Metabolic Consequences of Infection of Grapevine (Vitis vinifera L.) cv. "Modra frankinja" with Flavescence Dorée Phytoplasma

. 2016 ; 7 () : 711. [epub] 20160523

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid27242887

Flavescence dorée, caused by the quarantine phytoplasma FDp, represents the most devastating of the grapevine yellows diseases in Europe. In an integrated study we have explored the FDp-grapevine interaction in infected grapevines of cv. "Modra frankinja" under natural conditions in the vineyard. In FDp-infected leaf vein-enriched tissues, the seasonal transcriptional profiles of 14 genes selected from various metabolic pathways showed an FDp-specific plant response compared to other grapevine yellows and uncovered a new association of the SWEET17a vacuolar transporter of fructose with pathogens. Non-targeted metabolome analysis from leaf vein-enriched tissues identified 22 significantly changed compounds with increased levels during infection. Several metabolites corroborated the gene expression study. Detailed investigation of the dynamics of carbohydrate metabolism revealed significant accumulation of sucrose and starch in the mesophyll of FDp-infected leaves, as well as significant up-regulation of genes involved in their biosynthesis. In addition, infected leaves had high activities of ADP-glucose pyrophosphorylase and, more significantly, sucrose synthase. The data support the conclusion that FDp infection inhibits phloem transport, resulting in accumulation of carbohydrates and secondary metabolites that provoke a source-sink transition and defense response status.

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Ahmad J. N., Renaudin J., Eveillard S. (2015). Molecular study of the effect of exogenous phytohormones application in stolbur phytoplasma infected tomatoes on disease development. Phytopathog. Molicutes 5, 121–122. 10.5958/2249-4677.2015.00052.3 DOI

Andersen C. L., Jensen J. L., Ørntoft T. F. (2004). Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64, 5245–5250. 10.1158/0008-5472.CAN-04-0496 PubMed DOI

André A., Maucourt M., Moing A., Rolin D., Renaudin J. (2005). Sugar import and phytopathogenicity of Spiroplasma citri: glucose and fructose play distinct roles. Mol. Plant Microbe Interact. 18, 33–42. 10.1094/MPMI-18-0033 PubMed DOI

Arnaud G., Malembic-Maher S., Salar P., Bonnet P., Maixner M., Marcone C., et al. . (2007). Multilocus sequence typing confirms the close genetic inter-relatedness between three distinct flavescence dorée phytoplasma strain clusters and group 16SrV phytoplasmas infecting grapevine and alder in Europe. Appl. Environ. Microbiol. 73, 4001–4010. 10.1128/AEM.02323-06 PubMed DOI PMC

Ballicora M., Iglesias A., Preiss J. (2004). ADPglucose pyrophosphorylase: a regulatory enzyme for plant starch synthesis. Photosynth. Res. 79, 1–24. 10.1023/B:PRES.0000011916.67519.58 PubMed DOI

Baroja-Fernández E., Muńoz F. J., Montero M., Etxeberria E., Sesma M. T., Ovecka M., et al. . (2009). Enhancing sucrose synthase activity in transgenic potato (Solanum tuberosum L.) tubers results in increased levels of starch, ADPglucose and UDPglucose and total yield. Plant Cell Physiol. 50, 1651–1662. 10.1093/pcp/pcp108 PubMed DOI

Berger S., Sinha A. K., Roitsch T. (2007). Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. J. Exp. Bot. 58, 4019–4026. 10.1093/jxb/erm298 PubMed DOI

Bertaccini A. (ed.). (2014). Phytoplasma and Phytoplasma Disease Managment: How to Reduce Economic Impact. COST Action FA0807. Bologna: IPWG.

Bertamini M., Nedunchezhian N. (2001). Effects of phytoplasma [stolbur-subgroup (Bois Noir-BN)] on photosynthetic pigments, saccharides, ribulose 1,5-bisphosphate carboxylase, nitrate and nitrite reductases, and photosynthetic activities in field-grown grapevine (Vitis vinifera L. cv. ‘Chardonnay’) leaves. Photosynthetica 39, 119–122. 10.1023/A:1012412406727 DOI

Boudon-Padieu E. (2002). Flavescence dorée of the grapevine: knowledge and new developments in epidemiology, etiology and diagnosis. ATTI Giornate Fitopatol. 1, 15–34.

