Signaling, regulation and metabolic interactions
Team composition :
- Michael HODGES DR2 CNRS
- Guillaume TCHERKEZ PR1 UPsud
- Valérie FLESCH MdC UPsud
- Bertrand GAKIERE MdC UPsud
- Marie GARMIER MdC UPsud
- Nathalie GLAB CR1 CNRS
- Mathieu JOSSIER MdC UPsud
- Aline MAHE MdC UPsud
- Martine THOMAS MdC UPsud
- Sophie MASSOT T UPsud
- Céline OURY AJT UPsud
- Edouard BOEX-FONTVIEILLE Post-doc SPS
- Linda DE BONT PhD student
- Younès DELLERO PhD student
Overview of research theme
The development of a sustainable agriculture and the use of plants for biomass energy and green chemistry need biochemical engineering to optimize plant metabolism. This is currently impeded by our poor understanding of critical metabolic steps that control complex plant metabolic networks and by the lack of an integrative and dynamic view of plant metabolism. It is a prerequisite to identify the metabolic bottlenecks that require improvement. Photosynthetic carbon assimilation is not a sufficient base from which to calculate growth, it is also necessary to consider many other metabolic pathways including photorespiration, respiration, nitrogen assimilation, amino acid synthesis, NAD biosynthesis. These processes interact within leaf cells, thus allowing the assimilation of both carbon and nitrogen but also leading to the liberation of both CO2 and NH3 that must be re-assimilated at a certain energetic cost.
A simplified scheme showing interactions between primary metabolic plant functions and highlighting C, N inputs and C, N outputs.
Respiration plays a central role in linking photosynthesis and N-assimilation since it provides intermediates (carbon skeletons, energy) for N-assimilation while causing C-loss in the form of CO2. Nevertheless, reducing respiration does not necessarily improve plant growth and net C-gain. Respiratory metabolism is dictated by metabolic imperatives that manifest themselves through the inhibition of leaf day respiration compared to the dark. Physiological experiments have shown that the inhibition of day respiration in the light is associated with a lower TCA pathway (TCAP) activity. Lower respiration also leads to lower photorespiration which in turn can affect nitrate assimilation. The intrinsic mechanism(s) by which respiration is down-regulated in the light is certainly a complex regulation-set based on redox-poise and effectors between plant cell compartments. Nevertheless, many uncertainties remain on metabolic fluxes and interactions with other metabolic pathways.
Our major aims are to obtain a better understanding of the interactions between primary metabolic pathways, to highlight limiting steps, and new regulatory steps that allow plants to modify and adapt their metabolisms to fluctuating environmental conditions.
Two principal research areas are developed :
• Signaling and regulation – to understand the role of regulatory proteins and metabolites on plant metabolism and growth and to discover new protein phosphorylation-associated regulations.
• Metabolic interactions and bypasses – to understand the interactions between photosynthesis, (photo)/respiration, N-metabolism, and NADH synthesis.
To attain our goals we combine biochemical, physiological (gas exchange), and “omics” analyses (including transcriptomics, phosphoproteomics, metabolomics), as well as cell and molecular biology. Purified recombinant proteins, selected mutant lines and stable isotope labeling are routinely used. Much of our work focuses on Arabidopsis thaliana as a plant model due to the genetic and proteomic resources available. However, certain physiological aspects of our research benefit from other plant species such as cocklebur, sunflower, geranium and rapeseed.
Signaling and regulation
SnRK1 (Snf1-Related protein Kinase 1) protein kinases. SnRK1 protein kinases, the plant orthologs of yeast Snf1 kinase and mammalian AMPK, are central components of plant stress response signalling cascades. These enzymes are complexes composed of a catalytic subunit (kinase ) and two regulatory subunits ( and ). SnRK1s help coordinate nutrient storage and remobilization, growth, and promote stress tolerance by regulating over a thousand genes and key biosynthetic enzymes. Despite their importance, little is known of how they are regulated and of the cellular processes they control in plants. Our work aims to assess the regulation of these complexes by upstream kinases (SnAK, SnRK1 Activating Kinases) and metabolites as well as to investigate the involvement of SnRK1 in cell cycle progression and cell proliferation.
• Recombinant protein technology was used to show that Arabidopsis SnAKs are activated by autophosphorylation that precedes a molecular mechanism of cross-phosphorylation between SnRK1 and SnAKs including an inhibitory feedback phosphorylation controlling SnAK (Crozet et al 2010 J Biol Chem).
• We have development a rapid immunoprecipitation-based protocol for SnRK1 enrichment allowing the analysis of SnRK1 response to various metabolites. Recently, mammalian AMPK-dependent phosphorylation of p27KIP1 was found to impact cell cycle progression, autophagy and apoptosis. To highlight a potential link between energy homeostasis and plant cell proliferation, we investigated whether a SnRK1-mediated phosphorylation of Arabidopsis p27KIP1 orthologs KRP could modulate cell cycle progression in plants.
• SnRK1 was found to phosphorylate Arabidopsis KRP6 and KRP7 at Thr152/151 respectively, as identified by tandem mass spectrometry and site-specific mutagenesis.
• Arabidopsis SnRK1 physically interacted with KRP6 in the nucleus of transformed BY-2 tobacco protoplasts but, in contrast to mammals, KRP6 Thr152-phosphorylation state alone did not modify its nuclear localization.
BiFC experiments indicate that KRP6 interacts with SnRK1 alpha 1 in the nucleus of BY2 protoplasts (left) while GFP-tagged KRP6 and site-directed mutagenesis show that Thr152 phosphorylation does not appear to modify KRP6 localization (right).
• Using a heterologous yeast system, cell proliferation was shown to be abolished by KRP6WT and KRP6T152A, but not by the phosphorylation-mimetic form KRP6T152D. Moreover, Arabidopsis SnRK1α1/KRP6 double overexpressors (OE) and OE-KRP6T152D plants showed a clear attenuation of KRP6-associated phenotypes.
Thus, the energy sensor SnRK1, through inhibition of KRP6 biological function by phosphorylation, appears to play a cardinal function in the control of cell proliferation in Arabidopsis plants (Guérinier et al 2013 Plant J).
This work benefited from 3 French Education Ministry PhD grants, and collaborations with E. Baena-Gonzales (Lisbon, Portugal), S. Nessler (LEBS, Gif/Yvette) and PAPPSO (Ferme du Moulon, Orsay).
Leaf Phosphoproteomics . To investigate the regulation of (photo)/respiratory enzymes by protein phosphorylation, a phosphoproteomics analysis of Arabidopsis leaves placed under light or dark conditions and at different CO2 concentrations to modulate (photo)/respiratory activities was carried out.
• This led to the identification of 2420 phosphopeptides (of 1552 proteins), while 264 phosphopeptides (203 proteins) showed a significant change in level between treatments with 22 phosphoproteins associated with “Metabolism”.
• A single respiratory enzyme phosphopeptide was detected in our analysis, while phosphopeptides were found for four different photorespiratory enzymes of which glycolate oxidase and serine hydroxymethyl transferase exhibited photorespiratory-dependent changes in phosphorylation level. We are currently trying to understand the role of these different phosphorylation events.
This work was initiated by an IFR87 grant and carried out in collaboration with PAPPSO (Ferme du Moulon, Gif/Yvette).
NAD(H) as a signal . NAD has recently been shown to be involved in several signalling pathways associated with stress tolerance and/or defense responses. The mechanisms by which NAD influences plant gene regulation, metabolism and physiology are not clear. Arabidopsis thaliana lines over-expressing E. coli NadC, encoding the NAD biosynthesis enzyme quinolinate phosphoribosyltransferase (QPT) accumulated NAD when given quinolinate. These lines were used as inducible systems to determine the consequences of increased leaf NAD content.
