Recovery from stolbur disease in grapevine involves changes in sugar transport and metabolism

Frontiers in Plant Science

Volumn 4, Issue JUN, 2013, Pages

  Santi, Simonetta ^a   De Marco, Federica ^a   Polizzotto, Rachele ^a   Grisan, Simone ^a   Musetti, Rita ^a  

^a UNIVERSITY OF UDINE   (Italy)

Author keywords

Callose; Cell wall invertase; Grapevine; Recovery; Stolbur; Sucrose synthase; Sucrose transporters

Indexed keywords

EID: 84900873806     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00171     Document Type: Article

References (69)

1. Afoufa-Bastien, D., Medici, A., Jeauffre, J., Coutos-Thévenot, P., Lemoine, R., Atanassova, R., et al. (2010). The Vitis vinifera sugar transporter gene family: phylogenetic overview and macroarray expression profiling. BMC Plant Biol. 10:245. doi: 10.1186/1471-2229-10-245
2. 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
3. Albertazzi, G., Milc, J., Caffagni, A., Francia, E., Roncaglia, E., Ferrari, F., et al. (2009). Gene expression in grapevine cultivars in response to Bois Noir phytoplasma infection. Plant Sci. 176, 792-804. doi: 10.1016/j.plantsci.2009.03.001
4. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., et al. (1997). Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402. doi: 10.1093/nar/25.17.3389
5. Amor, Y., Haigler, C. H., Johnson, S., Wainscott, M., and Delmer, D. P. (1995). A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc. Natl. Acad. Sci. U.S.A. 92, 9353-9357. doi: 10.1073/pnas.92.20.9353
6. Baroja-Fernández, E., Muñoza, F. G., Lia, J., Bahajia, A., Almagroa, G., Monteroa, M., et al. (2012). Sucrose synthase activity in the sus1/sus2/sus3/sus4 Arabidopsis mutant is sufficient to support normal cellulose and starch production. Proc. Natl. Acad. Sci. U.S.A. 109, 321-326. doi: 10.1073/pnas.1117099109
7. Barratt, D. H. P., Derbyshire, P., Findlay, K., Pike, M., Wellner, N., Lunn, J., et al. (2009). Normal growth of Arabidopsis requires cytosolic invertase but not sucrose synthase. Proc. Natl. Acad. Sci. U.S.A. 106, 13124-13129. doi: 10.1073/pnas.0900689106
8. Barratt, D. H. P., Kolling, K., Graf, A., Pike, M., Calder, G., Findlay, K., et al. (2011). Callose synthase GLS7 is necessary for normal phloem transport and inflorescence growth in Arabidopsis. Plant Physiol. 155, 328-341. doi: 10.1104/pp.110.166330
9. Belli, G., Bianco, P. A., and Conti, M. (2010). Grapevine yellows in Italy: past, present and future. J. Plant Pathol. 92, 303-326.
10. 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
11. Bertamini, M., Nedunchezhian, N., Tomasi, F., and Grando, M. S. (2002). Phytoplasma [Stolbur-subgroup (Bois Noir-BN)] infection inhibits photosynthetic pigments, ribulose-1, 5-bisphosphate carboxylase and photosynthetic activities in field grown grapevine (Vitis vinifera L. cv. Chardonnay) leaves. Physiol. Mol. Plant Pathol. 61, 357-366. doi: 10.1006/pmpp.2003.0449
12. Bieniawska, Z., Barratt, D. H. P., Garlick, A. P., Thole, V., Kruger, N. J., Martin, C., et al. (2007). Analysis of the sucrose synthase gene family in Arabidopsis. Plant J. 49, 810-828. doi: 10.1111/j.1365-313X.2006.03011.x
13. Bolouri-Moghaddam, M. R., and Van den Ende, W. (2012). Sugars and plant innate immunity. J. Exp. Bot. 63, 3989-3998. doi: 10.1093/jxb/ers129
14. Braun, E. J., and Sinclair, W. A. (1978). Translocation in phloem necrosis-diseased American elm seedlings. Phytopathology 68, 1733-1737. doi: 10.1094/Phyto-68-1733
15. Carraro, L., Ermacora, P., Loi, N., and Osler, R. (2004). The recovery phenomenon in apple proliferation infected apple trees. J. Plant Pathol. 86, 141-146.
16. Chandran, D., Inada, N., Hather, G., Kleindt, C. K., and Wildermuth, M. C. (2010). Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators. Proc. Natl. Acad. Sci. U.S.A. 107, 460-465. doi: 10.1073/pnas.0912492107
17. Chen, X.-Y., and Kim, J.-Y. (2009). Callose synthesis in higher plants. Plant Signal. Behav. 4, 489-492. doi: 10.4161/psb.4.6.8359
18. Christensen, N. M., Axelsen, K. B., Nicolaisen, M., and Schulz, A. (2005). Phytoplasmas and their interactions with hosts. Trends Plant Sci. 10, 526-535. doi: 10.1016/j.tplants.2005.09.008
19. 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
20. Coombe, B. C. (1992). Research on development and ripening of the grapeberry. Am. J. Enol. Vitic. 43, 101-110.
