Artículo

Peluffo, L.; Lia, V.; Troglia, C.; Maringolo, C.; Norma, P.; Escande, A.; Esteban Hopp, H.; Lytovchenko, A.; Fernie, A.R.; Heinz, R.; Carrari, F. "Metabolic profiles of sunflower genotypes with contrasting response to Sclerotinia sclerotiorum infection" (2010) Phytochemistry. 71(1):70-80
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Abstract:

We report a comprehensive primary metabolite profiling of sunflower (Helianthus annuus) genotypes displaying contrasting behavior to Sclerotinia sclerotiorum infection. Applying a GC-MS-based metabolite profiling approach, we were able to identify differential patterns involving a total of 63 metabolites including major and minor sugars and sugar alcohols, organic acids, amino acids, fatty acids and few soluble secondary metabolites in the sunflower capitulum, the main target organ of pathogen attack. Metabolic changes and disease incidence of the two contrasting genotypes were determined throughout the main infection period (R5.2-R6). Both point-by-point and non-parametric statistical analyses showed metabolic differences between genotypes as well as interaction effects between genotype and time after inoculation. Network correlation analyses suggested that these metabolic changes were synchronized in a time-dependent manner in response to the pathogen. Concerted differential metabolic changes were detected to a higher extent in the susceptible, rather than the resistant genotype, thereby allowing differentiation of modules composed by intermediates of the same pathway which are highly interconnected in the susceptible line but not in the resistant one. Evaluation of these data also demonstrated a genotype specific regulation of distinct metabolic pathways, suggesting the importance of detection of metabolic patterns rather than specific metabolite changes when looking for metabolic markers differentially responding to pathogen infection. In summary, the GC-MS strategy developed in this study was suitable for detection of differences in carbon primary metabolism in sunflower capitulum, a tissue which is the main entry point for this and other pathogens which cause great detrimental impact on crop yield. © 2009 Elsevier Ltd. All rights reserved.

Registro:

Documento: Artículo
Título:Metabolic profiles of sunflower genotypes with contrasting response to Sclerotinia sclerotiorum infection
Autor:Peluffo, L.; Lia, V.; Troglia, C.; Maringolo, C.; Norma, P.; Escande, A.; Esteban Hopp, H.; Lytovchenko, A.; Fernie, A.R.; Heinz, R.; Carrari, F.
Filiación:Instituto de Biotecnología, CICVyA, Instituto Nacional de Tecnología Agropecuaria (IB-INTA), Argentina
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina
Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina
Unidad integrada INTA Balcarce-Universidad Nacional de Mar del Plata, Argentina
Max-Planck-Institut für Molekulare Pflanzenphysiologie, Am Mühlenberg 1, 14476 Postdam, Golm, Germany
Palabras clave:Compositae; Head rot disease; Helianthus annuus L.; Metabolite profiling; Sink organ metabolism; Sunflower; Asteraceae; Helianthus; Helianthus annuus; Sclerotinia sclerotiorum
Año:2010
Volumen:71
Número:1
Página de inicio:70
Página de fin:80
DOI: http://dx.doi.org/10.1016/j.phytochem.2009.09.018
Título revista:Phytochemistry
Título revista abreviado:Phytochemistry
ISSN:00319422
