×

zbMATH — the first resource for mathematics

Modeling the diversion of primary carbon flux into secondary metabolism under variable nitrate and light/dark conditions. (English) Zbl 1343.92291
Summary: In plants, the partitioning of carbon resources between growth and defense is detrimental for their development. From a metabolic viewpoint, growth is mainly related to primary metabolism including protein, amino acid and lipid synthesis, whereas defense is based notably on the biosynthesis of a myriad of secondary metabolites. Environmental factors, such as nitrate fertilization, impact the partitioning of carbon resources between growth and defense. Indeed, experimental data showed that a shortage in the nitrate fertilization resulted in a reduction of the plant growth, whereas some secondary metabolites involved in plant defense, such as phenolic compounds, accumulated. Interestingly, sucrose, a key molecule involved in the transport and partitioning of carbon resources, appeared to be under homeostatic control. Based on the inflow/outflow properties of sucrose homeostatic regulation we propose a global model on how the diversion of the primary carbon flux into the secondary phenolic pathways occurs at low nitrate concentrations. The model can account for the accumulation of starch during the light phase and the sucrose remobilization by starch degradation during the night. Day-length sensing mechanisms for variable light-dark regimes are discussed, showing that growth is proportional to the length of the light phase. The model can describe the complete starch consumption during the night for plants adapted to a certain light/dark regime when grown on sufficient nitrate and can account for an increased accumulation of starch observed under nitrate limitation.
MSC:
92C80 Plant biology
92C40 Biochemistry, molecular biology
Software:
LSODE
PDF BibTeX XML Cite
Full Text: DOI
References:
[1] Abro, M. A.; Lecompte, F.; Bryone, F.; Nicot, P. C., Nitrogen fertilization of the host plant influences production and pathogenicity of botrytis cinerea secondary inoculum, Phytopathology, 103, 3, 261-267, (2013)
[2] Baudry, A.; Caboche, M.; Lepiniec, L., TT8 controls its own expression in a feedback regulation involving TTG1 and homologous MYB and bhlh factors, allowing a strong and cell-specific accumulation of flavonoids in arabidopsis thaliana, Plant J., 46, 5, 768-779, (2006)
[3] Bryant, J. P.; Chapin, F. S.; Klein, D. R., Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory, Oikos, 357-368, (1983)
[4] Bünning, E., The physiological clock, Circadian rhythms and biological chronometry, (1973), Springer-Verlag Berlin
[5] Caldana, C.; Li, Y.; Leisse, A.; Zhang, Y.; Bartholomaeus, L.; Fernie, A. R.; Willmitzer, L.; Giavalisco, P., Systemic analysis of inducible target of rapamycin mutants reveal a general metabolic switch controlling growth in arabidopsis thaliana, Plant J., 73, 6, 897-909, (2013)
[6] Cannon, W., Organization for physiological homeostasis, Physiol. Rev., 9, 399-431, (1929)
[7] Deprost, D.; Yao, L.; Sormani, R.; Moreau, M.; Leterreux, G.; Nicolai¨, M.; Bedu, M.; Robaglia, C.; Meyer, C., The arabidopsis TOR kinase links plant growth, yield, stress resistance and mrna translation, EMBO Rep., 8, 9, 864-870, (2007)
[8] Dijkwel, P. P.; Kock, P. A.; Bezemer, R.; Weisbeek, P. J.; Smeekens, S. C., Sucrose represses the developmentally controlled transient activation of the plastocyanin gene in arabidopsis thaliana seedlings, Plant Physiol., 110, 2, 455-463, (1996)
[9] Dobrenel, T.; Marchive, C.; Sormani, R.; Moreau, M.; Mozzo, M.; Montané, M.-H.; Menand, B.; Robaglia, C.; Meyer, C., Regulation of plant growth and metabolism by the TOR kinase, Biochem. Soc. Trans., 39, 2, 477-481, (2011)
[10] Doré, T.; Makowski, D.; Malézieux, E.; Munier-Jolain, N.; Tchamitchian, M.; Tittonell, P., Facing up to the paradigm of ecological intensification in agronomyrevisiting methods, concepts and knowledge, Eur. J. Agron., 34, 4, 197-210, (2011)
[11] Drengstig, T.; Jolma, I.; Ni, X.; Thorsen, K.; Xu, X.; Ruoff, P., A basic set of homeostatic controller motifs, Biophys. J., 103, 9, 2000-2010, (2012)
[12] Drengstig, T.; Ni, X.; Thorsen, K.; Jolma, I.; Ruoff, P., Robust adaptation and homeostasis by autocatalysis, J. Phys. Chem. B, 116, 18, 5355-5363, (2012)
[13] Dubos, C.; Le Gourrierec, J.; Baudry, A.; Huep, G.; Lanet, E.; Debeaujon, I.; Routaboul, J.-M.; Alboresi, A.; Weisshaar, B.; Lepiniec, L., MYBL2 is a new regulator of flavonoid biosynthesis in arabidopsis thaliana, Plant J., 55, 6, 940-953, (2008)
[14] Eimert, K.; Wang, S.-M.; Lue, W.; Chen, J., Monogenic recessive mutations causing both late floral initiation and excess starch accumulation in arabidopsis, Plant Cell, 7, 10, 1703-1712, (1995)
[15] Endler, A.; Meyer, S.; Schelbert, S.; Schneider, T.; Weschke, W.; Peters, S. W.; Keller, F.; Baginsky, S.; Martinoia, E.; Schmidt, U. G., Identification of a vacuolar sucrose transporter in barley and arabidopsis mesophyll cells by a tonoplast proteomic approach, Plant Physiol., 141, 1, 196-207, (2006)
[16] Farquhar, G.; von Caemmerer, S.v.; Berry, J., A biochemical model of photosynthetic CO_2 assimilation in leaves of C_3 species, Planta, 149, 1, 78-90, (1980)
[17] Feugier, F. G.; Satake, A., Dynamical feedback between Circadian clock and sucrose availability explains adaptive response of starch metabolism to various photoperiods, Front. Plant Sci., 3, 305, (2013)
[18] Fritz, C.; Palacios-Rojas, N.; Feil, R.; Stitt, M., Regulation of secondary metabolism by the carbon-nitrogen status in tobacconitrate inhibits large sectors of phenylpropanoid metabolism, Plant J., 46, 4, 533-548, (2006)
[19] Garner, W. W.; Allard, H. A., Effect of the relative length of day and night and other factors of the environment on growth and reproduction in plants, J. Agric. Res., 18, 553-606, (1920)
[20] Geiger, M.; Haake, V.; Ludewig, F.; Sonnewald, U.; Stitt, M., The nitrate and ammonium nitrate supply have a major influence on the response of photosynthesis, carbon metabolism, nitrogen metabolism and growth to elevated carbon dioxide in tobacco, Plant Cell Environ., 22, 10, 1177-1199, (1999)
[21] Gibon, Y.; Bläsing, O. E.; Palacios-Rojas, N.; Pankovic, D.; Hendriks, J. H.; Fisahn, J.; Höhne, M.; Günther, M.; Stitt, M., Adjustment of diurnal starch turnover to short daysdepletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period, Plant J., 39, 6, 847-862, (2004)
[22] Glynn, C.; Herms, D. A.; Orians, C. M.; Hansen, R. C.; Larsson, S., Testing the growth-differentiation balance hypothesisdynamic responses of willows to nutrient availability, New Phytol., 176, 3, 623-634, (2007)
[23] Hanson, J.; Hanssen, M.; Wiese, A.; Hendriks, M. M.; Smeekens, S., The sucrose regulated transcription factor bzip11 affects amino acid metabolism by regulating the expression of ASPARAGINE SYNTHETASE1 and PROLINE DEHYDROGENASE2, Plant J., 53, 6, 935-949, (2008)
[24] Herms, D. A.; Mattson, W. J., The dilemma of plantsto grow or defend, Q. Rev. Biol., 67, 3, 283-335, (1992)
[25] Huang, Y.; Drengstig, T.; Ruoff, P., Integrating fluctuating nitrate uptake and assimilation to robust homeostasis, Plant Cell Environ., 35, 917-928, (2012)
[26] Huber, S., Huber, J., McMichael, R., 1992. The regulation of sucrose synthesis in leaves. In: Pollock, C., Farrar, J., Gordon, A. (Eds.), Carbon Partitioning: Within and Between Organisms. Bios Scientific Publishers, Oxford, pp. 1-26.
[27] Kallarackal, J.; Bauer, S. N.; Nowak, H.; Hajirezaei, M.-R.; Komor, E., Diurnal changes in assimilate concentrations and fluxes in the phloem of castor Bean (ricinus communis L.) and tansy (tanacetum vulgare L.), Planta, 236, 1, 209-223, (2012)
[28] Kingston-Smith, A. H.; Bollard, A. L.; Minchin, F. R, Stress-induced changes in protease composition are determined by nitrogen supply in non-nodulating white clover, J. Exp. Bot., 56, 412, 745-753, (2005)
[29] Koricheva, J.; Larsson, S.; Haukioja, E.; Keinänen, M., Regulation of woody plant secondary metabolism by resource availabilityhypothesis testing by means of meta-analysis, Oikos, 212-226, (1998)
[30] Larbat, R.; Le Bot, J.; Bourgaud, F.; Robin, C.; Adamowicz, S., Organ-specific responses of tomato growth and phenolic metabolism to nitrate limitation, Plant Biol., 14, 5, 760-769, (2012)
[31] Le Bot, J.; Bénard, C.; Robin, C.; Bourgaud, F.; Adamowicz, S., The ‘trade-off’ between synthesis of primary and secondary compounds in Young tomato leaves is altered by nitrate nutritionexperimental evidence and model consistency, J. Exp. Bot., 60, 4301-4314, (2009)
[32] Lillo, C.; Lea, U. S.; Ruoff, P., Nutrient depletion as a key factor for manipulating gene expression and product formation in different branches of the flavonoid pathway, Plant Cell Environ., 31, 5, 587-601, (2008)
[33] Loomis, W., 1932. Growth-differentiation balance vs. carbohydrate-nitrogen ratio. Proc. Am. Soc. Hortic. Sci. 29, 240-245.
[34] Lu, Y.; Gehan, J. P.; Sharkey, T. D., Daylength and Circadian effects on starch degradation and maltose metabolism, Plant Physiol., 138, 4, 2280-2291, (2005)
[35] Marschner, P., Marschner’s mineral nutrition of higher plants, (2012), Academic Press, Amsterdam
[36] Massad, T. J.; Dyer, L. A.; Vega, G., Costs of defense and a test of the carbon-nutrient balance and growth-differentiation balance hypotheses for two co-occurring classes of plant defense, PLOS One, 7, 10, e47554, (2012)
[37] Matsui, K.; Umemura, Y.; Ohme-Takagi, M., Atmybl2, a protein with a single myb domain, acts as a negative regulator of anthocyanin biosynthesis in arabidopsis, Plant J., 55, 6, 954-967, (2008)
[38] McKey, D., Adaptive patterns in alkaloid physiology, Am. Nat., 305-320, (1974)
[39] Menand, B.; Desnos, T.; Nussaume, L.; Berger, F.; Bouchez, D.; Meyer, C.; Robaglia, C., Expression and disruption of the arabidopsis TOR (target of rapamycin) gene, Proc. Natl. Acad. Sci. USA, 99, 9, 6422-6427, (2002)
[40] Miller, A. J.; Smith, S. J., The mechanism of nitrate transport across the tonoplast of barley root cells, Planta, 187, 4, 554-557, (1992)
[41] Miller, A. J.; Smith, S. J., Cytosolic nitrate ion homeostasiscould it have a role in sensing nitrogen status?, Ann. Bot., 101, 4, 485-489, (2008)
[42] Mooney, K. A.; Halitschke, R.; Kessler, A.; Agrawal, A. A., Evolutionary trade-offs in plants mediate the strength of trophic cascades, Science, 327, 5973, 1642-1644, (2010)
[43] Nemie-Feyissa, D.; Olafsdottir, S. M.; Heidari, B.; Lillo, C., Nitrogen depletion and small R3-MYB transcription factors affecting anthocyanin accumulation in arabidopsis leaves, Phytochemistry, 98, 34-40, (2014)
[44] Nguyen, P. M.; Niemeyer, E. D., Effects of nitrogen fertilization on the phenolic composition and antioxidant properties of basil (ocimum basilicum L.), J. Agric. Food Chem., 56, 18, 8685-8691, (2008)
[45] Ni, X.; Drengstig, T.; Ruoff, P., The control of the controllermolecular mechanisms for robust perfect adaptation and temperature compensation, Biophys. J., 97, 1244-1253, (2009)
[46] Peuke, A.; Rokitta, M.; Zimmermann, U.; Schreiber, L.; Haase, A., Simultaneous measurement of water flow velocity and solute transport in xylem and phloem of adult plants of ricinus communis over a daily time course by nuclear magnetic resonance spectrometry, Plant Cell Environ., 24, 5, 491-503, (2001)
[47] Pokhilko, A.; Ebenhöh, O., Mathematical modelling of diurnal regulation of carbohydrate allocation by osmo-related processes in plants, J. R. Soc. Interface, 12, 104, 20141357, (2015)
[48] Pokhilko, A.; Flis, A.; Sulpice, R.; Stitt, M.; Ebenhöh, O., Adjustment of carbon fluxes to light conditions regulates the daily turnover of starch in plantsa computational model, Mol. BioSyst., 10, 3, 613-627, (2014)
[49] Pretorius, J.; Nieuwoudt, D.; Eksteen, D., Sucrose synthesis and translocation in zea mays L. during early growth, when subjected to N and K deficiency, S. Afr. J. Plant Soil, 16, 4, 173-179, (1999)
[50] Radhakrishnan, K., Hindmarsh, A., 1993. Description and Use of LSODE, the Livermore Solver for Ordinary Differential Equations. NASA Reference Publication 1327, Lawrence Livermore National Laboratory Report UCRL-ID-113855. National Aeronautics and Space Administration, Lewis Research Center, Cleveland, OH 44135-3191.
[51] Romberger, J.A., 1963. Meristems, Growth, and Development in Woody Plants: An Analytical Review of Anatomical, Physiological, and Morphogenic Aspects. No. 1293. US Government Printing Office.
[52] Royer, M.; Larbat, R.; Le Bot, J.; Adamowicz, S.; Robin, C., Is the C:N ratio a reliable indicator of C allocation to primary and defence-related metabolisms in tomato?, Phytochemistry, 88, 25-33, (2013)
[53] Rubin, G.; Tohge, T.; Matsuda, F.; Saito, K.; Scheible, W.-R., Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in arabidopsis, Plant Cell, 21, 11, 3567-3584, (2009)
[54] Scheible, W.-R.; Lauerer, M.; Schulze, E.-D.; Caboche, M.; Stitt, M., Accumulation of nitrate in the shoot acts as a signal to regulate shoot-root allocation in tobacco, Plant J., 11, 4, 671-691, (1997)
[55] Scheible, W.-R.; Morcuende, R.; Czechowski, T.; Fritz, C.; Osuna, D.; Palacios-Rojas, N.; Schindelasch, D.; Thimm, O.; Udvardi, M. K.; Stitt, M., Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of arabidopsis in response to nitrogen, Plant Physiol., 136, 1, 2483-2499, (2004)
[56] Scialdone, A.; Howard, M., How plants manage food reserves at nightquantitative models and open questions, Front. Plant Sci., 6, 204, (2015)
[57] Scialdone, A.; Mugford, S. T.; Feike, D.; Skeffington, A.; Borrill, P.; Graf, A.; Smith, A. M.; Howard, M., Arabidopsis plants perform arithmetic division to prevent starvation at night, Elife, 2, e00669, (2013)
[58] Seaton, D. D.; Ebenhöh, O.; Millar, A. J.; Pokhilko, A., Regulatory principles and experimental approaches to the Circadian control of starch turnover, J. R. Soc. Interface, 11, 91, 20130979, (2014)
[59] Smith, A. M.; Stitt, M., Coordination of carbon supply and plant growth, Plant Cell Environ., 30, 9, 1126-1149, (2007)
[60] Smith, J. A.C.; Milburn, J. A., Phloem transport, solute flux and the kinetics of sap exudation in ricinus communis L, Planta, 148, 1, 35-41, (1980)
[61] Solfanelli, C.; Poggi, A.; Loreti, E.; Alpi, A.; Perata, P., Sucrose-specific induction of the anthocyanin biosynthetic pathway in arabidopsis, Plant Physiol., 140, 2, 637-646, (2006)
[62] Stamp, N., Out of the quagmire of plant defense hypotheses, Q. Rev. Biol., 78, 1, 23-55, (2003)
[63] Stamp, N., Can the growth-differentiation balance hypothesis be tested rigorously?, Oikos, 107, 2, 439-448, (2004)
[64] Stewart, A.; Chapman, W.; Jenkins, G.; Graham, I.; Martin, T.; Crozier, A., The effect of nitrogen and phosphorus deficiency on flavonol accumulation in plant tissues, Plant Cell Environ., 24, 11, 1189-1197, (2001)
[65] Stitt, M.; Zeeman, S. C., Starch turnoverpathways, regulation and role in growth, Curr. Opin. Plant Biol., 15, 3, 282-292, (2012)
[66] Taiz, L.; Zeiger, E.; Møller, I. M.; Murphy, A. S., Plant physiology and development, (2015), Sinauer Sunderland
[67] Teng, S.; Keurentjes, J.; Bentsink, L.; Koornneef, M.; Smeekens, S., Sucrose-specific induction of anthocyanin biosynthesis in arabidopsis requires the MYB75/PAP1 gene, Plant Physiol., 139, 4, 1840-1852, (2005)
[68] Thorsen, K., Drengstig, T., Ruoff, P., 2013. Control theoretic properties of physiological controller motifs. In: ICSSE 2013, IEEE International Conference on System Science and Engineering. Budapest, pp. 165-170.
[69] Tognetti, J. A.; Horacio, P.; Martinez-Noel, G., Sucrose signaling in plantsa world yet to be explored, Plant Signal. Behav., 8, 3, e23316, (2013)
[70] Vidal, E. A.; Gutierrez, R. A., A systems view of nitrogen nutrient and metabolite responses in arabidopsis, Curr. Opin. Plant Biol., 11, 5, 521-529, (2008)
[71] Von Caemmerer, S.; Farquhar, G., Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves, Planta, 153, 4, 376-387, (1981)
[72] Wilkie, J.; Johnson, M.; Reza, K., Control engineering. an introductory course, (2002), Palgrave New York
[73] Wind, J.; Smeekens, S.; Hanson, J., Sucrosemetabolite and signaling molecule, Phytochemistry, 71, 14, 1610-1614, (2010)
[74] Xu, G.; Fan, X.; Miller, A. J., Plant nitrogen assimilation and use efficiency, Annu. Rev. Plant Biol., 63, 153-182, (2012)
[75] Yi, T.; Huang, Y.; Simon, M.; Doyle, J., Robust perfect adaptation in bacterial chemotaxis through integral feedback control, Proc. Natl. Acad. Sci. USA, 97, 9, 4649-4653, (2000)
[76] Zhang, X.; Myers, A. M.; James, M. G., Mutations affecting starch synthase III in arabidopsis alter leaf starch structure and increase the rate of starch synthesis, Plant Physiol., 138, 2, 663-674, (2005)
[77] Züst, T., Joseph, B., Shimizu, K.K., Kliebenstein, D.J., Turnbull, L.A., 2011. Using knockout mutants to reveal the growth costs of defensive traits. Proc. R. Soc. Lond. B: Biol. Sci., http://dx.doi.org/10.1098/rspb.2010.2475.
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. It attempts to reflect the references listed in the original paper as accurately as possible without claiming the completeness or perfect precision of the matching.