21. Davies, C., and Robinson, S. P. (1996). Sugar accumulation in grape berries: cloning of two putative vacuolar invertase cDNAs and their expression in grapevine tissues. Plant Physiol. 111, 275-283. doi: 10.1104/pp.111.1.275
22. Davies, C., Wolf, T., and Robinson, S. P. (1999). Three putative sucrose transporters are differentially expressed in grapevine tissues. Plant Sci. 147, 93-100. doi: 10.1016/S0168-9452(99)00059-X
23. Davis, J. K. (2012). Combining polysaccharide biosynthesis and transport in a single enzyme: dual-function cell wall glycan synthases. Front. Plant Sci. 3:138. doi: 10.3389/fpls.2012.00138 doi: 10.3389/fpls.2012.00138
24. Ehlers, K., Knoblauch, M., and van Bel, A. J. E. (2000). Ultrastructural features of well-preserved and injured sieve elements: minute clamps keep the phloem transport conduits free for mass flow. Protoplasma 214, 80-92. doi: 10.1007/BF02524265
25. Endeshaw, S. T., 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
26. Endler, A., Meyer, S., Schelbert, S., Schneider, T., Weschke, W., Peters, S. W., et al. (2006). Identification of a vacuolar sucrose transporter in barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach. Plant Physiol. 141, 196-207. doi: 10.1104/pp.106.079533
27. Essmann, J., Schmitz-Thom, I., Schon, H., Sonnewald, S., Weis, E., and Scharte, J. (2008). RNA interference-mediated repression of cell wall invertase impairs defense in source leaves of tobacco. Plant Physiol. 147, 1288-1299. doi: 10.1104/pp.108.121418
28. Firrao, G., Gibb, K., and Stereten, C. (2005). Short taxonomic guide to the genus 'Candidatus phytoplasma'. J. Plant Pathol. 87, 249-263. doi: 10.4454/jpp.v87i4.926
29. Fotopoulos, V., Gilbert, M. J., Pittman, J. K., Marvier, A. C., Buchanan, A. J., Sauer, N., et al. (2003). The monosaccharide transporter gene, AtSTP4 and the cell-wall invertase, at beta fruct1, are induced in Arabidopsisduring infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol. 132, 821-829. doi: 10.1104/pp.103.021428
30. Fujii, S., Hayashi, T., and Mizuno, K. (2010). Sucrose synthase is an integral component of the cellulose synthesis machinery. Plant Cell Physiol. 51, 294-301. doi: 10.1093/pcp/pcp190
31. +-mediated remote control of reversible sieve tube occlusion in Vicia faba. J. Exp. Bot. 58, 2827-2838. doi: 10.1093/jxb/erm143
32. Hayes, A., Feechan, A., and Dry, I. B. (2010). Involvement of abscisic acid in the coordinated regulation of a stress-inducible hexose transporter (VvHT5) and a cell wall invertase in grapevine in response to biotrophic fungal infection. Plant Physiol. 153, 211-221. doi: 10.1104/pp.110.154765
33. Hren, M., Nikolic, 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
34. Hren, M., Ravnikar, M., Brzin, J., Ermacora, P., Carraro, L., Bianco, P. A., 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
35. Kartte, S., and Seemüller, E. (1991). Histopathology of apple proliferation in Malus taxa and hybrids of different susceptibility. J. Phytopathol. 131, 149-160. doi: 10.1111/j.1439-0434.1991.tb04740.x
36. Knoblauch, M., and van Bel, A. J. E. (1998). Sieve tubes in action. Plant Cell 10, 35-50.
37. 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
38. Lee, I. M., Davis, R. E., and Gundersen-Rindal, D. E. (2000). Phytoplasma: phytopathogenic mollicutes. Annu. Rev. Microbiol. 54, 221-255. doi: 10.1146/annurev.micro.54.1.221
39. 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
40. 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
41. 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
42. Muller, P. Y., Janovjak, H., Miserez, A. R., and Dobbie, Z. (2002). Processing of gene expression data generated by quantitative realtime RT-PCR. Biotechniques 32, 1372-1379.
43. + influx is involved in sieve-tube blockage. Mol. Plant Microbe Interact. 26, 379-386. doi: 10.1094/MPMI-08-12-0207-R
44. Musetti, R., and Favali, M. A. (1999). Histological and ultrastructural comparative study between Prunus varieties of different susceptibility to plum leptonecrosis. Cytobios 99, 73-82.
45. Musetti, R., Favali, M. A., Carraro, L., and Osler, R. (1994). Histological detection of Mycoplasma-like organisms causing leptonecrosis in plum trees. Cytobios 78, 81-90.
46. 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. doi: 10.1071/FP06308