CODEN:PYTCA
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00319422_v71_n1_p70_Peluffo

Referencias:

  • Abood, J.K., Lösel, D.M., Changes in carbohydrate composition of cucumber leaves during the development of powdery mildew infection (2003) Plant Pathol., 52, pp. 256-265
  • Aebi, H., Catalase in vitro (1984) Meth. Enzymol., 105, pp. 121-125
  • Al-Chaarani, G.R., Roustaee, A., Gentzbittel, L., Mokrani, L., Barrault, G., Dechamp-Guillaume, G., Sarrafi, A., A QTL analysis of sunflower partial resistance to downy mildew (Plasmopara halstedii) and black stem (Phoma macdonaldii) by the use of recombinant inbred lines (RILs) (2002) Theor. Appl. Genet., 104, pp. 490-496
  • Al-Chaarani, G.R., Gentzbittel, L., Huang, X.Q., Sarrafi, A., Genotypic variation and identification of QTLs of agronomic traits, using AFLP and SSR markers in RILs of sunflower (Helianthus annuus L.) (2004) Theor. Appl. Genet., 109, pp. 1353-1360
  • Baxter, C.J., Redestig, H., Schauer, N., Repsilber, D., Patil, K.R., Nielsen, J., Selbig, J., Sweetlove, L.J., The metabolic response of heterotrophic Arabidopsis cells to oxidative stress (2007) Plant Physiol., 143, pp. 312-325
  • Bednarek, P., Schneider, B., Svatos, A., Oldham, L.J., Hahlbrock, K., Structural complexity, differential response to infection, and tissue specificity of indolic and phenylpropanoid secondary metabolism in Arabidopsis roots (2005) Plant Physiol., 38, pp. 1058-1070
  • Berger, S., Sinha, A.K., Roitsch, T., Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions (2007) J. Ex. Bot., 58, pp. 4019-4026
  • Bert, P.F., Jouan, I., De Labrouhe, D.T., Serre, F., Nicolas, P., Vear, F., Comparative genetic analysis of quantitative traits in sunflower (Helianthus annuus L.) 1. QTL involved in resistance to Sclerotinia sclerotiorum and Diaporthe helianthi (2002) Theor. Appl. Genet., 105, pp. 985-993
  • Bert, P.F., Dechamp-Guillaume, G., Serre, F., Jouan, I., Tourvieille de Labrouhe, D., Nicolas, P., Vear, F., Comparative genetic analysis of quantitative traits in sunflower (Helianthus annuus L.) 3. Characterisation of QTL involved in resistance to Sclerotinia sclerotiorum and Phoma macdonaldi (2004) Theor. Appl. Genet., 109, pp. 865-874
  • Boland, G.J., Hall, R., Index of plant hosts of Sclerotinia sclerotiorum (1994) Can. J. Plant Pathol., 16, pp. 93-108
  • Campbell, C.L., Madden, L.V., (1990) Introduction to Plant Disease Epidemiology, , John Willey and Sons, New York
  • Carter, C., Thornburg, R.W., Tobacco nectarin I - purification and characterization as a germin-like, manganese superoxide dismutase implicated in the defense of floral reproductive tissues (2000) J. Biol. Chem., 275, pp. 36726-36733
  • Cessna, S.G., Sears, V.E., Dickman, M.B., Low, P.S., Oxalic acid, a pathogenicity factor for Sclerotinia sclerotiorum, suppresses the oxidative burst of the host plant (2000) Plant Cell, 12, pp. 2191-2200
  • Chandra-Shekara, A.C., Venugopal, S.C., Barman, S.R., Kachroo, A., Kachroo, P., Plastidial fatty acid levels regulate resistance gene-dependent defense signaling in Arabidopsis (2007) Proc. Natl. Acad. Sci. USA, 104, pp. 7277-7282
  • Chou, H.-M., Bundock, N., Rolfe, S.A., Scholes, J.D., Infection of Arabidopsis thaliana leaves with Albugo Candida (white blister rust) causes a reprogramming of host metabolism (2000) Mol. Plant Pathol., 1, pp. 99-113
