Metabolic consequences of infection of grapevine (vitis vinifera l.) cv. “modra frankinja” with flavescence dorée phytoplasma

Frontiers in Plant Science

Volumn 7, Issue MAY2016, 2016, Pages

  Prezelj, Nina ^a   Covington, Elizabeth ^a   Roitsch, Thomas ^b,c   Gruden, Kristina ^a   Fragner, Lena ^d   Weckwerth, Wolfram ^d   Chersicola, Marko ^a,e   Vodopivec, Maja ^a   Dermastia, Marina ^a  

^a NATIONAL INSTITUTE OF BIOLOGY   (Slovenia)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c Global Change Research Centre   (Czech Republic)

^d UNIVERSITY OF VIENNA   (Austria)

^e JO EF STEFAN INSTITUTE   (Slovenia)

Author keywords

Fructose; Gene expression; Metabolome; Starch; Sucrose synthase; SWEET17a

Indexed keywords

EID: 84969504999     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.00711     Document Type: Article

References (101)

1. Ahmad, J. N., Renaudin, J., and 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. doi: 10. 5958/2249-4677. 2015. 00052. 3
2. Andersen, C. L., Jensen, J. L., and 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. doi: 10. 1158/0008-5472. CAN-04-0496
3. André, A., Maucourt, M., Moing, A., Rolin, D., and Renaudin, J. (2005). Sugar import and phytopathogenicity of Spiroplasma citri: glucose and fructose play distinct roles. Mol. Plant Microbe Interact. 18, 33-42. doi: 10. 1094/MPMI-18-0033
4. 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. doi: 10. 1128/AEM. 02323-06
5. Ballicora, M., Iglesias, A., and Preiss, J. (2004). ADPglucose pyrophosphorylase: a regulatory enzyme for plant starch synthesis. Photosynth. Res. 79, 1-24. doi: 10. 1023/B: PRES. 0000011916. 67519. 58
6. 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. doi: 10. 1093/pcp/pcp108
7. Berger, S., Sinha, A. K., and Roitsch, T. (2007). Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. J. Exp. Bot. 58, 4019-4026. doi: 10. 1093/jxb/erm298
8. Bertaccini, A. (ed.). (2014). Phytoplasma and Phytoplasma Disease Managment: How to Reduce Economic Impact. COST Action FA0807. Bologna: IPWG.
9. Bertamini, M., and 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. doi: 10. 1023/A: 1012412406727
10. Boudon-Padieu, E. (2002). Flavescence dorée of the grapevine: knowledge and new developments in epidemiology, etiology and diagnosis. ATTI Giornate Fitopatol. 1, 15-34.
11. Brzin, J., Petrovič, N., Ravnikar, M., and Kovač, M. (2011). Induction of sucrose synthase in the phloem of phytoplasma infected maize. Biol. Plant. 55, 711-715. doi: 10. 1007/s10535-011-0173-9
12. 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.
13. 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. doi: 10. 1016/j. cub. 2013. 03. 021
14. Chen, L. -Q. (2014). SWEET sugar transporters for phloem transport and pathogen nutrition. New Phytol. 201, 1150-1155. doi: 10. 1111/nph. 12445
15. 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. doi: 10. 1038/nature09606
16. 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. doi: 10. 1126/science. 1213351
17. 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. doi: 10. 1104/pp. 104. 041012
18. Christensen, N. M., Nicolaisen, M., Hansen, M., and Schulz, A. (2004). Distribution of phytoplasmas in infected plants as revealed by real-time PCR and bioimaging. Mol. Plant Microbe Interact. 17, 1175-1184. doi: 10. 1094/MPMI. 2004. 17. 11. 1175
19. Constable, F. E. (2010). Phytoplasma Epidemiology, Grapevines as a Model, in Phytoplasmas: Genomes, Plant Hosts and Vectors. Wallingford, UK: CAB International.
20. Contaldo, N., Bertaccini, A., Paltrinieri, S., Windsor, H. M., and Windsor, G. D. (2012). Axenic culture of plant pathogenic phytoplasmas. Phytopathol. Mediterr. 51, 607-617. doi: 10. 14601/Phytopathol_Mediterr-11773
21. 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. doi: 10. 1093/database/bav012
22. Dermastia, M., Nikolić, P., Chersicola, M., and Gruden, K. (2015). Transcriptional profiling in infected and recovered grapevine plant responses to 'Candidatus Phytoplasma solani'. Phytopathog. Molicutes 5, 123-124. doi: 10. 5958/2249-4677. 2015. 00053. 5
23. Ehness, R., Ecker, M., Godt, D. E., and 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. doi: 10. 1105/tpc. 9. 10. 1825
24. Endeshaw, S., Murolo, S., Romanazzi, G., and 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. doi: 10. 1111/j. 1399-3054. 2012. 01576. x
25. 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. doi: 10. 1016/j. pbi. 2015. 04. 005
26. Fiehn, O. (2002). Metabolomics-the link between genotypes and phenotypes. Plant Mol. Biol. 48, 155-171. doi: 10. 1023/A: 1013713905833
27. Foyer, C., and 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. doi: 10. 1111/j. 1365-3040. 2005. 01327. x
28. Frías, M., Brito, N., and 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. doi: 10. 1111/j. 1364-3703. 2012. 00842. x
29. 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. doi: 10. 1111/pce. 12255
30. Gambino, G., Boccacci, P., Margaria, P., Palmano, S., and Gribaudo, I. (2013). Hydrogen peroxide accumulation and transcriptional changes in grapevines recovered from flavescence dorée disease. Phytopathology 103, 776-784. doi: 10. 1094/PHYTO-11-12-0309-R
31. 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. doi: 10. 1094/MPMI-02-11-0040
32. Gaurivaud, P., Danet, J. L., Laigret, F., Garnier, M., and Bové, J. M. (2000). Fructose utilization and phytopathogenicity of Spiroplasma citri. Mol. Plant Microbe Interact. 13, 1145-1155. doi: 10. 1094/MPMI. 2000. 13. 10. 1145
33. Geigenberger, P., Langenberger, S., Wilke, I., Heineke, D., Heldt, H. W., and Stitt, M. (1993). Sucrose is metabolised by sucrose synthase and glycolysis within the phloem complex of Ricinus communis L. seedlings. Planta 190, 446-453. doi: 10. 1007/bf00224782
34. Godt, D. E., Riegel, A., and 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. doi: 10. 1016/S0176-1617(11)82046-8
35. Großkinsky, D. K., Svensgaard, J., Christensen, S., and 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. doi: 10. 1093/jxb/erv345
36. 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. doi: 10. 1104/pp. 113. 232751
37. Gutha, L. R., Casassa, L. F., Harbertson, J. F., and 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. doi: 10. 1186/1471-2229-10-187
38. Hren, M., Boben, J., Rotter, A., Kralj, P., Gruden, K., and 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. doi: 10. 1111/j. 1365-3059. 2007. 01688. x
39. 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. doi: 10. 1186/1471-2164-10-460
40. 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. doi: 10. 1111/j. 1365-3059. 2008. 01904. x
41. Izawa, T. (2015). Deciphering and prediction of plant dynamics under field conditions. Curr. Opin. Plant Biol. 24, 87-92. doi: 10. 1016/j. pbi. 2015. 02. 003
42. 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. doi: 10. 1038/nature06148
43. 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. doi: 10. 1093/jxb/erv228
44. Junqueira, A., Bedendo, I., and Pascholati, S. (2004). Biochemical changes in corn plants infected by the maize bushy stunt phytoplasma. Physiol. Mol. Plant Pathol. 65, 181-185. doi: 10. 1016/j. pmpp. 2005. 01. 005
45. Koch, K. (2004). Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr. Opin. Plant Biol. 7, 235-246. doi: 10. 1016/j. pbi. 2004. 03. 014
46. 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. doi: 10. 1093/bioinformatics/bti236
47. Kube, M., Mitrovic, J., Duduk, B., Rabus, R., and Seemüller, E. (2012). Current view on phytoplasma genomes and encoded metabolism. Scientific World Journal 2012: 185942. doi: 10. 1100/2012/185942
48. Landi, L., and 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. doi: 10. 1021/jf104297n
49. 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. doi: 10. 1093/jxb/ert394
50. Lee, I. -M., Martini, M., Marcone, C., and 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. doi: 10. 1099/ijs. 0. 02697-0
