The influence of alternative pathways of respiration that utilize branched-chain amino acids following water shortage in Arabidopsis

Plant Cell and Environment

Volumn 39, Issue 6, 2016, Pages 1304-1319

  Pires, Marcel V ^a,b   Pereira Júnior, Adilson A ^a   Medeiros, David B ^b   Daloso, Danilo M ^a,b   Pham, Phuong Anh ^a   Barros, Kallyne A ^b   Engqvist, Martin K M ^c,d   Florian, Alexandra ^a   Krahnert, Ina ^a   Maurino, Veronica G ^c   Araújo, Wagner L ^b   Fernie, Alisdair R ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^b FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^c HEINRICH HEINE UNIVERSITY   (Germany)

^d CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

Branched chain amino acids; Drought; ETF ETFQO pathway; Metabolomics; Respiration; Tricarboxylic acid cycle

Indexed keywords

AMINO ACID; DICOTYLEDON; DROUGHT STRESS; ENZYME ACTIVITY; METABOLISM; NITRATE; PHYTOCHEMISTRY; RESPIRATION; SENESCENCE; TOLERANCE;

ARABIDOPSIS;

BRANCHED CHAIN AMINO ACID; TRICARBOXYLIC ACID;

ARABIDOPSIS; CELL RESPIRATION; CITRIC ACID CYCLE; DEHYDRATION; METABOLISM; PATHOPHYSIOLOGY; PHOTOSYNTHESIS; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

AMINO ACIDS, BRANCHED-CHAIN; ARABIDOPSIS; CELL RESPIRATION; CITRIC ACID CYCLE; DEHYDRATION; PHOTOSYNTHESIS; REAL-TIME POLYMERASE CHAIN REACTION; TRICARBOXYLIC ACIDS;

EID: 84959561152     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12682     Document Type: Article

References (89)

