Alterations in primary and secondary metabolism in Vitis vinifera ‘Malvasía de Banyalbufar’ upon infection with Grapevine leafroll-associated virus 3

Physiologia Plantarum

Volumn 157, Issue 4, 2016, Pages 442-452

  Montero, Rafael ^a   Pérez Bueno, María Luisa ^b   Barón, Matilde ^b   Florez Sarasa, Igor ^c   Tohge, Takayuki ^c   Fernie, Alisdair Robert ^c   ouad, Hanan El aou ^d   Flexas, Jaume ^d   Bota, Josefina ^d  

^a Govern de les Illes Balears   (Spain)

^b CSIC   (Spain)

^c MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^d UNIVERSITAT DE LES ILLES BALEARS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RESPIRATION; CLOSTEROVIRIDAE; FLUORESCENCE; LIGHT; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; RADIATION RESPONSE; SECONDARY METABOLISM; VIROLOGY; VITIS;

CELL RESPIRATION; CLOSTEROVIRIDAE; FLUORESCENCE; LIGHT; PHOTOSYNTHESIS; PLANT DISEASES; PLANT LEAVES; SECONDARY METABOLISM; VITIS;

EID: 85027933444     PISSN: 00319317     EISSN: 13993054     Source Type: Journal    
DOI: 10.1111/ppl.12440     Document Type: Article

References (62)