NAD metabolism has a major role in many plant pathways and responses to the environment that involve different sub-cellular compartments
• Metabolic profiling showed changes in several metabolites including aspartate-derived amino acids and NAD-derived nicotinic acid.
• Large-scale transcriptomic analyses indicated an NAD promoted induction of pathogen-related genes such as the salicylic acid (SA)-responsive defense marker PR1. Comparison with transcriptomic databases showed that gene expression under high NAD content was similar to that obtained under biotic stress, eliciting conditions or SA treatment.
• Upon inoculation with the avirulent strain of Pseudomonas syringae pv. tomato Pst-AvrRpm1, the NadC lines showed enhanced resistance to bacterial infection and exhibited an ICS1-dependent build-up of both conjugated and free SA pools. We conclude that a higher NAD content is beneficial to plant immunity by stimulating SA-dependent signalling and pathogen resistance (Guérard et al 2011 Plant Physiol Biochem ; Pétriacq et al 2012 Plant J ; Pétriacq et al 2012 Plant Signal Behav).
This work has benefited from 2 French Education Ministry PhD grants and several IFR87 collaborative grants.
Metabolic interactions and bypasses The combined use of stable isotope labeling (13C, 15N, 3H) coupled to gas exchange measurements, IRMS and NMR analyses has led our team to publish the following original results and conclusions concerning interactions between respiration, photorespiration and N-assimilation. • In the light the TCA (or Krebs) ‘‘cycle’’ does not work in the forward direction like a proper cycle but, rather, operates in both the reverse and forward directions to produce fumarate and 2-oxoglutarate (2OG), respectively (Tcherkez et al 2008 Plant Physiol). Such a functional division of the cycle plausibly reflects the compromise between two contrasted forces : (1) The feedback inhibition by NADH and ATP on TCA enzymes in the light, and (2) the need to provide pH-buffering organic acids and C-skeletons for nitrate absorption and assimilation.
• Both glycolysis and TCA pathway (TCAP) activities are inversely related to the ambient CO2/O2 ratio : day respiratory metabolism is enhanced under high photorespiratory (low CO2) conditions. Such a relationship also correlates with the dihydroxyacetone phosphate/glucose-6-phosphate ratio, suggesting that photosynthetic products exert a control on day respiration (Tcherkez et al 2010 Proc Natl Acad Sci USA). Thus, day respiration is inhibited by phosphoryl (ATP/ADP) and reductive (NADH/NAD) poise but it is up-regulated by photorespiration. This may be related to the need for NH2 transfers during the recovery of photorespiratory cycle intermediates. Indeed, high photorespiratory conditions appear to stimulate TCAP 2OG production for Glu metabolism (Tcherkez et al 2012 Plant Cell Environ).
• The remobilization of night-stored C-reserves plays a significant role in providing 2OG for Glu synthesis in illuminated rapeseed leaves, and therefore the natural day-night cycle seems critical for N assimilation (Gauthier et al 2010 New Phytol).
• Phosphoenolpyruvate metabolism is reversible in the light due to the involvement of the pyruvate Pi dikinase (Tcherkez et al 2011 Plant Physiol).
• Arabidopsis leaves (of isocitrate dehydrogenase homo/hemizygous mutants for mitochondrial NAD-dependent and cytosolic NADP-dependent enzymes) with extremely low 2OG production capacities exhibit a stimulated Lys metabolism bypass pathway to generate 2OG for Glu metabolism (Boex-Fontvieille et al 2013 New Phytol).
Isotope labeling (13C-Glucose, 13C-Lysine) coupled to LC-MS analysis showed an increase in an alternative 2OG-producing pathway via the synthesis & subsequent metabolism of lysine.
We are also interested in understanding the interaction between NAD and plant primary metabolisms. Little is known about NAD synthesis in plants, except the identification of at least two possible pathways. The manipulation of Arabidospsis thaliana NAD biosynthetic enzymes is being used to constitutively deregulate NAD production. • This approach has pointed out the critical role of NAD in C/N interactions by affecting N assimilation under photorespiratory conditions. These results pave the way for a better understanding of key regulatory mechanisms underlying coordinated plant metabolic interactions. • The present work clearly establishes (1) the importance of these NAD synthesis pathways, and (2) highlights the potential influence of NAD content on plant function and growth.