47. Musetti, R., Paolacci, A., Ciaffi, M., Tanzarella, O. A., Polizzotto, R., Tubaro, F., et al. (2010). Phloem cytochemical modification and gene expression following the recovery of apple plants from apple proliferation disease. Phytopathology 100, 390-399. doi: 10.1094/PHYTO-100-4-0390
48. Musetti, R., Sanità di Toppi, L., Ermacora, P., and Favali, M. A. (2004). Recovery in apple trees infected with the apple proliferation phytoplasma: An ultrastructural and biochemical study. Phytopathology 94, 203-208. doi: 10.1094/PHYTO.2004.94.2.203
49. Musetti, R., Sanità di Toppi, L., Martini, M., Ferrini, F., Loschi, A., Favali, M. A., et al. (2005). Hydrogen peroxide localization and antioxidant status in the recovery of apricot plants from European Stone Fruit Yellows. Eur. J. Plant Pathol. 112, 53-61. doi: 10.1007/s10658-004-8233-z
50. Nakashima, J., Laosinchai, W., Cui, X., and Brown, R. M. (2003). New insight into the mechanism of cellulose and callose biosynthesis: proteases may regulate callose biosynthesis upon wounding. Cellulose 10, 369-386. doi: 10.1023/A:1027336605479
51. Osler, R., Carraro, L., Loi, N., and Refatti, E. (1993). Symptom expression and disease occurrence of a yellows disease of grapevine in northeastern Italy. Plant Dis. 77, 496-498. doi: 10.1094/PD-77-0496
52. Osler, R., Loi, N., Carraro, L., Ermacora, P., and Refatti, E. (2000). "Recovery in plants affected by phytoplasmas", in Proceedings 5th Congress of the European Foundation for Plant Pathology, ed. Società Italiana di Patologia Vegetale, Taormina, 589-592.
53. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acid Res. 29, e45.
54. Reinders, A., Sivitz, A. B., and Ward, J. M. (2012). Evolution of plant sucrose uptake transporters (SUTs). Front. Plant Sci. 3:22. doi: 10.3389/fpls.2012.00022
55. Roitsch, T., Balibrea, M. E., Hofmann, M., Proels, R., and Sinha, A. K. (2003). Extracellular invertase: key metabolic enzyme and PR protein. J. Exp. Bot. 54, 513-524.
56. Roitsch, T., and Gonzàlez, 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
57. Rolland, F., Baena-Gonzalez, E., and Sheen, J. (2006). Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu. Rev. Plant Biol. 57, 675-709. doi: 10.1146/annurev.arplant.57.032905.105441
58. Santi, S., Grisan, S., Pierasco, A., De Marco, F., and Musetti, R. (2013). 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
59. Sauer, N. (2007). Molecular physiology of higher plant sucrose transporters. FEBS Lett. 581, 2309-2317. doi: 10.1016/j.febslet.2007.03.048
60. Solfanelli, C., Poggi, A., Loreti, E., Alpi, A., and Perata G. (2006). Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol. 140, 637-646. doi: 10.1104/pp.105.072579
61. Sutton, P. N., Gilbert, M. J., Williams, L. E., and Hall, J. L. (2007). Powdery mildew infection of wheat leaves changes host solute transport and invertase activity. Physiol. Plant. 129, 787-795. doi: 10.1111/j.1399-3054.2007.00863.x
62. van Bel, A. J. E., Ehlers, K., and Knoblauch, M. (2002). Sieve elements caught in the act. Trends Plant Sci. 7, 126-132. doi: 10.1016/S1360-1385(01)02225-7
63. van der Schoot, C., and van Bel, A. J. E. (1989). Glass microelectrode measurements of sieve tube membrane potentials in internode discs and petiole strips of tomato (Solanum lycopersicon L.). Protoplasma 149, 144-154. doi: 10.1007/BF01322986
64. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., et al. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, research 0034. doi: 10.1186/gb-2002-3-7-research0034
65. Verma, D. P. S., and Hong, Z. (2001). Plant callose synthase complexes. Plant Mol. Biol. 47, 693-701. doi: 10.1023/A:1013679111111
66. Weisburg, W. G., Tully, J. G., Rose, D. L., Petzel, J. P., Oyaizu, H., Yang, D., et al. (1989). A phylogenetic analysis of the mycoplasmas: basis for their classification. J. Bacteriol. 171, 6455-6467.
67. Winkel-Shirley, B. (2001). Flavonoid biosynthesis: a colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol. 126, 485-493. doi: 10.1104/pp.126.2.485
68. Winter, H., and Huber, S. (2000). Regulation of sucrose metabolism in higher plants: localisation and regulation of activity of key enzymes. Crit. Rev. Plant Sci. 19, 31-67. doi: 10.1016/S0735-2689(01)80002-2
69. Xie, B., Wang, X., Zhu, M., Zhang, Z., and Hong, Z. (2011). CalS7 encodes a callose synthase responsible for callose deposition in the phloem. Plant J. 65, 1-14. doi: 10.1111/j.1365-313X.2010.04399.x