Brzin J., Petrovič N., Ravnikar M., Kovač M. (2011). Induction of sucrose synthase in the phloem of phytoplasma infected maize. Biol. Plant. 55, 711–715. 10.1007/s10535-011-0173-9 DOI

Carle P., Malembic-Maher S., Arricau-Bouvery N., Desque D., Eveillard S., Carrère S., et al. (2011). ‘Flavescence dorée’ phytoplasma genome: a metabolism oriented towards glycolysis and protein degradation. Bull. Insectol. 64, S13–S14.

Chardon F., Bedu M., Calenge F., Klemens P. A. W., Spinner L., Clement G., et al. . (2013). Leaf fructose content is controlled by the vacuolar transporter SWEET17 in Arabidopsis. Curr. Biol. 23, 697–702. 10.1016/j.cub.2013.03.021 PubMed DOI

Chen L.-Q. (2014). SWEET sugar transporters for phloem transport and pathogen nutrition. New Phytol. 201, 1150–1155. 10.1111/nph.12445 PubMed DOI

Chen L.-Q., Hou B.-H., Lalonde S., Takanaga H., Hartung M. L., Qu X.-Q., et al. . (2010). Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468, 527–532. 10.1038/nature09606 PubMed DOI PMC

Chen L.-Q., Qu X.-Q., Hou B.-H., Sosso D., Osorio S., Fernie A. R., et al. . (2012). Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335, 207–211. 10.1126/science.1213351 PubMed DOI

Choi Y. H., Tapias E. C., Kim H. K., Lefeber A. W., Erkelens C., Verhoeven, et al. . (2004). Metabolic discrimination of Catharanthus roseus leaves infected by phytoplasma using 1H-NMR spectroscopy and multivariate data analysis. Plant Physiol. 135, 2398–23410. 10.1104/pp.104.041012 PubMed DOI PMC

Christensen N. M., Nicolaisen M., Hansen M., Schulz A. (2004). Distribution of phytoplasmas in infected plants as revealed by real-time PCR and bioimaging. Mol. Plant Microbe Interact. 17, 1175–1184. 10.1094/MPMI.2004.17.11.1175 PubMed DOI

Constable F. E. (2010). Phytoplasma Epidemiology, Grapevines as a Model, in Phytoplasmas: Genomes, Plant Hosts and Vectors. Wallingford, UK: CAB International.

Contaldo N., Bertaccini A., Paltrinieri S., Windsor H. M., Windsor G. D. (2012). Axenic culture of plant pathogenic phytoplasmas. Phytopathol. Mediterr. 51, 607–617. 10.14601/Phytopathol_Mediterr-11773 DOI

Derbyshire M. K., Gonzales N. R., Lu S., He J., Marchler G. H., Wang Z., et al. . (2015). Improving the consistency of domain annotation within the conserved domain database. Database 2015:bav012. 10.1093/database/bav012 PubMed DOI PMC

Dermastia M., Nikolić P., Chersicola M., Gruden K. (2015). Transcriptional profiling in infected and recovered grapevine plant responses to ‘Candidatus Phytoplasma solani’. Phytopathog. Molicutes 5, 123–124. 10.5958/2249-4677.2015.00053.5 DOI

Ehness R., Ecker M., Godt D. E., Roitsch T. (1997). Glucose and stress independently regulate source and sink metabolism and defense mechanisms via signal transduction pathways involving protein phosphorylation. Plant Cell 9, 1825–1841. 10.1105/tpc.9.10.1825 PubMed DOI PMC

Endeshaw S., Murolo S., Romanazzi G., Neri D. (2012). Effects of Bois noir on carbon assimilation, transpiration, stomatal conductance of leaves and yield of grapevine (Vitis vinifera) cv. Chardonnay. Physiol. Plant. 145, 286–295. 10.1111/j.1399-3054.2012.01576.x PubMed DOI

Eom J.-S., Chen L.-Q., Sosso D., Julius B. T., Lin I. W., Qu X.-Q., et al. . (2015). SWEETs, transporters for intracellular and intercellular sugar translocation. Curr. Opin. Plant Biol. 25, 53–62. 10.1016/j.pbi.2015.04.005 PubMed DOI