51. Lee, I. -M., Zhao, Y., Davis, R. E., Wei, W., and Martini, M. (2007). Prospects of DNA-based systems for differentiation and classification of phytoplasmas. Bull. Insectol. 60, 239-244.
52. 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. doi: 10. 3389/fpls. 2013. 00272
53. Leon, R., Sanatamaria, J. M., Alpizar, L., Escamilla, J. A., and Oropeza, C. (1996). Physiological and biochemical changes in shoots of coconut palms affected by lethal yellowing. New Phytol. 134, 227-234. doi: 10. 1111/j. 1469-8137. 1996. tb04627. x
54. Lepka, P., Stitt, M., Moll, E., and 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. doi: 10. 1006/pmpp. 1999. 0202
55. 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. doi: 10. 1104/pp. 113. 229740
56. Maejima, K., Oshima, K., and Namba, S. (2014). Exploring the phytoplasmas, plant pathogenic bacteria. J. Gen. Plant Pathol. 80, 210-221. doi: 10. 1007/s10327-014-0512-8
57. Malembic-Maher, S., Salar, P., Filippin, L., Carle, P., Angelini, E., and 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. doi: 10. 1099/ijs. 0. 025411-0
58. Marcone, C. (2014). Molecular biology and pathogenicity of phytoplasmas. Ann. Appl. Biol. 165, 199-221. doi: 10. 1111/aab. 12151
59. Margaria, P., Abbà, S., and 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. doi: 10. 1186/1471-2164-14-38
60. Margaria, P., Ferrandino, A., Caciagali, P., Kedrina, O., Schubert, A., and 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. doi: 10. 1111/pce. 12332
61. Margaria, P., and Palmano, S. (2011). Response of the Vitis vinifera L. cv. 'Nebbiolo' proteome to Flavescence dorée phytoplasma infection. Proteomics 11, 212-224. doi: 10. 1002/pmic. 201000409
62. 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. doi: 10. 1007/s11306-012-0473-x
63. Maust, B. E., Espadas, F., Talavera, C., Aguilar, M., Santamaría, J. M., and Oropeza, C. (2003). Changes in carbohydrate metabolism in coconut palms infected with the lethal yellowing phytoplasma. Phytopathology 93, 976-981. doi: 10. 1094/PHYTO. 2003. 93. 8. 976
64. Mehle, N., Rupar, M., Seljak, G., Ravnikar, M., and Dermastia, M. (2011). Molecular diversity of 'flavescence dorée' phytoplasma strains in Slovenia. Bull. Insectol. 64, S29-S30.
65. 2+ influx is involved in sieve-tube blockage. Mol. Plant Microbe Interact. 26, 379-386. doi: 10. 1094/MPMI-08-12-0207-R
66. 2 in the recovery of grapevine (Vitis vinifera, cv. Prosecco) from Flavescence dorée disease. Funct. Plant Biol. 34, 750-758. doi: 10. 1071/FP06308
67. Nelson, N. (1944). Photometric adaptation of the somogyi method for determination of glucose. J. Biol. Chem. 153, 375-380.
68. Nicolaisen, M., and 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. doi: 10. 1111/j. 1439-0434. 2007. 01372. x
69. 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. doi: 10. 1371/journal. pone. 0036882
70. 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. doi: 10. 1016/j. meegid. 2009. 05. 009
71. Prezelj, N., Nikolić, P., Gruden, K., Ravnikar, M., and Dermastia, M. (2013). Spatiotemporal distribution of flavescence dorée phytoplasma in grapevine. Plant Pathol. 62, 760-766. doi: 10. 1111/j. 1365-3059. 2012. 02693. x
72. 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. doi: 10. 1099/ijs. 0. 044750-0
73. Roitsch, T. (1999). Source-sink regulation by sugar and stress. Curr. Opin. Plant Biol. 2, 198-206. doi: 10. 1016/S1369-5266(99)80036-3
74. Roitsch, T., and Ehness, R. (2000). Regulation of source/sink relations by cytokinins. Plant Growth Regul. 32, 359-367. doi: 10. 1023/A: 1010781500705
75. Roitsch, T., and González, M. C. (2004). Function and regulation of plant invertases: sweet sensations. Trends Plant Sci. 9, 606-613. doi: 10. 1016/j. tplants. 2004. 10. 009
76. Rojas, C. M., Senthil-Kumar, M., Tzin, V., and Mysore, K. S. (2014). Regulation of primary metabolism during plant-pathogen interactions and its contribution to plant. Front. Plant Sci. 5: 17. doi: 10. 3389/fpls. 2014. 00017
