Salicylic acid is an indispensable component of the Ny-1 resistance-gene-mediated response against Potato virus y infection in potato

Journal of Experimental Botany

Volumn 65, Issue 4, 2014, Pages 1095-1109

  Baebler, S ^a   Witek, K ^b,e   Petek, M ^a   Stare, K ^a   Tusek Znidaric M ^a   Pompe Novak, M ^a   Renaut, J ^c   Szajko, K ^d   Strzelczyk Zyta, D ^d   Marczewski, W ^d   Morgiewicz, K ^b   Gruden, K ^a   Hennig, J ^b  

^a NATIONAL INSTITUTE OF BIOLOGY   (Slovenia)

^b INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^c LUXEMBOURG INSTITUTE OF SCIENCE AND TECHNOLOGY   (Luxembourg)

^d PLANT BREEDING AND ACCLIMATIZATION INSTITUTE NATIONAL RESEARCH INSTITUTE   (Poland)

^e SAINSBURY LABORATORY   (United Kingdom)

Author keywords

Plant pathogen interactions; Potato virus Y; Potyviridae; salicylic acid; Solanum tuberosum; whole transcriptome analysis.

Indexed keywords

CYCLOPENTANE DERIVATIVE; ETHYLENE; ETHYLENE DERIVATIVE; JASMONIC ACID; OXYLIPIN; PHYTOHORMONE; REACTIVE OXYGEN METABOLITE; SALICYLIC ACID; TRANSCRIPTOME; VEGETABLE PROTEIN;

APOPTOSIS; ARTICLE; DOWN REGULATION; ENERGY METABOLISM; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT DISEASE; PLANT IMMUNITY; PLANT LEAF; PLANT-PATHOGEN INTERACTIONS; POTATO; POTYVIRUS; SIGNAL TRANSDUCTION; VIROLOGY; WHOLE TRANSCRIPTOME ANALYSIS.;

PLANT-PATHOGEN INTERACTIONS; POTATO VIRUS Y; POTYVIRIDAE; SALICYLIC ACID; SOLANUM TUBEROSUM; WHOLE TRANSCRIPTOME ANALYSIS.;

APOPTOSIS; CYCLOPENTANES; DOWN-REGULATION; ENERGY METABOLISM; ETHYLENES; GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; OXYLIPINS; PHOTOSYNTHESIS; PLANT DISEASES; PLANT GROWTH REGULATORS; PLANT IMMUNITY; PLANT LEAVES; PLANT PROTEINS; POTYVIRUS; REACTIVE OXYGEN SPECIES; SALICYLIC ACID; SIGNAL TRANSDUCTION; SOLANUM TUBEROSUM; TRANSCRIPTOME;

EID: 84903363229     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert447     Document Type: Article

References (74)

1. Alamillo JM, Saénz P, García JA. 2006. Salicylic acid-mediated and RNA-silencing defense mechanisms cooperate in the restriction of systemic spread of plum pox virus in tobacco. The Plant Journal 48, 217-227..
2. Baebler S, Krei-Stres H, Rotter A, et al. 2009. PVYNTN elicits a diverse gene expression response in different potato genotypes in the first 12 h after inoculation. Molecular Plant Pathology 10, 263-275..
3. Baebler S, Stare K, Kova M, et al. 2011. Dynamics of responses in compatible potato-Potato virus Y interaction are modulated by salicylic acid. PloS One 6, e29009..
4. 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. Physiologia Plantarum 122, 419-428..
5. Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, DeLucia EH. 2010. Biotic stress globally downregulates photosynthesis genes. Plant, Cell and Environment 33, 1597-1613..
6. Bolton MD. 2009. Primary metabolism and plant defense-fuel for the fire. Molecular Plant-Microbe Interactions 22, 487-497..
7. Chandra-Shekara AC, Gupte M, Navarre D, Raina S, Raina R, Klessig D, Kachroo P. 2006. Light-dependent hypersensitive response and resistance signaling against Turnip Crinkle Virus in Arabidopsis. The Plant Journal 45, 320-334..
8. Chen H, Nelson RS, Sherwood JL. 1994. Enhanced recovery of transformants of Agrobacterium tumefaciens after freeze-thaw transformation and drug selection. Biotechniques 16, 664-8, 670..
9. Chou HM, Bundock N, Rolfe SA, Scholes JD. 2000. Infection of Arabidopsis thaliana leaves with Albugo candida (white blister rust) causes a reprogramming of host metabolism. Molecular Plant Pathology 1, 99-113..
10. Chrzanowska M. 1991. New isolates of the necrotic strain of Potato virus Y (PVYN) found recently in Poland. Potato Research 34, 179-182..
11. Di Carli M, Benvenuto E, Donini M. 2012. Recent Insights into plant-virus interactions through proteomic analysis. Journal of Proteome Research 11, 4765-4780..
12. Dobnik D, Baebler S, KogovSek P, Pompe-Novak M, Stebih D, Panter G, Janez N, Morisset D, Zel J, Gruden K. 2013. 1,3-glucanase class III promotes spread of PVYNTN and improves in planta protein production. Plant Biotechnology Reports 7, 547-555..
13. Du Y, Tejos R, Beck M, Himschoot E, Li H, Robatzek S, Vanneste S, Friml J. 2013. Salicylic acid interferes with clathrinmediated endocytic protein trafficking. Proceedings of the National Academy of Sciences, USA 110, 7946-7951..
14. Edgar R, Domrachev M, Lash AE. 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Research 30, 207-210..
15. Halim VA, Altmann S, Ellinger D, Eschen-Lippold L, Miersch O, Scheel D, Rosahl S. 2009. PAMP-induced defense responses in potato require both salicylic acid and jasmonic acid. The Plant Journal 57, 230-242..
16. Halim VA, Eschen-Lippold L, Altmann S, Birschwilks M, Scheel D, Rosahl S. 2007. Salicylic acid is important for basal defense of Solanum tuberosum Against Phytophthora infestans. Molecular Plant- Microbe Interactions 20, 1346-1352..
17. Hennig J, Malamy J, Grynkiewicz G, Indulski J, Klessig DF. 1993. Interconversion of the salicylic acid signal and its glucoside in tobacco. The Plant Journal 4, 593-600..
18. Hinrich-Berger J. 1999. Cytological responses of susceptible and extremely resistant potato plants to inoculation with Potato virus Y. Physiological and Molecular Plant Pathology 55, 143-150..
19. Huang Z, Yeakley JM, Garcia EW, Holdridge JD, Fan JB, Whitham SA. 2005. Salicylic acid-dependent expression of host genes in compatible Arabidopsis-virus interactions. Plant Physiology 137, 1147-1159..
20. Iglesias VA, Meins F Jr. 2000. Movement of plant viruses is delayed in a beta-1,3-glucanase-deficient mutant showing a reduced plasmodesmatal size exclusion limit and enhanced callose deposition. The Plant Journal 21, 157-166..
21. Ishihara T, Sakurai N, Sekine KT, Hase S, Ikegami M, Shibata D, Takahashi H. 2004. Comparative analysis of expressed sequence tags in resistant and susceptible ecotypes of Arabidopsis thaliana infected with cucumber mosaic virus. Plant Cell Physiology 45, 470-480..
22. Jay F, Wang Y, Yu A, Taconnat L, Pelletier S, Colot V, Renou JP, Voinnet O. 2011. Misregulation of AUXIN RESPONSE FACTOR 8 underlies the developmental abnormalities caused by three distinct viral silencing suppressors in Arabidopsis. PLoS Pathogens 7, e1002035..
23. Jones JD, Dangl JL. 2006. The plant immune system. Nature 444, 323-329..
24. Jovel J, Walker M, Sanfaçon H. 2011. Salicylic acid-dependent restriction of tomato ringspot virus spread in tobacco is accompanied by a hypersensitive response, local RNA silencing, and moderate systemic resistance. Molecular Plant-Microbe Interactions 24, 706-718..
25. Kloosterman B, De Koeyer D, Griffiths R, et al. 2008. Genes driving potato tuber initiation and growth: identification based on transcriptional changes using the POCI array. Functional and Integrative Genomics 8, 329-340..
26. KogovSek P, Ravnikar M. 2013. Physiology of the potato-Potato virus Y interaction. In: Lüttge U, Beyschlag W, Francis D, Cushman J, editors, Progress in Botany 74 . Berlin, Heidelberg: Springer Berlin Heidelberg..
27. Krei-Stres H, Vuak C, Ravnikar M, Kova? M. 2005. Systemic Potato virus YNTN infection and levels of salicylic and gentisic acids in different potato genotypes. Plant Pathology 54, 441-447..
28. Krzymowska M, Konopka-Postupolska D, Sobczak M, Macioszek V, Ellis BE, Hennig J. 2007. Infection of tobacco with different Pseudomonas syringae pathovars leads to distinct morphotypes of programmed cell death. The Plant Journal 50, 253-264..
29. Lewsey M, Palukaitis P, Carr JP. 2009. Plant-virus interactions: defence and counter-defence. In: Parker J, editor, Molecular aspects of plant disease resistance . Wiley-Blackwell, Oxford. pp 134-176..
30. Mac A, Krzymowska M, Barabasz A, Hennig J. 2004. Transcriptional regulation of the gluB promoter during plant response to infection. Cellular and Molecular Biology Letters 9, 843-853..
31. Malamy J, Carr JP, Klessig DF, Raskin I. 1990. Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250, 1002-1004..
32. Malamy J, Hennig J, Klessig DF. 1992. Temperature-dependent induction of salicylic acid and its conjugates during the resistance response to tobacco mosaic virus infection. The Plant Cell 4, 359-366..
33. Marathe R, Guan Z, Anandalakshmi R, Zhao H, Dinesh-Kumar SP. 2004. Study of Arabidopsis thaliana resistome in response to cucumber mosaic virus infection using whole-genome microarray. Plant Molecular Biology 55, 501-520..
34. Mur LA, Brown IR, Darby RM, Bestwick CS, Bi YM, Mansfield JW, Draper J. 2000. A loss of resistance to avirulent bacterial pathogens in tobacco is associated with the attenuation of a salicylic acid-potentiated oxidative burst. The Plant Journal 23, 609-621..
35. Mur L, Kenton P, Lloyd AJ, Ougham H, Prats E. 2008. The hypersensitive response; the centenary is upon us but how much do we know? Journal of Experimental Botany 59, 501-520..
36. Mur LAJ, Bi YM, Darby RM, Firek S, Draper J. 1997. Compromising early salicylic acid accumulation delays the hypersensitive response and increases viral dispersal during lesion establishment in TMV-infected tobacco. The Plant Journal 12, 1113-1126..
37. Navarre DA, Mayo D. 2004. Differential characteristics of salicylic acid-mediated signaling in potato. Physiological and Molecular Plant Pathology 64, 179-188..
38. O'Brien J, Daudi A, Butt VS, Bolwell GP. 2012. Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 236, 765-779..
39. Pacheco R, García-Marcos A, Manzano A, de Lacoba MG, Camanes G, García-Agustín P, Díaz-Ruíz JR, Tenllado F. 2012. Comparative analysis of transcriptomic and hormonal responses to compatible and incompatible plant-virus interactions that lead to cell death. Molecular Plant-Microbe Interactions 25, 709-723..
40. Palukaitis P, Carr JP. 2008. Plant resistance responses to viruses. Journal of Plant Pathology 90, 153-171..
41. Peterhansel C, Freialdenhoven A, Kurth J, Kolsch R, Schulze- Lefert P. 1997. Interaction analyses of genes required for resistance responses to powdery mildew in barley reveal distinct pathways leading to leaf cell death. The Plant Cell 9, 1397-1409..
42. Pompe-Novak M, Wrischer M, Ravnikar M. 2001. Ultrastructure of chloroplasts in leaves of potato plants infected by Potato virus YNTN. Phyton 41, 215-226..
43. Postnikova O, Nemchinov LG. 2012. Comparative analysis of microarray data in Arabidopsis transcriptome during compatible interactions with plant viruses. Virology Journal 9, 101..
44. R Core Team. 2012. R: a language and environment for statistical computing . Vienna, Austria: R Foundation for Statistical Computing..
45. