, Mathew MK (2013) Mitochondrial VDAC and hexokinase together modulate plant programmed cell death. Protoplasma 250: 875-884
34. Guiboileau A, Sormani R, Meyer C, Masclaux-Daubresse C (2010) Senescence and death of plant organs: nutrient recycling and developmental regulation. C R Biol 333: 382-391
35. Gullberg J, Jonsson P, Nordstrom A, Sjostrom M, Moritz T (2004) Design of experiments: an efficient strategy to identify factors influencing extraction and derivatization of Arabidopsis thaliana samples in metabolomic studies with gas chromatography/mass spectrometry. Anal Biochem 331: 283-295
36. Haferkamp I, Schmitz-Esser S (2012) The plant mitochondrial carrier family: functional and evolutionary aspects. Front Plant Sci 3: 2
37. Hancock JT (2012) NO synthase? Generation of nitric oxide in plants. Period Biol 114: 19-24
38. Himelblau E, Amasino RM (2001) Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence. J Plant Physiol 158: 1317-1323
39. Hooper CM, Tanz SK, Castleden IR, Vacher MA, Small ID, Millar AH (2014) SUBAcon: a consensus algorithm for unifying the subcellular localization data of the Arabidopsis proteome. Bioinformatics 30: 3356-3364
40. Ishizaki K, Larson TR, Schauer N, Fernie AR, Graham IA, Leaver CJ (2005) The critical role of Arabidopsis electron-transfer flavoprotein: ubiquinone oxidoreductase during dark-induced starvation. Plant Cell 17: 2587-2600
41. Ishizaki K, Schauer N, Larson TR, Graham IA, Fernie AR, Leaver CJ (2006) The mitochondrial electron transfer flavoprotein complex is essential for survival of Arabidopsis in extended darkness. Plant J 47: 751-760
42. Ivanova A, Law SR, Narsai R, Duncan O, Lee JH, Zhang B, Van Aken O, Radomiljac JD, van der Merwe M, Yi K, et al (2014) A functional antagonistic relationship between auxin and mitochondrial retrograde signaling regulates ALTERNATIVE OXIDASE1a expression in Arabidopsis. Plant Physiol 165: 1233-1254
43. Jonsson P, Johansson AI, Gullberg J, Trygg JAJ, Grung B, Marklund S, Sjostrom M, Antti H, Moritz T (2005) High-throughput data analysis for detecting and identifying differences between samples in GC/MSbased metabolomic analyses. Anal Chem 77: 5635-5642
44. Kawakami N, Watanabe A (1988) Senescence-specific increase in cytosolic glutamine synthetase and its mRNA in radish cotyledons. Plant Physiol 88: 1430-1434
45. Kayala MA, Baldi P (2012) Cyber-T web server: differential analysis of high-throughput data. Nucleic Acids Res 40: W553-W559
46. Keech O (2011) The conserved mobility of mitochondria during leaf senescence reflects differential regulation of the cytoskeletal components in Arabidopsis thaliana. Plant Signal Behav 6: 147-150
47. Keech O, Dizengremel P, Gardestrom P (2005) Preparation of leaf mitochondria from Arabidopsis thaliana. Physiol Plant 124: 403-409
48. Keech O, Pesquet E, Ahad A, Askne A, Nordvall D, Vodnala SM, Tuominen H, Hurry V, Dizengremel P, Gardestrom P (2007) The different fates of mitochondria and chloroplasts during dark-induced senescence in Arabidopsis leaves. Plant Cell Environ 30: 1523-1534
49. Keech O, Pesquet E, Gutierrez L, Ahad A, Bellini C, Smith SM, Gardestrom P (2010) Leaf senescence is accompanied by an early disruption of the microtubule network in Arabidopsis. Plant Physiol 154: 1710-1720
50. Keskitalo J, Bergquist G, Gardestrom P, Jansson S (2005) A cellular timetable of autumn senescence. Plant Physiol 139: 1635-1648
51. Law SR, Narsai R, Taylor NL, Delannoy E, Carrie C, Giraud E, Millar AH, Small I, Whelan J (2012) Nucleotide and RNA metabolism prime translational initiation in the earliest events of mitochondrial biogenesis during Arabidopsis germination. Plant Physiol 158: 1610-1627
52. Law SR, Narsai R, Whelan J (2014) Mitochondrial biogenesis in plants during seed germination. Mitochondrion 19 Pt B: 214-221
53. Li RJ, Hua W, Lu YT (2006) Arabidopsis cytosolic glutamine synthetase AtGLN1; 1 is a potential substrate of AtCRK3 involved in leaf senescence. Biochem Biophys Res Commun 342: 119-126
54. Lin BL, Wang JS, Liu HC, Chen RW, Meyer Y, Barakat A, Delseny M (2001) Genomic analysis of the Hsp70 superfamily in Arabidopsis thaliana. Cell Stress Chaperones 6: 201-208