1. Araújo WL, Nunes-Nesi A, Osorio S, Usadel B, Fuentes D, Nagy R, Balbo I, Lehmann M, Studart-Witkowski C, Tohge T, Martinoia E, Jordana X, DaMatta F, Fernie AR (2011) Antisense inhibition of the iron-sulphur subunit of succinate dehydrogenase enhances photosynthesis and growth in tomato via an organic acid-mediated effect on stomatal aperture. Plant Cell 23: 600–627
2. Balachandran S, Osmond BC (1994) Susceptibility of tobacco leaves to photoinhibition following infection with two strains of tobacco mosaic virus under different light and nitrogen nutrition regimes. Plant Physiol 104: 1051–1057
3. Balachandran S, Hurry VM, Kelley SE, Osmond CB, Robinson SA, Rohozinski J, Seaton GGR, Sims DA (1997) Concepts of plant biotic stress. Some insights into the stress physiology of virus-infected plants, from the perspective of photosynthesis. Physiol Plant 100: 203–213
4. Barón M, Flexas J, Delucia EH (2012) Photosynthetic responses to biotic stress. In: Flexas J, Loreto F, Medrano H (eds) Terrestrial Photosynthesis in a Changing Environment: A Molecular, Physiological, and Ecological Approach. Cambridge University Press, Cambridge, UK, pp 331–350
5. Basso MF, Fajardo TVM, Eiras M, Ayub RA, Nickel O (2010) Detecção e identificação molecular de vírus associados a videiras sintomáticas e assintomáticas. Ciência Rural 40: 2249–2255
6. Bauer N, Fulgosi H, Jelaska S (2011) Overexpression of phenylalanine ammonia-lyase in transgenic roots of Coleus blumei alters growth and rosmarinic acid synthesis. Food Technol Biotechnol 49: 24–31
7. Berger S, Papadopoulos M, Schreiber U, Kaiser W, Roitsch T (2004) Complex regulation of gene expression, photosynthesis and sugar levels by pathogen infection in tomato. Physiol Plant 122: 419–428
8. Berger S, Benediktyová Z, Matouš K, Bonfig K, Mueller MJ, Nedbal L, Roitsch T (2007) Visualization of dynamics of plant-pathogen interaction by novel combination of chlorophyll fluorescence imaging and statistical analysis: differential effects of virulent and avirulent strains of P. syringae and of oxylipins on A. thaliana. J Exp Bot 58: 797–806
9. Bonfig KB, Schreiber U, Gabler A, Roitsch T, Berger S (2006) Infection with virulent and avirulent P. syringae strains differentially effects photosynthesis and sink metabolism in Arabidopsis leaves. Planta 225: 1–12
10. Buschmann C, Lichtenthaler HK (1998) Principles and characteristics of multi-colour fluorescence imaging of plants. J Plant Physiol 152: 297–314
11. Buschmann C, Langsdorf G, Lichtenthaler HK (2000) Imaging of the blue, green, and red fluorescence emission of plants: an overview. Photosynthetica 38: 483–491
12. Cerovic ZG, Samson G, Morales F, Tremblay N, Moya I (1999) Ultraviolet-induced fluorescence for plant monitoring: present state and prospects. Agronomie 19: 543–578
13. Cerovic ZG, Ounis A, Cartelat A, Latouche G, Goulas Y, Meyer S, Moya I (2002) The use of chlorophyll fluorescence excitation spectra for the non-destructive in situ assessment of UV-absorbing compounds in leaves. Plant Cell Environ 25: 1663–1676
14. Chaerle L, Hagenbeek D, De Bruyne E, Valcke R, Van Der Straeten D (2004) Thermal and chlorophyll-fluorescence imaging distinguish plant pathogen interaction at an early stage. Plant Cell Physiol 45: 887–896
15. Charles JG, Froud KJ, van der Brink R, Allan DJ (2009) Mealybugs and the spread of Grapevine leafroll-associated virus 3 (GLRaV-3) in a New Zealand vineyard. Australas Plant Pathol 38: 576–583
16. Chou HM, Bundock N, Rolfe AS, Scholes DJ (2000) Infection of Arabidopsis thaliana leaves with Albugo candida (white blister rust) causes a reprogramming of host metabolism. Mol Plant Pathol 2: 99–113
17. Christov I, Stefanov D, Velinov T, Goltsev V, Georgieva K, Abracheva P (2007) The symptomless leaf infection with grapevine leafroll associated virus 3 in grown in vitro plants as a simple model system for investigation of viral effects on photosynthesis. J Plant Physiol 164: 1124–1133
18. Clark MF, Adams AN (1977) Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. J Gen Virol 34: 475–483
19. Dixon RA, Achnine L, Kota P, Liu CJ, Srinivasa Reddy MS, Wang L (2002) The phenylpropanoid pathway and plant defence – a genomics perspective. Mol Plant Pathol 3: 371–390
20. Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11: 539–548