  • Christensen, A.B., Thordal-Christensen, H., Zimmermann, G., Gjetting, T., Lyngkjaer, M.F., Dudler, R., Schweizer, P., The germin-like protein GLP4 exhibits superoxide dismutase activity and is an important component of quantitative resistance in wheat and barley (2004) MPMI, 17, pp. 109-117
  • Chung, H.S., Koo, A.J.K., Gao, X., Jayanty, S., Thines, B., Jones, A.D., Howe, G.A., Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory (2008) Plant Physiol., 146, pp. 952-964
  • Depuydt, S., Trenkamp, S., Fernie, A.R., Elftieh, S., Renou, J.-P., Vuylsteke, M., Holsters, M., Vereecke, D., An integrated genomics approach to define niche establishment by Rhodococcus fascians (2009) Plant Physiol., 149, pp. 1366-1386
  • Desbrosses, G., Kopka, J., Udvardi, M.K., Lotus japonicus metabolic profiling development of gas chromatography-mass spectrometry resources for the study of plant-microbe interactions (2005) Plant Physiol., 137, pp. 1302-1318
  • Divon, H.H., Ziv, C., Davydov, O., Yarden, O., Fluhr, R., The global nitrogen regulator, FNR1, regulates fungal nutrition-genes and fitness during Fusarium oxysporum pathogenesis (2006) Mol. Plant Pathol., 7, pp. 485-497
  • Dumas, B., Sailland, A., Cheviet, J.P., Freyssinet, G., Pallett, K., Identification of barley oxalate oxidase as a germin-like protein (1993) Comptes Rendus de l'Academie des Sciences Serie III-Sciences de la Vie, 316, pp. 793-798
  • Dutton, M.V., Evans, C.S., Oxalate production by fungi: its role in pathogenicity and ecology in the soil environment (1996) Can. J. Microbiol., 42, pp. 881-895
  • Escande, A.R., Laich, F.S., Pedraza, M.V., Field testing of honeybee-dispersed Trichoderma spp. to manage sunflower head rot (Sclerotinia sclerotiorum) (2002) Plant Pathol., 51, pp. 346-351
  • Fernie, A.R., The future of metabolic phytochemistry: larger numbers of metabolites, higher resolution, greater understanding (2007) Phytochemistry, 68, pp. 2861-2880
  • Fernie, A.R., Trethewey, R.N., Krotzky, A.J., Willmitzer, L., Metabolite profiling: from diagnostics to systems biology (2004) Nat. Rev. Mol. Cell Biol., 5, pp. 1-7
  • Fiehn, O., Kopka, J., Dörmann, P., Altmann, T., Trethewey, R.N., Willmitzer, L., Metabolite profiling for plant functional genomics (2000) Nat. Biotechnol., 18, pp. 1157-1161
  • Fotopoulos, V., Gilbert, M.J., Pittman, J.K., Marvier, A.C., Buchanan, A.J., Sauer, N., Hall, J.L., Williams, L.E., The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atβfruct1, are induced in arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum (2003) Plant Physiol., 132, pp. 821-829
  • Gentzbittel, L., Mouzeyar, S., Badaoui, S., Mestries, E., Vear, F., Tourvieille De Labrouhe, D., Nicolas, P., Cloning of molecular markers for disease resistance in sunflower, Helianthus annuus L (1998) Theor. Appl. Genet., 96, pp. 519-525
  • Godfrey, D., Able, A.J., Dry, I.B., Induction of a grapevine germin-like protein (VvGLP3) gene is closely linked to the site of Erysiphe necator infection: a possible role in defense? (2007) MPMI, 20 (9), pp. 1112-1125
  • Godoy, G., Steadman, J.R., Dickman, M.B., Dam, R., Use of mutants to demonstrate the role of oxalic acid in pathogenicity of Sclerotinia sclerotiorum on Phaseolus vulgaris (1990) Physiol. Mol. Plant Pathol., 37, pp. 179-191