Fiehn O. (2002). Metabolomics – the link between genotypes and phenotypes. Plant Mol. Biol. 48, 155–171. 10.1023/A:1013713905833 PubMed DOI

Foyer C., Noctor G. (2005). Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ. 28, 1056–1071. 10.1111/j.1365-3040.2005.01327.x DOI

Frías M., Brito N., González C. (2013). The Botrytis cinerea cerato-platanin BcSpl1 is a potent inducer of systemic acquired resistance (SAR) in tobacco and generates a wave of salicylic acid expanding from the site of application. Mol. Plant Pathol. 14, 191–196. 10.1111/j.1364-3703.2012.00842.x PubMed DOI PMC

Gai Y. P., Han X. J., Li Y. Q., Yuan C.-Z., Mo Y. Y., Guo F.-Y., et al. . (2014). Metabolomic analysis reveals the potential metabolites and pathogenesis involved in mulberry yellow dwarf disease. Plant Cell Environ. 37, 1474–1490. 10.1111/pce.12255 PubMed DOI

Gambino G., Boccacci P., Margaria P., Palmano S., Gribaudo I. (2013). Hydrogen peroxide accumulation and transcriptional changes in grapevines recovered from flavescence dorée disease. Phytopathology 103, 776–784. 10.1094/PHYTO-11-12-0309-R PubMed DOI

Gamm M., Héloir M. C., Bligny R., Vaillant-Gaveau N., Trouvelot S., Alcaraz, et al. . (2011). Changes in carbohydrate metabolism in Plasmopara viticola-infected grapevine leaves. Mol. Plant Microbe Interact. 24, 1061–1073. 10.1094/MPMI-02-11-0040 PubMed DOI

Gaurivaud P., Danet J. L., Laigret F., Garnier M., Bové J. M. (2000). Fructose utilization and phytopathogenicity of Spiroplasma citri. Mol. Plant Microbe Interact. 13, 1145–1155. 10.1094/MPMI.2000.13.10.1145 PubMed DOI

Geigenberger P., Langenberger S., Wilke I., Heineke D., Heldt H. W., Stitt M. (1993). Sucrose is metabolised by sucrose synthase and glycolysis within the phloem complex of Ricinus communis L. seedlings. Planta 190, 446–453. 10.1007/bf00224782 DOI

Godt D. E., Riegel A., Roitsch T. (1995). Regulation of sucrose synthase expression in Chenopodium rubrum: characterisation of sugar induced expression in photoautotrophic suspension cultures and sink tissue specific expression in plants. J. Plant Physiol. 146, 231–238. 10.1016/S0176-1617(11)82046-8 DOI

Großkinsky D. K., Svensgaard J., Christensen S., Roitsch T. (2015). Plant phenomics and the need for physiological phenotyping across scales to narrow the genotype-to-phenotype knowledge gap. J. Expt. Bot. 66, 5429–5440. 10.1093/jxb/erv345 PubMed DOI

Guo W.-J., Nagy R., Chen H.-Y., Pfrunder S., Yu Y.-C., Santelia D., et al. . (2014). SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of Arabidopsis roots and leaves. Plant Physiol. 164, 777–789. 10.1104/pp.113.232751 PubMed DOI PMC

Gutha L. R., Casassa L. F., Harbertson J. F., Naidu R. A. (2010). Modulation of flavonoid biosynthetic pathway genes and anthocyanins due to virus infection in grapevine (Vitis vinifera L.) leaves. BMC Plant Biol. 10:187. 10.1186/1471-2229-10-187 PubMed DOI PMC

Hren M., Boben J., Rotter A., Kralj P., Gruden K., Ravnikar M. (2007). Real-time PCR detection systems for Flavescence dorée and Bois noir phytoplasmas in grapevine: comparison with conventional PCR detection and application in diagnostics. Plant Pathol. 56, 785–796. 10.1111/j.1365-3059.2007.01688.x DOI

Hren M., Nikolić P., Rotter A., Blejec A., Terrier N., Ravnikar M., et al. . (2009a). ‘Bois noir’ phytoplasma induces significant reprogramming of the leaf transcriptome in the field grown grapevine. BMC Genomics 10:460. 10.1186/1471-2164-10-460 PubMed DOI PMC