21. Endeshaw ST, Sabbatini P, Romanazzi G, Annemiek C, Schilder AC, Neri D (2014) Effects of grapevine leafroll associated virus 3 infection on growth,leaf gas exchange, yield and basic fruit chemistry of Vitis vinifera L. cv. Cabernet Franc. Sci Hortic 170: 228–236
22. Fujiwara A, Shimura H, Masuta C, Sano S, Inukai T (2011) Exogenous ascorbic acid derivatives and dehydroascorbic acid are effective antiviral agents against Turnip mosaic virus in Brassica rapa. J Gen Plant Pathol 79: 198–204
23. Gambino G, Cuozzo D, Fasoli M, Pagliarani C, Vitali M, Boccacci P, Pezzotti M, Mannini F (2012) Co-evolution between Grapevine rupestris stem pitting-associated virus and Vitis vinifera L. leads to decreased defence responses and increased transcription of genes related to photosynthesis. J Exp Bot 63: 5919–5933
24. Granum E, Pérez-Bueno ML, Calderón CE, Ramos C, de Vicente A, Cazorla FM, Barón M (2015) Metabolic responses of avocado plants to stress induced by Rosellinia necatrix analysed by fluorescence and thermal imaging. Eur J Plant Pathol 142: 625–632
25. Gutha RL, Casassa LF, Harbertson JF, Rayapati A, Naidu RA (2010) Modulation of flavonoid biosynthetic pathway genes and anthocyanins due to virus infection in grapevine (Vitis vinifera L.) leaves. BMC Plant Biol 10: 187
26. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circ Calif Agric Exp Sta 347: 1–32
27. Kangasjärvi S, Neukermans J, Li S, Aro EM, Noctor G (2012) Photosynthesis, photorespiration, and light signalling in defence responses. J Exp Bot 63: 1619–1636
28. Komar V, Vigne E, Demangeat G, Fuchs M (2007) Beneficial effect of selective virus elimination on the performance of Vitis vinifera cv. Chardonnay. Am J Enol Vitic 58: 202–210
29. Kopka J, Schauer N, Krueger S, Birkemeyer C, Usadel B, Bergmüller E, Dörmann P, Weckwerth W, Gibon Y, Stitt M, Willmitzer L, Fernie AR, Steinhauser D (2005) GMD@CSB.DB: the Golm Metabolome Database. Bioinformatics 21: 1635–1638
30. Kovermann P, Meyer S, Hortensteiner S, Picco C, Scholz-Starke J, Ravera S, Lee Y, Martinoia E (2007) The Arabidopsis vacuolar malate channel is a member of the ALMT family. Plant J 52: 1169–1180
31. Lichtenthaler HK, Miehé JA (1997) Fluorescence imaging as a diagnostic tool for plant stress. Trends Plant Sci 2: 316–320
32. Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Protoc 1: 387–396
33. Lohaus G, Heldt HW, Osmond CB (2000) Infection with phloem limited Abutilon mosaic virus causes localized carbohydrate accumulation in leaves of Abutilon striatum: relationships to symptom development and effects on chlorophyll fluorescence quenching during photosynthetic induction. Plant Biol 2: 161–167
34. Maree HJ, Almeida RPP, Bester R, Chooi KM, Cohen D, Dolja VV, Fuchs MF, Golino DA, Jooste AEC, Martelli GP, Naidu RA, Rowhani A, Saldarelli P, Burger JT (2013) Grapevine leafroll-associated virus 3. Front Microbiol 4: 82
35. Martelli GP (2012) Grapevine virology highlights 2010–2012. Proceedings of the 17th Meeting of the International Council for the Study of Virus and Virus-like Diseases of the Grapevine. ICVG, Davis, California, USA, October 7–14, 2012, pp. 13–32
36. Morales F, Cartelat A, Alvarez-Fernández A, Moya I, Cerovic ZG (2005) Time-resolved spectral studies of blue-green fluorescence of artichoke (Cynara cardunculus L. var. Scolymus) leaves: identification of chlorogenic acid as one of the major fluorophores and age-mediated changes. J Agric Food Chem 53: 9668–9678
37. Moutinho-Pereira J, Correia CM, Gonçalves B, Bacelar EA, Coutinho JF, Ferreira HF, Lousada JL, Cortez MI (2012) Impacts of leafroll-associated viruses (GLRaV-1 and -3) on the physiology of the Portuquese grapevine cultivar ‘Touringa Nacional’ growing under field conditions. Ann Appl Biol 3: 237–249
38. Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64: 3983–3998
39. Osman F, Rowhani A (2008) Real-time RT-PCR (TaqMan®) assays for the detection of viruses associated with Rugose wood complex of grapevine. J Virol Meth 154: 69–75
40. Osman F, Leutenegger C, Golino D, Rowhani A (2007) Real-time RT-PCR (TaqMan®) assays for the detection of Grapevine leafroll associated viruses 1–5 and 9. J Virol Meth 141: 22–29
41. Osmond CB, Daley PF, Badger MR, Lüttge U (1998) Chlorophyll fluorescence quenching during photosynthetic induction in leaves of Abutilon striatum Dicks infected with Abutilon mosaic virus observed with a field-portable imaging system. Bot Acta 111: 390–397