  • Guimerà, R., Nunes Amaral, L.A., Functional cartography of complex metabolic networks (2005) Nature, 433, pp. 895-900
  • Hall, J.L., Williams, L.E., Assimilate transport and partitioning in fungal biotrophic interactions (2000) Aust. J. Plant Pathol., 27, pp. 549-559
  • Hu, X., Bidney, D.L., Yalpani, N., Duvick, J.P., Crasta, O., Folkerts, O., Lu, G., Overexpression of a gene encoding hydrogen peroxide-generating oxalate oxidase evokes defense responses in sunflower (2003) Plant Physiol., 133, pp. 170-181
  • Jobic, C., Boisson, A.M., Gout, E., Rascle, C., Fevre, M., Cotton, P., Bligny, R., Metabolic processes and carbon nutrient exchanges between host and pathogen sustain the disease development during sunflower infection by Sclerotinia sclerotiorum (2007) Planta, 226, pp. 251-265
  • Jubault, M., Hamon, C., Gravot, A., Lariagon, C., Delourme, R., Bouchereau, A., Manzanares-Dauleux, M.J., Differential regulation of root arginine catabolism and polyamine metabolism in clubroot-susceptible and partially resistant Arabidopsis genotypes (2008) Plant Physiol., 146, pp. 2008-2019
  • Kachroo, A., Daqi, F., Havens, W., Navarre, D., Kachroo, P., Ghabrial, S., An oleic acid-mediated pathway induces constitutive defense signaling and enhanced resistance to multiple pathogens in soybean (2008) Mol. Plant Microbe Interact., 21, pp. 564-575
  • Kachroo, A., Venugopal, S.C., Lapchyk, L., Falcone, D., Hildebrand, D., Kachroo, P., Oleic acid levels regulated by glycerolipid metabolism modulate defense gene expression in Arabidopsis (2004) Proc. Natl. Acad. Sci. USA, 101, pp. 5152-5157
  • Kiani, S.P., Talia, P., Maury, P., Grieu, P., Heinz, R., Perrault, A., Nishinakamasu, V., Sarrafi, A., Genetic analysis of plant water status and osmotic adjustment in recombinant inbred lines of sunflower under two water treatments (2007) Plant Sci., 172, pp. 773-787
  • Kim, K.S., Min, J.Y., Dickman, M., Oxalic acid an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development (2008) Mol. Plant Microbe Interact., 21, pp. 605-612
  • Kocal, N., Sonnewald, U., Sonnewald, S., Cell wall bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestros pv vesicatoria (2008) Plant Physiol., 148, pp. 1523-1536
  • Korkina, L.G., Phenylpropanoids as naturally occurring antioxidants: from plant defense to human health (2007) Cell Mol. Biol., 53, pp. 15-25
  • Lindon, J.C., Holmes, E., Bollard, M.E., Stanley, E.G., Nicholson, J.K., Metabonomics technologies and their applications in physiological monitoring, drug safety assessment and disease diagnosis (2004) Biomarkers, 9, pp. 1-31
  • Lipka, V., Dittgen, J., Bednarek, P., Bhat, R., Wiermer, M., Stein, M., Landtag, J., Scheel, D., Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis (2005) Science, 310, pp. 1180-1183
  • Lisec, J., Schauer, N., Kopka, J., Willmitzer, L., Fernie, A.R., Gas chromatography mass spectrometry-based metabolite profiling in plants (2006) Nat. Protoc., 1, pp. 387-396
  • Lytovchenko, A., Bieberich, K., Willmitzer, L., Fernie, A.R., Carbon assimilation and metabolism in potato leaves deficient in plastidial phosphoglucomutase (2002) Planta, 215, pp. 802-811
  • Maringolo, C., QTL Mapping to Resistance to Sclerotinia Head Rot of Sunflower (Sclerotinia sclerotiorum (Lib.) De Bary) (2007) Magister Scientiae, , Thesis. Facultad de Ciencias Agrarias. Universidad Nacional de Mar del Plata. INTA. Experimental Research Station Balcarce, Argentina
  • Mestries, E., Gentzbittel, L., Tourvieille De Labrouhe, D., Nicolas, P., Vear, F., Analyses of quantitative trait loci associated with resistance to Sclerotinia sclerotiorum in sunflowers (Helianthus annuus L.) using molecular markers (1998) Mol. Breed., 4, pp. 215-226
  • Meyer, R.C., Steinfath, M., Lisec, J., Becher, M., Witucka-Wall, H., Törjék, O., Fiehn, O., Altmann, T., The metabolic signature related to high plant growth rate in Arabidopsis thaliana (2007) Proc. Natl. Acad. Sci. USA, 104, pp. 4759-4764
  • Micic, Z., Hahn, V., Bauer, E., Melchinger, A.E., Knapp, S.J., Tang, S., Schon, C.C., Identification and validation of QTL for Sclerotinia midstalk rot resistance in sunflower by selective genotyping (2005) Theor. Appl. Genet., 111, pp. 233-242
  • Micic, Z., Hahn, V., Bauer, E., Schon, C.C., Knapp, S.J., Tang, S., Melchinger, A.E., QTL mapping of midstalk Sclerotinia - rot resistance in sunflower (2004) Theor. Appl. Genet., 109, pp. 1474-1484
  • Micic, Z., Hahn, V., Bauer, E., Schon, C.C., Melchinger, A.E., QTL mapping of resistance to Sclerotinia midstalk rot in RIL of sunflower population NDBLOSsel × CM625 (2005) Theor. Appl. Genet., 110, pp. 1490-1498
  • Mikkelsen, M.D., Halkier, B.A., Metabolic engineering of valine- and isoleucine-derived glucosinolates in Arabidopsis expressing CYP79D2 from cassava (2003) Plant Physiol., 131, pp. 773-779
  • Paniego, N., Heinz, R., Hopp, H.E., Sunflower (2006) Genome Mapping and Molecular Breeding Vol. II (Oilseeds), pp. 153-178. , Kole C. (Ed), Springer, Berlin, Heidelberg, Germany
  • Pedras, M.S., Zheng, Q.A., Gadagi, R.S., Rimmer, S.R., Phytoalexins and polar metabolites from the oilseeds canola and rapeseed: differential metabolic responses to the biotroph Albugo candida and to abiotic stress (2008) Phytochemistry, 69, pp. 894-910
  • Pedraza, M.V., (2005) Estudios tendientes al manejo integrado de la podredumbre húmeda del capítulo del girasol (Sclerotinia sclerotiorum), , PhD Thesis. Universidad Nacional de Mar del Plata. Facultad de Ciencias Agrarias Balcarce, 102p
  • Pereyra, V.R., Escande, A.R., (1994) Enfermedades del Girasol en la Argentina, Manual de Reconocimiento, , Instituto Nacional de Tecnologia Agropecuaria Sociedad Impresora Americana, Buenos Aires, Argentina
  • Prats, E., Bazzalo, M.E., León, A., Jorrín, J.V., Accumulation of soluble phenolic compounds in sunflower capitula correlates with resistance to Sclerotinia sclerotiorum (2003) Euphytica, 132, pp. 321-329
  • Prats, E., Bazzalo, M.E., León, A., Jorrin, J.V., Fungitoxic effect of scopolin and related coumarins on Sclerotinia sclerotiorum. A way to overcome sunflower head rot (2006) Euphytica, 147, pp. 451-460
  • Prats, E., Galindo, J.C., Bazzalo, M.E., Leon, A., Macias, F.A., Rubiales, D., Jorrin, J.V., Antifungal activity of a new phenolic compound from capitulum of a head rot-resistant sunflower genotype (2007) J. Chem. Ecol., 33, pp. 2245-2253
  • Price, J., Li, T.C., Kang, S.G., Na, J.K., Jang, J.C., Mechanisms of glucose signaling during germination of Arabidopsis (2003) Plant Physiol., 132, pp. 1424-1438
  • Rhoads, D.M., Umbach, A.L., Subbaiah, C.C., Siedow, J.N., Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling (2006) Plant Physiol., 141, pp. 357-366