Hren M., Ravnikar M., Brzin J., Ermacora P., Carraro L., Bianco, et al. (2009b). Induced expression of sucrose synthase and alcohol dehydrogenase I genes in phytoplasma-infected grapevine plants grown in the field. Plant Pathol. 58, 170–180. 10.1111/j.1365-3059.2008.01904.x DOI

Izawa T. (2015). Deciphering and prediction of plant dynamics under field conditions. Curr. Opin. Plant Biol. 24, 87–92. 10.1016/j.pbi.2015.02.003 PubMed DOI

Jaillon O., Aury J.-M., Noel B., Policriti A., Clepet C., Casagrande A., et al. . (2007). The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449, 463–467. 10.1038/nature06148 PubMed DOI

Jammer A., Gasperl A., Luschin-Ebengreuth N., Heyneke E., Chu H., Cantero-Navarro, et al. . (2015). Simple and robust determination of the activity signature of key carbohydrate metabolism enzymes for physiological phenotyping in model and crop plants. J. Exp. Bot. 66, 5531–5542. 10.1093/jxb/erv228 PubMed DOI

Junqueira A., Bedendo I., Pascholati S. (2004). Biochemical changes in corn plants infected by the maize bushy stunt phytoplasma. Physiol. Mol. Plant Pathol. 65, 181–185. 10.1016/j.pmpp.2005.01.005 DOI

Koch K. (2004). Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr. Opin. Plant Biol. 7, 235–246. 10.1016/j.pbi.2004.03.014 PubMed DOI

Kopka J., Schauer N., Krueger S., Birkemeyer C., Usadel B., Bergmüller, et al. . (2005). GMD@CSB.DB: the Golm metabolome database. Bioinformatics 21, 1635–1638. 10.1093/bioinformatics/bti236 PubMed DOI

Kube M., Mitrovic J., Duduk B., Rabus R., Seemüller E. (2012). Current view on phytoplasma genomes and encoded metabolism. ScientificWorldJournal 2012:185942. 10.1100/2012/185942 PubMed DOI PMC

Landi L., Romanazzi G. (2011). Seasonal variation of defense-related gene expression in leaves from Bois noir affected and recovered grapevines. J. Agr. Food Chem. 59, 6628–6637. 10.1021/jf104297n PubMed DOI

Lecourieux F., Kappel C., Lecourieux D., Serrano A., Torres E., Arce-Johnson P., et al. . (2014). An update on sugar transport and signalling in grapevine. J. Exp. Bot. 65, 821–832. 10.1093/jxb/ert394 PubMed DOI

Lee I.-M., Martini M., Marcone C., Zhu S. F. (2004). Classification of phytoplasma strains in the elm yellows group (16SrV) and proposal of ‘Candidatus Phytoplasma ulmi’ for the phytoplasma associated with elm yellows. Int. J. Syst. Evol. Microbiol. 54, 337–347. 10.1099/ijs.0.02697-0 PubMed DOI

Lee I.-M., Zhao Y., Davis R. E., Wei W., Martini M. (2007). Prospects of DNA-based systems for differentiation and classification of phytoplasmas. Bull. Insectol. 60, 239–244.

Lemoine R., LaCamera S., Atanassova R., Dédaldéchamp F., Allario T., Pourtau N., et al. . (2013). Source-to-sink transport of sugar and regulation by environmental factors. Front. Plant Sci. 4:272. 10.3389/fpls.2013.00272 PubMed DOI PMC

Leon R., Sanatamaria J. M., Alpizar L., Escamilla J. A., Oropeza C. (1996). Physiological and biochemical changes in shoots of coconut palms affected by lethal yellowing. New Phytol. 134, 227–234. 10.1111/j.1469-8137.1996.tb04627.x DOI

Lepka P., Stitt M., Moll E., Seemüller E. (1999). Effect of phytoplasmal infection on concentration and translocation of carbohydrates and amino acids in periwinkle and tobacco. Physiol. Mol. Plant Pathol. 55, 59–68. 10.1006/pmpp.1999.0202 DOI

Lu Y.-T., Li M.-Y., Cheng K.-T., Tan C. M., Su L.-W., Lin W.-Y., et al. . (2014). Transgenic plants that express the phytoplasma effector SAP11 Show altered phosphate starvation and defense responses. Plant Physiol. 164, 1456–1469. 10.1104/pp.113.229740 PubMed DOI PMC