1. Angelovici R., Lipka A.E., Deason N., Gonzalez-Jorge S., Lin H.N., Cepela J., ... DellaPenna D. (2013) Genome-wide analysis of branched-chain amino acid levels in Arabidopsis seeds. Plant Cell 25, 4827-4843.
2. Araújo W.L., Ishizaki K., Nunes-Nesi A., Larson T.R., Tohge T., Krahnert I., ... Fernie A.R. (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.
3. Araújo W.L., Ishizaki K., Nunes-Nesi A., Tohge T., Larson T.R., Krahnert I., ... Fernie A.R. (2011a) Analysis of a range of catabolic mutants provides evidence that phytanoyl-coenzyme a does not act as a substrate of the electron-transfer flavoprotein/electron-transfer flavoprotein:ubiquinone oxidoreductase complex in Arabidopsis during dark-induced senescence. Plant Physiology 157, 55-69.
4. Araújo W.L., Nunes-Nesi A. & Fernie A.R. (2014) On the role of plant mitochondrial metabolism and its impact on photosynthesis in both optimal and sub-optimal growth conditions. Photosynthesis Research 119, 141-156.
5. Araújo W.L., Nunes-Nesi A., Nikoloski Z., Sweetlove L.J. & Fernie A.R. (2012) Metabolic control and regulation of the tricarboxylic acid cycle in photosynthetic and heterotrophic plant tissues. Plant, Cell and Environment 35, 1-21.
6. Araújo W.L., Nunes-Nesi A., Osorio S., Usadel B., Fuentes D., Nagy R., ... Fernie A.R. (2011b) Antisense inhibition of the iron-sulphur subunit of succinate dehydrogenase enhances photosynthesis and growth in tomato via an organic acid-mediated effect on stomatal aperture. Plant Cell 23, 600-627.
7. Araújo W.L., Tohge T., Ishizaki K., Leaver C.J. & Fernie A.R. (2011c) Protein degradation - an alternative respiratory substrate for stressed plants. Trends in Plant Science 16, 489-498.
8. Atkin O.K. & Macherel D. (2009) The crucial role of plant mitochondria in orchestrating drought tolerance. Annals of Botany 103, 581-597.
9. Bartels D. & Sunkar R. (2005) Drought and salt tolerance in plants. Critical Reviews in Plant Sciences 24, 23-58.
10. Bartoli C.G., Gomez F., Gergoff G., Guiamet J.J. & Puntarulo S. (2005) Up-regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions. Journal of Experimental Botany 56, 1269-1276.
11. Bauwe H., Hagemann M. & Fernie A.R. (2010) Photorespiration: players, partners and origin. Trends in Plant Science 15, 330-336.
12. Beckmann J.D. & Frerman F.E. (1985) Electron-transfer flavoprotein-ubiquinone oxidoreductase from pig liver: purification and molecular, redox, and catalytic properties. Biochemistry 24, 3913-3921.
13. Binder S. (2010) Branched-chain amino acid metabolism in Arabidopsis thaliana. In The Arabidopsis Book 8, e0137.
14. Binder S., Knill T. & Schuster J. (2007) Branched-chain amino acid metabolism in higher plants. Physiologia Plantarum 129, 68-78.
15. Bowne J.B., Erwin T.A., Juttner J., Schnurbusch T., Langridge P., Bacic A. & Roessner U. (2012) Drought responses of leaf tissues from wheat cultivars of differing drought tolerance at the metabolite level. Molecular Plant 5, 418-429.
16. Bradford M.M. (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Analytical Biochemistry 72, 248-254.
17. Buchanan-Wollaston V., Page T., Harrison E., Breeze E., Lim P.O., Nam H.G., ... Leaver C.J. (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant Journal 42, 567-585.
18. Bugos R.C., Chiang V.L., Zhang X.H., Campbell E.R., Podila G.K. & Campbell W.H. (1995) RNA isolation from plant tissues recalcitrant to extraction in guanidine. Biotechniques 19, 734-737.
19. Caldana C., Degenkolbe T., Cuadros-Inostroza A., Klie S., Sulpice R., Leisse A., ... Hannah M.A. (2011) High-density kinetic analysis of the metabolomic and transcriptomic response of Arabidopsis to eight environmental conditions. Plant Journal 67, 869-884.
20. Carrari F., Baxter C., Usadel B., Urbanczyk-Wochniak E., Zanor M.-I., Nunes-Nesi A., ... Fernie A.R. (2006) Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior. Plant Physiology 142, 1380-1396.
21. 2 by both Rubisco and PEPcase while sucrose acts as a substrate during light-induced stomatal opening. Plant, Cell & Environment 38, 2353-2371.
22. Däschner K., Couee I. & Binder S. (2001) The mitochondrial isovaleryl-coenzyme A dehydrogenase of Arabidopsis oxidizes intermediates of leucine and valine catabolism. Plant Physiology 126, 601-612.
23. Dinakar C., Abhaypratap V., Yearla S.R., Raghavendra A.S. & Padmasree K. (2010) Importance of ROS and antioxidant system during the beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Planta 231, 461-474.