  • Rice, W., Analysing tables of statistical tests (1989) Evolution, 43, pp. 223-225
  • Rodríguez, M.A., Venedikian, N., Bazzalo, M.E., Godeas, A., Histopathology of Sclerotinia sclerotiorum attack on flower parts of Helianthus annuus heads in tolerant and susceptible varieties (2004) Mycopathologia, 157, pp. 291-302
  • Roessner, U., Wagner, C., Kopka, J., Trethewey, R.N., Willmitzer, L., Simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry (2000) Plant J., 23, pp. 131-142
  • Roessner, U., Luedemann, A., Brust, D., Fiehn, O., Linke, T., Willmitzer, L., Fernie, A.R., Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems (2001) Plant Cell, 13, pp. 11-29
  • Roessner-Tunali, U., Hegemann, B., Lytovchenko, A., Carrari, F., Bruedigam, C., Granot, D., Fernie, A.R., Metabolic profiling of transgenic tomato plants overexpressing hexokinase reveals that the influence of hexose phosphorylation diminishes during fruit development (2003) Plant Physiol., 133, pp. 84-99
  • Roitsch, T., Balibrea, M.E., Hofmann, M., Proels, R., Sinha, A.K., Extracellular invertase: key metabolic enzyme and PR protein (2003) J. Exp. Bot., 382, pp. 513-524
  • Rönicke, S., Hahn, V., Vogler, A., Friedt, W., Quantitative trait loci analysis of resistance to Sclerotinia sclerotiorum in sunflower (2005) Phytopathology, 95, pp. 834-839
  • Schauer, N., Semel, Y., Roessner, U., Gur, A., Balbo, I., Carrari, F., Pleban, T., Fernie, A.R., Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement (2006) Nat. Biotechnol., 24, pp. 447-454
  • Scheideler, M., Schlaich, N.L., Fellenberg, K., Beissbarth, T., Hauser, N.C., Vingron, M., Slusarenko, A.J., Hoheisel, J.D., Monitoring the switch from housekeeping to pathogen defense metabolism in Arabidopsis thaliana using cDNA arrays (2002) J. Biol. Chem., 277, pp. 10555-10561
  • Sheveleva, E., Chmara, W., Bohnert, H.J., Jensen, R.G., Increased salt and drought tolerance by d-ononitol production in transgenic Nicotiana tabacum L (1997) Plant Physiol., 115, pp. 1211-1219
  • Schneiter, A.A., Miller, J.F., Description of sunflower growth stages (1981) Crop Sci., 21, pp. 901-903
  • Scholes, J.D., Lee, P.J., Horton, P., Lewis, D.H., Invertase: understanding changes in the photosynthetic and carbohydrate metabolism of barley leaves infected with powdery mildew (1994) New Phytol., 126, pp. 213-222
  • Senkoylu, N., Dale, N., Nutritional evaluation of a high-oil sunflower meal in broiler starter diets (2006) J. Appl. Poult. Res., 15, pp. 40-47
  • Sumner, L.W., Mendes, P., Dixon, R.A., Plant metabolomics: large-scale phytochemistry in the functional genomics era (2003) Phytochemistry, 62, pp. 817-836
  • Swarbrick, P.J., Schulze-Lefert, P., Scholes, J.D., Metabolic consequences of susceptibility and resistance in barley leaves challenged with powdery mildew (2006) Plant Cell Environ., 29, pp. 1061-1076
  • Tang, X., Frederick, R.D., Zhou, J., Halterman, D.A., Jia, Y., Martin, G.B., Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase (1996) Science, 274, pp. 260-263
  • Tang, S., Yu, J.K., Slabaugh, M.B., Shintani, D.K., Knapp, S.J., Simple sequence repeat map of the sunflower genome (2002) Theor. Appl. Genet., 105, pp. 1124-1136
  • Tavernier, V., Cadiou, S., Pageau, K., Laugé, R., Reisdorf-Cren, M., Langin, T., Masclaux-Daubresse, C., The plant nitrogen mobilization promoted by Colletotrichum lindemuthianum in Phaseolus leaves depends on fungus pathogenicity (2007) J. Exp. Bot., 58, pp. 3351-3360