55. Lister R, Chew O, Lee MN, Heazlewood JL, Clifton R, Parker KL, Millar AH, Whelan J (2004) A transcriptomic and proteomic characterization of the Arabidopsis mitochondrial protein import apparatus and its response to mitochondrial dysfunction. Plant Physiol 134: 777-789
56. Logan DC, Leaver CJ (2000) Mitochondria-targeted GFP highlights the heterogeneity of mitochondrial shape, size and movement within living plant cells. J Exp Bot 51: 865-871
57. 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
58. 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. Ann Bot (Lond) 105: 1141-1157
59. Mendel RR, Leimkuhler S (2015) The biosynthesis of the molybdenum cofactors. J Biol Inorg Chem 20: 337-347
60. Monne M, Miniero DV, Obata T, Daddabbo L, Palmieri L, Vozza A, Nicolardi MC, Fernie AR, Palmieri F (2015) Functional characterization and organ distribution of three mitochondrial ATP-Mg/Pi carriers in Arabidopsis thaliana. Biochim Biophys Acta 1847: 1220-1230
61. Nogueira FT, Sassaki FT, Maia IG (2011) Arabidopsis thaliana uncoupling proteins (AtUCPs): insights into gene expression during development and stress response and epigenetic regulation. J Bioenerg Biomembr 43: 71-79
62. Palmieri F, Pierri CL, De Grassi A, Nunes-Nesi A, Fernie AR (2011) Evolution, structure and function of mitochondrial carriers: a review with new insights. Plant J 66: 161-181
63. Palmieri L, Todd CD, Arrigoni R, Hoyos ME, Santoro A, Polacco JC, Palmieri F (2006) Arabidopsis mitochondria have two basic amino acid transporters with partially overlapping specificities and differential expression in seedling development. Biochim Biophys Acta 1757: 1277-1283
64. Pan X, Chen Z, Yang X, Liu G (2014) Arabidopsis voltage-dependent anion channel 1 (AtVDAC1) is required for female development and maintenance of mitochondrial functions related to energy-transaction. PLoS ONE 9: e106941
65. Paul VD, Lill R (2015) Biogenesis of cytosolic and nuclear iron-sulfur proteins and their role in genome stability. Biochim Biophys Acta 1853: 1528-1539
66. Peng C, Uygun S, Shiu SH, Last RL (2015) The impact of the branchedchain ketoacid dehydrogenase complex on amino acid homeostasis in Arabidopsis. Plant Physiol 169: 1807-1820
67. Pistelli L, Perata P, Alpi A (1992) Effect of leaf senescence on glyoxylate cycle enzyme-activities. Aust J Plant Physiol 19: 723-729
68. Planchais S, Cabassa C, Toka I, Justin AM, Renou JP, Savoure A, Carol P (2014) BASIC AMINO ACID CARRIER 2 gene expression modulates arginine and urea content and stress recovery in Arabidopsis leaves. Front Plant Sci 5: 330
69. Pracharoenwattana I, Smith SM (2008) When is a peroxisome not a peroxisome?. Trends Plant Sci 13: 522-525
70. Pratelli R, Voll LM, Horst RJ, FrommerWB, Pilot G (2010) Stimulation of nonselective amino acid export by glutamine dumper proteins. Plant Physiol 152: 762-773
71. Quint M, Drost HG, Gabel A, Ullrich KK, Bonn M, Grosse I (2012) A transcriptomic hourglass in plant embryogenesis. Nature 490: 98-101
72. Reimand J, Kull M, Peterson H, Hansen J, Vilo J (2007) g: Profiler: a webbased toolset for functional profiling of gene lists from large-scale experiments. Nucleic Acids Res 35: W193-W200
73. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17: 208-212
74. Robert N, d’Erfurth I, Marmagne A, Erhardt M, Allot M, Boivin K, Gissot L, Monachello D, Michaud M, Duchene AM, et al (2012) Voltage-dependentanion- channels (VDACs) in Arabidopsis have a dual localization in the cell but show a distinct role in mitochondria. Plant Mol Biol 78: 431-446
75. Ruberti C, Barizza E, Bodner M, La Rocca N, De Michele R, Carimi F, Lo Schiavo F, Zottini M (2014) Mitochondria change dynamics and morphology during grapevine leaf senescence. PLoS ONE 9: e102012
76. Schauer N, Steinhauser D, Strelkov S, Schomburg D, Allison G, Moritz T, Lundgren K, Roessner-Tunali U, Forbes MG, Willmitzer L, et al (2005) GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Lett 579: 1332-1337
77. Schippers JH, Schmidt R, Wagstaff C, Jing HC (2015) Living to die and dying to live: the survival strategy behind leaf senescence. Plant Physiol 169: 914-930
78. Shrawat AK, Carroll RT, DePauw M, Taylor GJ, Good AG (2008) Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase. Plant Biotechnol J 6: 722-732
79. Smart CM (1994) Gene-expression during leaf senescence. New Phytol 126: 419-448
80. Sweetlove LJ, Lytovchenko A, MorganM, Nunes-Nesi A, Taylor NL, Baxter CJ, Eickmeier I, Fernie AR (2006) Mitochondrial uncoupling protein is required for efficient photosynthesis. Proc Natl Acad Sci USA 103: 19587-19592
81. Tang GL, Zhu XH, Gakiere B, Levanony H, Kahana A, Galili G (2002) The bifunctional LKR/SDH locus of plants also encodes a highly active monofunctional lysine-ketoglutarate reductase using a polyadenylation signal located within an intron. Plant Physiol 130: 147-154
82. Tanz SK, Castleden I, Hooper CM, Vacher M, Small I, Millar HA (2013) SUBA3: a database for integrating experimentation and prediction to define the subcellular location of proteins in Arabidopsis. Nucleic Acids Res 41: D1185-D1191
83. Thomas H, Huang L, Young M, Ougham H (2009) Evolution of plant senescence. BMC Evol Biol 9: 163
84. Toka I, Planchais S, Cabassa C, Justin AM, De Vos D, Richard L, Savoure A, Carol P (2010) Mutations in the hyperosmotic stress-responsive mitochondrial BASIC AMINO ACID CARRIER2 enhance proline accumulation in Arabidopsis. Plant Physiol 152: 1851-1862
85. Van Aken O, Zhang B, Carrie C, Uggalla V, Paynter E, Giraud E, Whelan J (2009) Defining the mitochondrial stress response in Arabidopsis thaliana. Mol Plant 2: 1310-1324
86. 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 Physiol 141: 776-792
87. van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, Hara-Nishimura I, Jones AM, Kawai-Yamada M, Lam E, Mundy J, et al (2011) Morphological classification of plant cell deaths. Cell Death Differ 18: 1241-1246
88. Van Hoewyk D, Abdel-Ghany SE, Cohu CM, Herbert SK, Kugrens P, Pilon M, Pilon-Smits EA (2007) Chloroplast iron-sulfur cluster protein maturation requires the essential cysteine desulfurase CpNifS. Proc Natl Acad Sci USA 104: 5686-5691
89. Vanlerberghe GC (2013) Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. Int J Mol Sci 14: 6805-6847
90. Vianello A, Zancani M, Peresson C, Petrussa E, Casolo V, Krajnakova J, Patui S, Braidot E,Macri F (2007) Plant mitochondrial pathway leading to programmed cell death. Physiol Plant 129: 242-252
91. Wang T, Li R, Wen L, Fu D, Zhu B, Luo Y, Zhu H (2015) Functional analysis and RNA sequencing indicate the regulatory role of Argonaute1 in tomato compound leaf development. PLoS ONE 10: e0140756
92. Wang Y, Carrie C, Giraud E, Elhafez D, Narsai R, Duncan O, Whelan J, Murcha MW (2012) Dual location of the mitochondrial preprotein transporters B14.7 and Tim23-2 in complex I and the TIM17: 23 complex in Arabidopsis links mitochondrial activity and biogenesis. Plant Cell 24: 2675-2695
93. Wang Y, Law SR, Ivanova A, van Aken O, Kubiszewski-Jakubiak S, Uggalla V, van der Merwe M, Duncan O, Narsai R, Whelan J, et al (2014) The mitochondrial protein import component, TRANSLOCASE OF THE INNER MEMBRANE17-1, plays a role in defining the timing of germination in Arabidopsis. Plant Physiol 166: 1420-1435
94. Watanabe M, Balazadeh S, Tohge T, Erban A, Giavalisco P, Kopka J, Mueller-Roeber B, Fernie AR, Hoefgen R (2013) Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis. Plant Physiol 162: 1290-1310
95. Woo HR, Koo HJ, Kim J, Jeong H, Yang JO, Lee IH, Jun JH, Choi SH, Park SJ, Kang B, et al (2016) Programming of plant leaf senescence with temporal and inter-organellar coordination of transcriptome in Arabidopsis. Plant Physiol 171: 452-467
96. Wydro MM, Sharma P, Foster JM, Bych K, Meyer EH, Balk J (2013) The evolutionarily conserved iron-sulfur protein INDH is required for complex I assembly and mitochondrial translation in Arabidopsis. Plant Cell 25: 4014-4027
97. Zallot R, Agrimi G, Lerma-Ortiz C, Teresinski HJ, Frelin O, Ellens KW, Castegna A, Russo A, de Crecy-Lagard V, Mullen RT, et al (2013) Identification of mitochondrial coenzyme A transporters from maize and Arabidopsis. Plant Physiol 162: 581-588
98. Zhang L, Becker DF (2015) Connecting proline metabolism and signaling pathways in plant senescence. Front Plant Sci 6: 552
99. Zimmermann P, Zentgraf U (2005) The correlation between oxidative stress and leaf senescence during plant development. Cell Mol Biol Lett 10: 515-534
100. Zottini M, Barizza E, Bastianelli F, Carimi F, Lo Schiavo F (2006) Growth and senescence of Medicago truncatula cultured cells are associated with characteristic mitochondrial morphology. New Phytol 172: 239-247