24. Ding G., Che P., Ilarslan H., Wurtele E.S. & Nikolau B.J. (2012) Genetic dissection of methylcrotonyl CoA carboxylase indicates a complex role for mitochondrial leucine catabolism during seed development and germination. Plant Journal 70, 562-577.
25. Dinneny J.R., Long T.A., Wang J.Y., Jung J.W., Mace D., Pointer S., ... Benfey P.N. (2008) Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science 320, 942-945.
26. Dumas R., Biou V., Halgand F., Douce R. & Duggleby R.G. (2001) Enzymology, structure, and dynamics of acetohydroxy acid isomeroreductase. Accounts of Chemical Research 34, 399-408.
27. Engqvist M., Drincovich M.F., Fluegge U.-I. & Maurino V.G. (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. Journal of Biological Chemistry 284, 25026-25037.
28. Engqvist M.K.M., Kuhn A., Wienstroer J., Weber K., Jansen E.E.W., Jakobs C., ... Maurino V.G. (2011) Plant D-2-hydroxyglutarate dehydrogenase participates in the catabolism of lysine especially during senescence. Journal of Biological Chemistry 286, 11382-11390.
29. Fahnenstich H., Saigo M., Niessen M., Zanor M.I., Andreo C.S., Fernie A.R., ... Maurino V.G. (2007) Alteration of organic acid metabolism in Arabidopsis overexpressing the maize C(4)NADP-malic enzyme causes accelerated senescence during extended darkness. Plant Physiology 145, 640-652.
30. Fernie A.R., Aharoni A., Willmitzer L., Stitt M., Tohge T., Kopka J., ... DeLuca V. (2011) Recommendations for reporting metabolite data. Plant Cell 23, 2477-2482.
31. Flexas J., Bota J., Galmes J., Medrano H. & Ribas-Carbo M. (2006) Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiologia Plantarum 127, 343-352.
32. Foyer C.H. & Noctor G. (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiology 155, 2-18.
33. Frerman F.E. (1988) Acyl-CoA dehydrogenases, electron transfer flavoprotein and electron transfer flavoprotein dehydrogenase. Biochemical Society Transactions 16, 416-418.
34. Gechev T., Benina M., Obata T., Tohge T., Sujeeth N., Minkov I., ... Toneva V. (2013) Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis. Cellular and Molecular Life Sciences 70, 689-709.
35. Geigenberger P., Fernie A.R., Gibon Y., Christ M. & Stitt M. (2000) Metabolic activity decreases as an adaptive response to low internal oxygen in growing potato tubers. Biological Chemistry 381, 723-740.
36. Geisler D.A., Päpke C., Obata T., Nunes-Nesi A., Matthes A., Schneitz K., ... Persson S. (2012) Downregulation of the δ-subunit reduces mitochondrial ATP synthase levels, alters respiration, and restricts growth and gametophyte development in Arabidopsis. Plant Cell 24, 2792-2811.
37. Giraud E., Ho L.H.M., Clifton R., Carroll A., Estavillo G., Tan Y.-F., ... Whelan J. (2008) The absence of ALTERNATIVE OXIDASE1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiology 147, 595-610.
38. Heazlewood J.L., Tonti-Filippini J.S., Gout A.M., Day D.A., Whelan J. & Millar A.H. (2004) Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16, 241-256.
39. Hildebrandt T.M., Nesi A.N., Araújo W.L. & Braun H.-P. (2015) Amino acid catabolism in plants. Molecular Plant 8, 1563-1579.
40. Hüdig M., Maier A., Scherrers I., Seidel L., Jansen E.E.W., Mettler-Altmann T., ... Maurino V.G. (2015) Plants possess a cyclic mitochondrial metabolic pathway similar to the mammalian metabolic repair mechanism involving malate dehydrogenase and l-2-hydroxyglutarate dehydrogenase. Plant and Cell Physiology 56, 1820-1830.
41. Ishizaki K., Larson T.R., Schauer N., Fernie A.R., Graham I.A. & Leaver C.J. (2005) The critical role of Arabidopsis electron-transfer flavoprotein:ubiquinone oxidoreductase during dark-induced starvation. Plant Cell 17, 2587-2600.
42. Ishizaki K., Schauer N., Larson T.R., Graham I.A., Fernie A.R. & Leaver C.J. (2006) The mitochondrial electron transfer flavoprotein complex is essential for survival of Arabidopsis in extended darkness. Plant Journal 47, 751-760.
43. Jacoby R.P., Li L., Huang S., Pong L.C., Millar A.H. & Taylor N.L. (2012) Mitochondrial composition, function and stress response in plants. Journal of Integrative Plant Biology 54, 887-906.
44. Kirma M., Araujo W.L., Fernie A.R. & Galili G. (2012) The multifaceted role of aspartate-family amino acids in plant metabolism. Journal of Experimental Botany 63, 4995-5001.
45. Kochevenko A., Araujo W.L., Maloney G.S., Tieman D.M., Phuc Thi D., Taylor M.G., ... Fernie A.R. (2012) Catabolism of branched chain amino acids supports respiration but not volatile synthesis in tomato fruits. Molecular Plant 5, 366-375.
46. Kopka J., Schauer N., Krueger S., Birkemeyer C., Usadel B., Bergmuller E., ... Steinhauser D. (2005) GMD@CSB.DB: the Golm metabolome database. Bioinformatics 21, 1635-1638.