  • Tohge, T., Fernie, A.R., Web-based resources for mass-spectrometry-based metabolomics: a users guide (2009) Phytochemistry, 70, pp. 450-456
  • Vilo, J., Kapushesky, M., Kemmeren, P., Sarkans, U., Brazma, A., Expression profiler (2003) The Analysis of Gene Expression Data: Methods and Software, , Parmigiani G., Garrett E., Irizarry R., and Zeger S. (Eds), Springer Verlag, New York, NY (p. 5)
  • Voegele, R.T., Wirsel, S., Möll, U., Lechner, M., Mendgen, K., Cloning and characterization of a novel invertase from the obligate biotroph Uromyces fabae and analysis of expression patterns of host and pathogen invertases in the course of infection (2006) Mol. Plant Microbe Interact., 19, pp. 625-634
  • Wagner, C., Sefkow, M., Kopka, J., Construction and application of a mass spectral and retention time index database generated from plant GC/EI-TOF-MS metabolite profiles (2003) Phytochemistry, 62, pp. 887-900
  • Zhao, J., Wang, J., An, L., Doergue, R.W., Chen, Z.J., Grau, C.R., Meng, J., Osborn, T.C., Analysis of gene expression profiles in response to Sclerotinia (2007) Planta, 227, pp. 13-24
  • Zhu, L., Liu, X., Liu, X., Jeannotte, R., Reese, J., Harris, M., Stuart, J., Chen, M., Hessian fly (Mayetiola destructor) attack causes dramatic shift in carbon/nitrogen metabolism in wheat (2007) Mol. Plant Microbe Interact., 21, pp. 70-78
  • Zrenner, R., Salanoubat, M., Willmitzer, L., Sonnewald, U., Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.) (1995) Plant J., 7, pp. 97-107
  • Zucker, M., Sequential induction of phenylalanine ammonia-lyase and a lyase-inactivating system in potato tuber disks (1968) Plant Physiol., 43, pp. 365-374
  • Zulak, K.G., Cornish, A., Daskalchuk, T.E., Deyholos, M.K., Goodenowe, D.B., Gordon, P.M., Klassen, D., Facchini, P.J., Gene transcript and metabolite profiling of elicitor-induced opium poppy cell cultures reveals the coordinate regulation of primary and secondary metabolism (2007) Planta, 225, pp. 1085-1106

Citas:

---------- APA ----------
Peluffo, L., Lia, V., Troglia, C., Maringolo, C., Norma, P., Escande, A., Esteban Hopp, H.,..., Carrari, F. (2010) . Metabolic profiles of sunflower genotypes with contrasting response to Sclerotinia sclerotiorum infection. Phytochemistry, 71(1), 70-80.
http://dx.doi.org/10.1016/j.phytochem.2009.09.018
---------- CHICAGO ----------
Peluffo, L., Lia, V., Troglia, C., Maringolo, C., Norma, P., Escande, A., et al. "Metabolic profiles of sunflower genotypes with contrasting response to Sclerotinia sclerotiorum infection" . Phytochemistry 71, no. 1 (2010) : 70-80.
http://dx.doi.org/10.1016/j.phytochem.2009.09.018
---------- MLA ----------
Peluffo, L., Lia, V., Troglia, C., Maringolo, C., Norma, P., Escande, A., et al. "Metabolic profiles of sunflower genotypes with contrasting response to Sclerotinia sclerotiorum infection" . Phytochemistry, vol. 71, no. 1, 2010, pp. 70-80.
http://dx.doi.org/10.1016/j.phytochem.2009.09.018
---------- VANCOUVER ----------
Peluffo, L., Lia, V., Troglia, C., Maringolo, C., Norma, P., Escande, A., et al. Metabolic profiles of sunflower genotypes with contrasting response to Sclerotinia sclerotiorum infection. Phytochemistry. 2010;71(1):70-80.
http://dx.doi.org/10.1016/j.phytochem.2009.09.018