This work is/has been financed by successive ANR JC grants, a LabEx SPS Flagship project grant, several IFR87 grants, and four French Education Ministry PhD grants and benefited from the IFR87 Metabolism-Metabolome platform and collaborations with R. Bligny (Grenoble), S. Nogues (Barcelona, Spain), G. Farquhar (Canberra, Australia) and M. Babour (Sydney, Australia).
1. Baud, S., Feria Bourrellier, A.B., Azzopardi, M., Berger, A., Dechorgnat, J., Daniel-Vedele, F., Lepiniec, L., Miquel, M., Rochat, C., Hodges, M., and Ferrario-Mery, S. (2010). PII is induced by WRINKLED1 and fine-tunes fatty acid composition in seeds of Arabidopsis thaliana. Plant J 64, 291-303.
2. Capelle, V., Remoue, C., Moreau, L., Reyss, A., Mahe, A., Massonneau, A., Falque, M., Charcosset, A., Thevenot, C., Rogowsky, P., Coursol, S., and Prioul, J.L. (2010). QTLs and candidate genes for desiccation and abscisic acid content in maize kernels. BMC Plant Biol 10, 2.
3. Crozet, P., Jammes, F., Valot, B., Ambard-Bretteville, F., Nessler, S., Hodges, M., Vidal, J., and Thomas, M. (2010). Cross-phosphorylation between Arabidopsis thaliana sucrose nonfermenting 1-related protein kinase 1 (AtSnRK1) and its activating kinase (AtSnAK) determines their catalytic activities. J Biol Chem 285, 12071-12077.
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5. Feria Bourrellier, A.B., Valot, B., Guillot, A., Ambard-Bretteville, F., Vidal, J., and Hodges, M. (2010). Chloroplast acetyl-CoA carboxylase activity is 2-oxoglutarate-regulated by interaction of PII with the biotin carboxyl carrier subunit. Proc Natl Acad Sci USA 107, 502-507.
6. Gauthier, P., Bligny, R., Gout, E., Mahe, A., Nogues, S., Hodges, M., and Tcherkez, G. (2010). In folio isotopic tracing demonstrates that nitrogen assimilation into glutamate is mostly independent from current CO2 assimilation in illuminated leaves of Brassica napus. New Phytol 185, 988-999.
7. Mhamdi, A., Mauve, C., Gouia, H., Saindrenan, P., Hodges, M., and Noctor, G. (2010). Cytosolic NADP-dependent isocitrate dehydrogenase contributes to redox homeostasis and the regulation of pathogen responses in Arabidopsis leaves. Plant Cell Environ 33, 1112-1123.
8. Sienkiewicz-Porzucek, A., Sulpice, R., Osorio, S., Krahnert, I., Leisse, A., Urbanczyk-Wochniak, E., Hodges, M., Fernie, A.R., and 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. Mol Plant 3, 156-173.
9. Tcherkez, G. (2010). Do metabolic fluxes matter for interpreting isotopic respiratory signals ? New Phytol 186, 566-568 ; author reply 569-571.
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11. Barbour, M.M., Tcherkez, G., Bickford, C.P., Mauve, C., Lamothe, M., Sinton, S., and Brown, H. (2011). delta13C of leaf-respired CO2 reflects intrinsic water-use efficiency in barley. Plant Cell Environ 34, 792-799.
12. Barbour, M.M., Hunt, J.E., Kodama, N., Laubach, J., McSeveny, T.M., Rogers, G.N., Tcherkez, G., and Wingate, L. (2011). Rapid changes in delta13C of ecosystem-respired CO2 after sunset are consistent with transient 13C enrichment of leaf respired CO2. New Phytol 190, 990-1002.
13. Foyer, C.H., Noctor, G., and Hodges, M. (2011). Respiration and nitrogen assimilation : targeting mitochondria-associated metabolism as a means to enhance nitrogen use efficiency. J Exp Bot 62, 1467-1482.
14. Gilbert, A., Silvestre, V., Robins, R.J., Tcherkez, G., and Remaud, G.S. (2011). A 13C NMR spectrometric method for the determination of intramolecular delta13C values in fructose from plant sucrose samples. New Phytol 191, 579-588.
15. Gilbert, A., Silvestre, V., Segebarth, N., Tcherkez, G., Guillou, C., Robins, R.J., Akoka, S., and Remaud, G.S. (2011). The intramolecular 13C-distribution in ethanol reveals the influence of the CO2-fixation pathway and environmental conditions on the site-specific 13C variation in glucose. Plant Cell Environ 34, 1104-1112.
16. Guerard, F., Petriacq, P., Gakiere, B., and Tcherkez, G. (2011). Liquid chromatography/time-of-flight mass spectrometry for the analysis of plant samples : A method for simultaneous screening of common cofactors or nucleotides and application to an engineered plant line. Plant Physiol Biochem 49, 1117-25.
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20. Virlouvet, L., Jacquemot, M.P., Gerentes, D., Corti, H., Bouton, S., Gilard, F., Valot, B., Trouverie, J., Tcherkez, G., Falque, M., Damerval, C., Rogowsky, P., Perez, P., Noctor, G., Zivy, M., and Coursol, S. (2011). The ZmASR1 protein influences branched-chain amino acid biosynthesis and maintains kernel yield in maize under water-limited conditions. Plant Physiol 157, 917-936.
21. Djebbar, R., Rzigui, T., Petriacq, P., Mauve, C., Priault, P., Fresneau, C., De Paepe, M., Florez-Sarasa, I., Benhassaine-Kesri, G., Streb, P., Gakiere, B., Cornic, G., and De Paepe, R. (2012). Respiratory complex I deficiency induces drought tolerance by impacting leaf stomatal and hydraulic conductances. Planta 235, 603-614.
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23. Gilbert, A., Silvestre, V., Robins, R.J., Remaud, G.S., and Tcherkez, G. (2012). Biochemical and physiological determinants of intramolecular isotope patterns in sucrose from C3, C4 and CAM plants accessed by isotopic 13C NMR spectrometry : a viewpoint. Natural Product Reports 29, 476-486.
24. Halter, D., Goulhen-Chollet, F., Gallien, S., Casiot, C., Hamelin, J., Gilard, F., Heintz, D., Schaeffer, C., Carapito, C., Van Dorsselaer, A., Tcherkez, G., Arsene-Ploetze, F., and Bertin, P.N. (2012). In situ proteo-metabolomics reveals metabolite secretion by the acid mine drainage bio-indicator, Euglena mutabilis. Isme Journal 6, 1391-1402.
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26. Petriacq, P., de Bont, L., Hager, J., Didierlaurent, L., Mauve, C., Guerard, F., Noctor, G., Pelletier, S., Renou, J.P., Tcherkez, G., and Gakiere, B. (2012). Inducible NAD overproduction in Arabidopsis alters metabolic pools and gene expression correlated with increased salicylate content and resistance to Pst-AvrRpm1. Plant J 70, 650-665.
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29. Tcherkez, G., Mahe, A., Guerard, F., Boex-Fontvieille, E.R., Gout, E., Lamothe, M., Barbour, M.M., and Bligny, R. (2012). Short-term effects of CO2 and O2 on citrate metabolism in illuminated leaves. Plant Cell Environ 35, 2208-2220.
30. Aranjuelo, I., Tcherkez, G., Molero, G., Gilard, F., Avice, J.C., Nogués, S. (2013). Concerted changes in N and C primary metabolism in alfalfa (Medicago sativa) under water restriction. J Exp Bot 64, 885-897.
31. Boex-Fontvieille, E., Gauthier, P., Gilard, F., Hodges, M., and Tcherkez, G. (2013) A new anaplerotic respiratory pathway involving lysine biosynthesis in isocitrate dehydrogenase-deficient Arabidopsis mutants. New Phytol In press.
32. Boex-Fontvieille, E., Daventura, M., Jossier, M., Zivy, M., Hodges, M., and Tcherkez, G. (2013) Photosynthetic control of Arabidopsis leaf cytoplasmic translation initiation by protein phosphorylation. PlosOne In press.
33. Gauthier, P.P., Lamothe, M., Mahe, A., Molero, G., Nogues, S., Hodges, M., and Tcherkez, G. (2013). Metabolic origin of delta(15)N values in nitrogenous compounds from Brassica napus L. leaves. Plant Cell Environ 36, 128-137.
34. Gaufichon, L., Masclaux-Daubresse, C., Tcherkez, G., Reisdorf-Cren, M., Sakakibara, Y., Hase, T., Clement, G., Avice, J.C., Grandjean, O., Marmagne, A., Boutet-Mercey, S., Azzopardi, M., Soulay, F., and Suzuki, A. (2013). Arabidopsis thaliana ASN2 encoding asparagine synthetase is involved in the control of nitrogen assimilation and export during vegetative growth. Plant Cell Environ 36, 328-342.
35. Guérinier, T., Millan, L., Crozet, P., Oury, C., Rey, F., Valot, B., Mathieu, C., Vidal, J., Hodges, M., Thomas, M., Glab, N. (2013). Phosphorylation of p27KIP1 homologs KRP6 and 7 by SNF1−Related protein Kinase−1 links plant energy homeostasis and cell proliferation. Plant J In press.
36. Haili, N., Arnal, N., Quadrado, M., Amiar, S., Tcherkez, G., Dahan, J., Briozzo, P., Colas des Francs-Small, C., Vrielynck, N., and Mireau, H. (2013). The pentatricopeptide repeat MTSF1 protein stabilizes the nad4 mRNA in Arabidopsis mitochondria. Nucleic Acids Res In press. 37. Hodges, M., Jossier, M., Boex-Fontvieille, E., and Tcherkez, G. (2013). Protein phosphorylation and photorespiration. Plant Biol In press.
38. Mondy, S., Lenglet, A., Cosson, V., Pelletier, S., Pateyron, S., Gilard, F., Scholte, M., Brocard, L., Couzigou, J.M., Tcherkez, G., Pean, M., and Ratet, P. (2013). GOLLUM [FeFe]-hydrogenase-like proteins are essential for plant development in normoxic conditions and modulate energy metabolism. Plant Cell Environ In press.
39. Peuke, A.D., Gessler, A., and Tcherkez, G. (2013). Experimental Evidence for Diel Delta n-Patterns in Different Tissues, Xylem and Phloem Saps of Castor Bean (Ricinus Communis L.). Plant Cell Environ In press.
40. Tcherkez, G. (2013). Modelling the reaction mechanism of ribulose-1,5-bisphosphate carboxylase/ oxygenase and consequences for kinetic parameters. Plant Cell Environ. In press.
41. Tcherkez, G. (2013). Is the recovery of (photo) respiratory CO2 and intermediates minimal ? New Phytol 198, 334-338.
42. Tcherkez, G.G., Bathellier, C., Stuart-Williams, H., Whitney, S., Gout, E., Bligny, R., Badger, M., and Farquhar, G.D. (2013). D2O solvent isotope effects suggest uniform energy barriers in ribulose-1,5-bisphosphate carboxylase/oxygenase catalysis. Biochemistry 52, 869-877.
43. Vieira, P., Escudero, C., Rodiuc, N., Boruc, J., Russinova, E., Glab, N., Mota, M., De Veylder, L., Abad, P., Engler, G., and de Almeida Engler, J. (2013). Ectopic expression of Kip-related proteins restrains root-knot nematode-feeding site expansion. New Phytol 199, 505-519.