42. Pacifico D, Caciagli P, Palmano S, Mannini F, Marzachì C (2011) Quantitation of Grapevine leafroll associated virus-1 and -3, Grapevine virus A, Grapevine fanleaf virus and Grapevine fleck virus in field-collected Vitis vinifera L. ‘Nebbiolo’ by real-time reverse transcription-PCR. J Virol Meth 172: 1–7
43. Parker D, Beckmann M, Zubair H, Enot DP, Caracuel-Rios Z, Overy DP, Snowdon S, Talbot NJ, Draper J (2009) Metabolomic analysis reveals a common pattern of metabolic re-programming during invasion of three host plant species by Magnaporthe grisea. Plant J 59: 723–737
44. Pérez-Bueno ML, Ciscato M, vandeVen M, García-Luque I, Valcke R, Barón M (2006) Imaging viral infection: studies on Nicotiana benthamiana plants infected with the pepper mild mottle tobamovirus. Photosynth Res 90: 111–123
45. Pérez-Bueno ML, Pineda M, Díaz-Casado E, Barón M (2014) Spatial and temporal dynamics of primary and secondary metabolism in Phaseolus vulgaris challenged by Pseudomonas syringae. Physiol Plant 153: 161–174
46. Petit AN, Vaillant N, Boulay M, Clement C, Fontaine F (2006) Alteration of photosynthesis in grapevines affected by esca. Phytopathology 96: 1060–1066
47. Pineda M, Soukupova J, Matouš K, Nedbal L, Barón M (2008a) Conventional and combinatorial chlorophyll fluorescence imaging of tobamovirus-infected plants. Photosynthetica 46: 441–451
48. Pineda M, Gáspár L, Morales F, Szigeti Z, Barón M (2008b) Multicolor fluorescence imaging of leaves – a useful tool for visualizing systemic viral infections in plants. Photochem Photobiol 84: 1048–1060
49. Rodríguez-Moreno L, Pineda M, Soukupová J, Macho AP, Beuzón CR, Barón M, Ramos C (2008) Early detection of bean infection by Pseudomonas syringae in asymptomatic leaf areas using chlorophyll fluorescence imaging. Photosynth Res 96: 27–35
50. Roessner U, Luedemann A, Brust D, Fiehn O, Linke T, Willmitzer L, Fernie AR (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13: 11–29
51. Sampol B, Bota J, Riera D, Medrano H, Flexas J (2003) Analysis of the virus-induced inhibition of photosynthesis in malmsey grapevines. New Phytol 160: 403–412
52. Schauer N, Steinhauser D, Strelkov S, Schomburg D, Allison G, Moritz T, Lundgren K, Roessner-Tunali U, Forbes MG, Willmitzer L, Fernie AR, Kopka J (2005) GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Lett 579: 1332–1337
53. Scholes JD, Rolfe SA (2009) Chlorophyll fluorescence imaging as tool for understanding the impact of fungal diseases on plant performance: a phenomics perspective. Funct Plant Biol 36: 880–892
54. Schulze J, Tesfaye M, Litjens RHMG, Bucciarelli B, Trepp G, Miller S, Samac D, Allan D, Vance CP (2002) Malate plays a central role in plant nutrition. Plant Soil 247: 133–139
55. Sefc KM, Leonhardt W, Steinkellner H (2000) Partial sequence identification of grapevine-leafroll-associated virus-1 and development of a highly sensitive IC-RT-PCR detection method. J Virol Meth 86: 101–106
56. Sørhagen K, Laxa M, Peterhansel C, Reumann S (2013) The emerging role of photorespiration and non-photorespiratory peroxisomal metabolism in pathogen defence. Plant Biol 15: 723–736
57. Swarbrick PJ, Schulze-Lefert P, Scholes JD (2006) Metabolic consequences of susceptibility and resistance (race-specific and broad-spectrum) in barley leaves challenged with powdery mildew. Plant Cell Environ 29: 1061–1076
58. Szigeti Z, Almási A, Sárvári E (2002) Changes in the photosynthetic functions in leaves of Chinese cabbage infected with Turnip yellow mosaic virus. Acta Biologica Szegediensis 46: 137–138
59. Tohge T, Fernie AR (2010) Combining genetic diversity, informatics and metabolomics to facilitate annotation of plant gene function. Nat Protoc 5: 1210–1227
60. Tsai CW, Daugherty MP, Almeida RPP (2012) Seasonal dynamics and virus translocation of Grapevine leafroll-associated virus 3 in grapevine cultivars. Plant Pathol 61: 977–985
61. Vega A, Gutierrez R, Peña-Neira A, Cramer G, Arce-Johnson P (2011) Compatible GLRaV-3 viral infections affect berry ripening decreasing sugar accumulation and anthocyanin biosynthesis in Vitis vinifera. Plant Mol Biol 77: 261–274
62. Velasco L, Bota J, Montero R, Cretazzo E (2014) Differences of three ampeloviruses multiplication in plant contribute to explain their incidences in vineyards. Plant Dis 98: 395–400