Maejima K., Oshima K., Namba S. (2014). Exploring the phytoplasmas, plant pathogenic bacteria. J. Gen. Plant Pathol. 80, 210–221. 10.1007/s10327-014-0512-8 DOI

Malembic-Maher S., Salar P., Filippin L., Carle P., Angelini E., Foissac X. (2011). Genetic diversity of European phytoplasmas of the 16SrV taxonomic group and proposal of ‘Candidatus Phytoplasma rubi’. Int. J. Syst. Evol. Microbiol. 61, 2129–2134. 10.1099/ijs.0.025411-0 PubMed DOI

Marcone C. (2014). Molecular biology and pathogenicity of phytoplasmas. Ann. Appl. Biol. 165, 199–221. 10.1111/aab.12151 DOI

Margaria P., Abbà S., Palmano S. (2013). Novel aspects of grapevine response to phytoplasma infection investigated by a proteomic and phospho-proteomic approach with data integration into functional networks. BMC Genomics 14:38. 10.1186/1471-2164-14-38 PubMed DOI PMC

Margaria P., Ferrandino A., Caciagali P., Kedrina O., Schubert A., Palmano S. (2014). Metabolic and transcript analysis of the flavonoid pathway in diseased and recovered Nebbiolo and Barbera grapevines (Vitis vinifera L.) following infection by Flavescence dorée phytoplasma. Plant Cell Environ. 37, 2183–2200. 10.1111/pce.12332 PubMed DOI

Margaria P., Palmano S. (2011). Response of the Vitis vinifera L. cv. ‘Nebbiolo’ proteome to Flavescence dorée phytoplasma infection. Proteomics 11, 212–224. 10.1002/pmic.201000409 PubMed DOI

Mari A., Lyon D., Fragner L., Montoro P., Piacente S., Wienkoop S., et al. . (2013). Phytochemical composition of Potentilla anserina L. analyzed by an integrative GC-MS and LC-MS metabolomics platform. Metabolomics 9, 599–607. 10.1007/s11306-012-0473-x PubMed DOI PMC

Maust B. E., Espadas F., Talavera C., Aguilar M., Santamaría J. M., Oropeza C. (2003). Changes in carbohydrate metabolism in coconut palms infected with the lethal yellowing phytoplasma. Phytopathology 93, 976–981. 10.1094/PHYTO.2003.93.8.976 PubMed DOI

Mehle N., Rupar M., Seljak G., Ravnikar M., Dermastia M. (2011). Molecular diversity of ‘flavescence dorée’ phytoplasma strains in Slovenia. Bull. Insectol. 64, S29–S30.

Musetti R., Buxa S. V., De Marco F., Loschi A., Polizzotto R., Kogel K. H., et al. . (2013). Phytoplasma-triggered Ca2+ influx is involved in sieve-tube blockage. Mol. Plant Microbe Interact. 26, 379–386. 10.1094/MPMI-08-12-0207-R PubMed DOI

Musetti R., Marabottini R., Badiani M., Martini M., Sanità di Toppi L., Borselli S., et al. (2007). On the role of H2O2 in the recovery of grapevine (Vitis vinifera, cv. Prosecco) from Flavescence dorée disease. Funct. Plant Biol. 34, 750–758. 10.1071/FP06308 PubMed DOI

Nelson N. (1944). Photometric adaptation of the somogyi method for determination of glucose. J. Biol.Chem. 153, 375–380.

Nicolaisen M., Horvath D. P. (2008). A branch-inducing phytoplasma in Euphorbia pulcherrima is associated with changes in expression of host genes. J. Phytopathol. 156, 403–407. 10.1111/j.1439-0434.2007.01372.x DOI

Papura D., Burban C., van Helden M., Giresse X., Nusillard B., Guillemaud T., et al. . (2012). Microsatellite and mitochondrial data provide evidence for a single major introduction for the neartic leafhopper Scaphoideus titanus in Europe. PLoS ONE 7:e368821. 10.1371/journal.pone.0036882 PubMed DOI PMC

Papura D., Giresse X., Delmotte F., Danet J. L., van Helden M., Foissac X., et al. . (2009). Comparing the spatial genetic structures of the Flavescence dorée phytoplasma and its leafhopper vector Scaphoideus titanus. Infect. Genet. Evol. 9, 67–876. 10.1016/j.meegid.2009.05.009 PubMed DOI

Prezelj N., Nikolić P., Gruden K., Ravnikar M., Dermastia M. (2013). Spatiotemporal distribution of flavescence dorée phytoplasma in grapevine. Plant Pathol. 62, 760–766. 10.1111/j.1365-3059.2012.02693.x PubMed DOI PMC

Quaglino F., Zhao Y., Casati P., Bulgari D., Bianco P. A., Wei W., et al. . (2013). ‘Candidatus Phytoplasma solani’, a novel taxon associated with stolbur- and bois noir-related diseases of plants. Int. J. Syst. Evol. Microbiol. 63, 2879–2894. 10.1099/ijs.0.044750-0 PubMed DOI

Roitsch T. (1999). Source-sink regulation by sugar and stress. Curr. Opin. Plant Biol. 2, 198–206. 10.1016/S1369-5266(99)80036-3 PubMed DOI

Roitsch T., Ehness R. (2000). Regulation of source/sink relations by cytokinins. Plant Growth Regul. 32, 359–367. 10.1023/A:1010781500705 DOI

Roitsch T., González M. C. (2004). Function and regulation of plant invertases: sweet sensations. Trends Plant Sci. 9, 606–613. 10.1016/j.tplants.2004.10.009 PubMed DOI

Rojas C. M., Senthil-Kumar M., Tzin V., Mysore K. S. (2014). Regulation of primary metabolism during plant-pathogen interactions and its contribution to plant. Front. Plant Sci. 5:17. 10.3389/fpls.2014.00017 PubMed DOI PMC

Rolland F., Moore B., Sheen J. (2002). Sugar sensing and signalling in plants. Plant Cell 14, 185–205. 10.1146/annurev.arplant.57.032905.105441 PubMed DOI PMC

Ruan Y.-L., Jin Y., Li G. J., Yang Y. J., Boyer J. S. (2010). Sugar input, metabolism and signaling mediated by invertase: roles in development, yield potential and response to drought and heat. Mol. Plant 3, 942–955. 10.1093/mp/ssq044 PubMed DOI

Rusjan D., Halbwirth H., Stich K., Mikulič-Petkovšek M., Veberič R. (2012b). Biochemical response of grapevine variety ‘Chardonnay’ (Vitis vinifera L.) to infection with grapevine yellows (Bois noir). Eur. J. Plant Pathol. 134, 231–237. 10.1007/s10658-012-9988-2 DOI

Rusjan D., Mikulič-Petkovšek M. (2015). Phenolic responses in 1-year-old canes of Vitis vinifera cv. Chardonnay induced by grapevine yellows (Bois noir). Aust. J. Grape Wine R. 21, 123–134. 10.1111/ajgw.12106 DOI

Rusjan D., Veberič R., Mikulič-Petkovšek M. (2012a). The response of phenolic compounds in grapes of the variety ‘Chardonnay’ (Vitis vinifera L.) to the infection by phytoplasma Bois noir. Eur. J. Plant Pathol. 133, 965–974. 10.1007/s10658-012-9967-7 DOI

Sabanadzovic S., Abou-Ghanem N., Castellano M. A., Digiaro M., Martelli G. P. (2000). Grapevine fleck virus-like viruses in Vitis. Arch.Virol. 145, 553–565. 10.1007/s007050050046 PubMed DOI

Santi S., De Marco F., Polizzotto R., Grisan S., Musetti R. (2013a). Recovery from stolbur disease in grapevine involves changes in sugar transport and metabolism. Front. Plant Sci. 4:171. 10.3389/fpls.2013.00171 PubMed DOI PMC

Santi S., Grisan S., Pierasco A., De Marco F., Musetti R. (2013b). Laser microdissection of grapevine leaf phloem infected by stolbur reveals site-specific gene responses associated to sucrose transport and metabolism. Plant Cell Environ. 36, 343–355. 10.1111/j.1365-3040.2012.02577.x PubMed DOI

Scharte J., Schön H., Weis E. (2005). Photosynthesis and carbohydrate metabolism in tobacco leaves during an incompatible interaction with Phytophthora ncotianae. Plant Cell Environ. 28, 1421–1435. 10.1111/j.1365-3040.2005.01380.x DOI