77. Rolland, F., Moore, B., and Sheen, J. (2002). Sugar sensing and signalling in plants. Plant Cell 14, 185-205. doi: 10. 1146/annurev. arplant. 57. 032905. 105441
78. Ruan, Y. -L., Jin, Y., Li, G. J., Yang, Y. J., and 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. doi: 10. 1093/mp/ssq044
79. Rusjan, D., Halbwirth, H., Stich, K., Mikulič-Petkovšek, M., and 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. doi: 10. 1007/s10658-012-9988-2
80. Rusjan, D., and 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. doi: 10. 1111/ajgw. 12106
81. Rusjan, D., Veberič, R., and 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. doi: 10. 1007/s10658-012-9967-7
82. Sabanadzovic, S., Abou-Ghanem, N., Castellano, M. A., Digiaro, M., and Martelli, G. P. (2000). Grapevine fleck virus-like viruses in Vitis. Arch. Virol. 145, 553-565. doi: 10. 1007/s007050050046
83. Santi, S., De Marco, F., Polizzotto, R., Grisan, S., and Musetti, R. (2013a). Recovery from stolbur disease in grapevine involves changes in sugar transport and metabolism. Front. Plant Sci. 4: 171. doi: 10. 3389/fpls. 2013. 00171
84. Santi, S., Grisan, S., Pierasco, A., De Marco, F., and 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. doi: 10. 1111/j. 1365-3040. 2012. 02577. x
85. Scharte, J., Schön, H., and Weis, E. (2005). Photosynthesis and carbohydrate metabolism in tobacco leaves during an incompatible interaction with Phytophthora ncotianae. Plant Cell Environ. 28, 1421-1435. doi: 10. 1111/j. 1365-3040. 2005. 01380. x
86. 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. doi: 10. 1111/j. 1365-294X. 2004. 02111. x
87. Smith, A. M., Zeeman, S. C., and Smith, S. M. (2005). Starch degradation. Annu. Rev. Plant Biol. 56, 73-98. doi: 10. 1146/annurev. arplant. 56. 032604. 144257
88. Solfanelli, C., Poggi, A., Loreti, E., Alpi, A., and Perata, P. (2006). Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol. 140, 637-646. doi: 10. 1104/pp. 105. 072579
89. Steffeck, R., Reisenzein, H., and Zeisner, N. (2007). Analysis of the pest risk from grapevine flavescence dorée phytoplasma to Austrian viticulture. OEPP/EPPO Bull. 37, 191-203. doi: 10. 1111/j. 1365-2338. 2007. 01102. x
90. Stein, S. E. (1999). An integrated method for spectrum extraction. J. Am. Soc. Mass Spectrometry 10, 770-781. doi: 10. 1016/S1044-0305(99)00047-1
91. Stitt, M., and Gibon, Y. (2014). Why measure enzyme activities in the era of systems biology? Trends Plant Sci. 19, 256-265. doi: 10. 1016/j. tplants. 2013. 11. 003
92. 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. doi: 10. 1007/s11306-007-0082-2
93. Takayanagi, T., and Yokotsuka, K. (1997). Relationship between sucrose accumulation and sucrose-metabolizing enzymes in developing grapes. Am. J. Enol. Viticult. 48, 403-407.
94. Tiessen, A., and 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. doi: 10. 3389/fpls. 2012. 00306
95. Van Damme, M., Huibers, R. P., Elberse, J., and 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. doi: 10. 1111/j. 1365-313X. 2008. 03427. x
96. 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. doi: 10. 1371/journal. pone. 0001326
97. 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. doi: 10. 1111/aab. 12025
98. Weckwerth, W. (2011). Green systems biology-from single genomes, proteomes and metabolomes to ecosystems research and biotechnology. J. Proteomics 75, 284-305. doi: 10. 1016/j. jprot. 2011. 07. 010
99. Weckwerth, W., Wenzel, K., and 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. doi: 10. 1002/pmic. 200200500
100. 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. doi: 10. 1111/tpj. 12719
101. Zhao, Y., Davis, R. E., Wei, W., and Lee, I. M. (2015). Should 'Candidatus Phytoplasma' be retained within the order Acholeplasmatales? Int. J. Syst. Evol. Microbiol. 65, 1075-1082. doi: 10. 1099/ijs. 0. 000050