47. 2 concentrations. Plant Physiology 102, 947-955.
48. Lawlor D.W. (2013) Genetic engineering to improve plant performance under drought: physiological evaluation of achievements, limitations, and possibilities. Journal of Experimental Botany 64, 83-108.
49. Lehmann M., Schwarzländer M., Obata T., Sirikantaramas S., Burow M., Olsen C.E., ... Laxa M. (2009) The metabolic response of Arabidopsis roots to oxidative stress is distinct from that of heterotrophic cells in culture and highlights a complex relationship between the levels of transcripts, metabolites, and flux. Molecular Plant 2, 390-406.
50. Lisec J., Schauer N., Kopka J., Willmitzer L. & Fernie A.R. (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nature Protocols 1, 387-396.
51. Luedemann A., Strassburg K., Erban A. & Kopka J. (2008) TagFinder for the quantitative analysis of gas chromatography-mass spectrometry (GC-MS)-based metabolite profiling experiments. Bioinformatics 24, 732-737.
52. Long S.P. & Bernacchi C.J. (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. Journal of Experimental Botany 54, 2393-2401.
53. Meyer E.H., Tomaz T., Carroll A.J., Estavillo G., Delannoy E., Tanz S.K., ... Millar A.H. (2009) Remodeled respiration in ndufs4 with low phosphorylation efficiency suppresses Arabidopsis germination and growth and alters control of metabolism at night. Plant Physiology 151, 603-619.
54. Medeiros D.M., Martins S.C.V, Cavalcanti J.H.F., Daloso D.M., Martinoia E., Nunes-Nesi A., ... Araújo W.L. (2016) Enhanced photosynthesis and growth in atquac1 knockout mutants are due to altered organic acid accumulation and an increase in both stomatal and mesophyll conductance. Plant Physiology DOI: 10.1104/pp.15.01053
55. Møller I.M. & Sweetlove L.J. (2010) ROS signalling - specificity is required. Trends in Plant Science 15, 370-374.
56. Niinemets Ü., Cescatti A., Rodeghiero M. & Tosens T. (2005) Leaf internal diffusion conductance limits photosynthesis more strongly in older leaves of Mediterranean evergreen broad-leaved species. Plant, Cell and Environment 28, 1552-1566.
57. Niinemets Ü., Cescatti A., Rodeghiero M. & Tosens T. (2006) Complex adjustments of photosynthetic potentials and internal diffusion conductance to current and previous light availabilities and leaf age in Mediterranean evergreen species Quercus ilex. Plant, Cell and Environment 29, 1159-1178.
58. Niinemets Ü., Díaz-Espejo A., Flexas J., Galmés J. & Warren C.R. (2009) Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field. Journal of Experimental Botany 60, 2249-2270.
59. Nunes-Nesi A., Araujo W.L. & Fernie A.R. (2011) Targeting mitochondrial metabolism and machinery as a means to enhance photosynthesis. Plant Physiology 155, 101-107.
60. Obata T. & Fernie A.R. (2012) The use of metabolomics to dissect plant responses to abiotic stresses. Cellular and Molecular Life Sciences 69, 3225-3245.
61. Oh S.A., Lee S.Y., Chung I.K., Lee C.H. & Nam H.G. (1996) A senescence-associated gene of Arabidopsis thaliana is distinctively regulated during natural and artificially induced leaf senescence. Plant Molecular Biology 30, 739-754.
62. Oliver M.J., Guo L., Alexander D.C., Ryals J.A., Wone B.W.M. & Cushman J.C. (2011) A sister group contrast using untargeted global metabolomic analysis delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus. Plant Cell 23, 1231-1248.
63. Pastore D., Trono D., Laus M.N., Di Fonzo N. & Flagella Z. (2007) Possible plant mitochondria involvement in cell adaptation to drought stress - a case study: durum wheat mitochondria. Journal of Experimental Botany 58, 195-210.
64. Peng C., Uygun S., Shiu S.-H. & Last R.L. (2015) The impact of the branched-chain ketoacid dehydrogenase complex on amino acid homeostasis in Arabidopsis. Plant Physiology 169, 1807-1820.
65. Plaxton W.C. & Podesta F.E. (2006) The functional organization and control of plant respiration. Critical Reviews in Plant Sciences 25, 159-198.
66. Porra R.J., Thompson W.A. & Kriedemann P.E. (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta 975, 384-394.
67. Ribas-Carbo M., Taylor N.L., Giles L., Busquets S., Finnegan P.M., Day D.A., ... Flexas J. (2005) Effects of water stress on respiration in soybean leaves. Plant Physiology 139, 466-473.
68. Rodeghiero M., Niinemets Ü. & Cescatti A. (2007) Major diffusion leaks of clamp-on leaf cuvettes still unaccounted: how erroneous are the estimates of Farquhar et al. model parameters? Plant, Cell and Environment 30, 1006-1022.
69. Ruzicka F.J. & Beinert H. (1977) A new iron-sulfur flavoprotein of the respiratory chain. A component of the fatty acid beta oxidation pathway. Journal of Biological Chemistry 252, 8440-8445.
70. Sharkey T.D. (1988) Estimating the rate of photorespiration in leaves. Physiologia Plantarum 73, 147-152.
71. Schuster J. & Binder S. (2005) The mitochondrial branched-chain aminotransferase (AtBCAT-1) is capable to initiate degradation of leucine, isoleucine and valine in almost all tissues in Arabidopsis thaliana. Plant Molecular Biology 57, 241-254.
72. Semel Y., Schauer N., Roessner U., Zamir D. & Fernie A.R. (2007) Metabolite analysis for the comparison of irrigated and non-irrigated field grown tomato of varying genotype. Metabolomics 3, 289-295.
73. Sienkiewicz-Porzucek A, Sulpice R, Osorio O, Krahnert I, Leisse A, Urbanczyk-Wochniak E, ... Nunes-Nesi A. (2010) Mild reductions in mitochondrial NAD-dependent isocitrate dehydrogenase activity result in altered nitrate assimilation and pigmentation but do not impact growth. Molecular Plant 3, 156-173
74. Singh B.K. & Shaner D.L. (1995) Biosynthesis of branched chain amino acids: from test tube to field. Plant Cell 7, 935-944.
75. Skirycz A., De Bodt S., Obata T., De Clercq I., Claeys H., De Rycke R., ... Inze D. (2010a) Developmental stage specificity and the role of mitochondrial metabolism in the response of Arabidopsis leaves to prolonged mild osmotic stress. Plant Physiology 152, 226-244.
76. Skirycz A., Memmi S., De Bodt S., Maleux K., Obata T., Fernie A.R., ... Inzé D. (2010b) A reciprocal 15N-labeling proteomic analysis of expanding Arabidopsis leaves subjected to osmotic stress indicates importance of mitochondria in preserving plastid functions. Journal of Proteome Research 10, 1018-1029.
77. Skirycz A., Vandenbroucke K., Clauw P., Maleux K., De Meyer B., Dhondt S., ... Inze D. (2011) Survival and growth of Arabidopsis plants given limited water are not equal. Nat Biotech 29, 212-214.
78. Taji T., Ohsumi C., Iuchi S., Seki M., Kasuga M., Kobayashi M., ... Shinozaki K. (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. The Plant Journal 29, 417-426.
79. Urano K., Maruyama K., Ogata Y., Morishita Y., Takeda M., Sakurai N., ... Shinozaki K. (2009) Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. Plant Journal 57, 1065-1078.
80. van Dongen J.T., Gupta K.J., Ramirez-Aguilar S.J., Araujo W.L., Nunes-Nesi A. & Fernie A.R. (2011) Regulation of respiration in plants: a role for alternative metabolic pathways. Journal of Plant Physiology 168, 1434-1443.
81. Verslues P.E., Agarwal M., Katiyar-Agarwal S., Zhu J. & Zhu J.-K. (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant Journal 45, 523-539.
82. Watmough N.J. & Frerman F.E. (2010) The electron transfer flavoprotein ubiquinone oxidoreductases. Biochimica et Biophysica Acta 1797, 1910-1916.
83. Weigelt K., Küster H., Radchuk R., Müller M., Weichert H., Fait A., ... Weber H. (2008) Increasing amino acid supply in pea embryos reveals specific interactions of N and C metabolism, and highlights the importance of mitochondrial metabolism. Plant Journal 55, 909-926.
84. Witt S., Galicia L., Lisec J., Cairns J., Tiessen A., Luis Araus J., ... Fernie A.R. (2012) Metabolic and phenotypic responses of greenhouse-grown maize hybrids to experimentally controlled drought stress. Molecular Plant 5, 401-417.
85. Woo N., Badger M. & Pogson B. (2008) A rapid, non-invasive procedure for quantitative assessment of drought survival using chlorophyll fluorescence. Plant Methods 4, 27.
86. Zanor M.I., Osorio S., Nunes-Nesi A., Carrari F., Lohse M., Usadel B., ... Fernie A.R. (2009) RNA interference of LIN5 in tomato confirms its role in controlling brix content, uncovers the influence of sugars on the levels of fruit hormones, and demonstrates the importance of sucrose cleavage for normal fruit development and fertility. Plant Physiology 150, 1204-1218.
87. Zhang J., Frerman F.E. & Kim J.-J.P. (2006) Structure of electron transfer flavoprotein-ubiquinone oxidoreductase and electron transfer to the mitochondrial ubiquinone pool. Proceedings of the National Academy of Sciences of the United States of America 103, 16212-16217.
88. Zhu J.-K. (2002) Salt and drought stress signal transduction in plants. Ann Rev Plant Biol 53, 247-273.
89. Zhu Q., Dugardeyn J., Zhang C., Mühlenbock P., Eastmond P.J., Valcke R., ... Van Der Straeten D. (2014) The Arabidopsis thaliana RNA editing factor SLO2, which affects the mitochondrial electron transport chain, participates in multiple stress and hormone responses. Molecular Plant 7, 290-310.