Schmidt D. D., Kessler A., Kessler D., Schmidt S., Lim M., Gase K., et al. . (2004). Solanum nigrum: a model ecological expression system and its tools. Mol. Ecol. 13, 981–995. 10.1111/j.1365-294X.2004.02111.x PubMed DOI

Smith A. M., Zeeman S. C., Smith S. M. (2005). Starch degradation. Annu. Rev. Plant Biol. 56, 73–98. 10.1146/annurev.arplant.56.032604.144257 PubMed DOI

Solfanelli C., Poggi A., Loreti E., Alpi A., Perata P. (2006). Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol. 140, 637–646. 10.1104/pp.105.072579 PubMed DOI PMC

Steffeck R., Reisenzein H., Zeisner N. (2007). Analysis of the pest risk from grapevine flavescence dorée phytoplasma to Austrian viticulture. OEPP/EPPO Bull. 37, 191–203. 10.1111/j.1365-2338.2007.01102.x DOI

Stein S. E. (1999). An integrated method for spectrum extraction. J. Am. Soc. Mass Spectrometry 10, 770–781. 10.1016/S1044-0305(99)00047-1 DOI

Stitt M., Gibon Y. (2014). Why measure enzyme activities in the era of systems biology? Trends Plant Sci. 19, 256–265. 10.1016/j.tplants.2013.11.003 PubMed DOI

Sumner L. W., Amberg A., Barrett D., Beale M. H., Beger R., Daykin C. A., et al. . (2007). Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI) Proposed minimum reporting standards for chemical analysis. Metabolomics 3, 211–221. 10.1007/s11306-007-0082-2 PubMed DOI PMC

Takayanagi T., Yokotsuka K. (1997). Relationship between sucrose accumulation and sucrose-metabolizing enzymes in developing grapes. Am. J. Enol. Viticult. 48, 403–407.

Tiessen A., Padilla-Chacon D. (2012). Subcellular compartmentation of sugar signaling: links among carbon cellular status, route of sucrolysis, sink-source allocation, and metabolic partitioning. Front. Plant Sci. 3:306. 10.3389/fpls.2012.00306 PubMed DOI PMC

Van Damme M., Huibers R. P., Elberse J., Van den Ackerveken G. (2008). Arabidopsis DMR6 encodes a putative 2OG-Fe(II) oxygenase that is defense-associated but required for susceptibility to downy mildew. Plant J. 54, 785–793. 10.1111/j.1365-313X.2008.03427.x PubMed DOI

Velasco R., Zharkikh A., Troggio M., Cartwright D. A., Cestaro A., Pruss D., et al. . (2007). A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS ONE 2:e1326. 10.1371/journal.pone.0001326 PubMed DOI PMC

Vitali M., Chitarra W., Galetto L., Bosco D., Narzachi C., Guillino M. L., et al. (2013). Flavescence dorée phytoplasma deregulates stomatal control of photosynthesis in Vitis vinifera. Ann. Appl. Biol. 162, 335–346. 10.1111/aab.12025 DOI

Weckwerth W. (2011). Green systems biology—from single genomes, proteomes and metabolomes to ecosystems research and biotechnology. J. Proteomics 75, 284–305. 10.1016/j.jprot.2011.07.010 PubMed DOI

Weckwerth W., Wenzel K., Fiehn O. (2004). Process for the integrated extraction, identification and quantification of metabolites, proteins and RNA to reveal their co-regulation in biochemical networks. Proteomics 4, 78–83. 10.1002/pmic.200200500 PubMed DOI

Zeilmaker T., Ludwig N. R., Elberse J., Seidl M. F., Berke L., Van Doorn A., et al. . (2015). DOWNY MILDEW RESISTANT 6 and DMR6-LIKE OXYGENASE 1 are partially redundant but distinct suppressors of immunity in Arabidopsis. Plant J. 81, 210–222. 10.1111/tpj.12719 PubMed DOI

Zhao Y., Davis R. E., Wei W., Lee I. M. (2015). Should ‘Candidatus Phytoplasma’ be retained within the order Acholeplasmatales? Int. J. Syst. Evol. Microbiol. 65, 1075–1082. 10.1099/ijs.0.000050 PubMed DOI

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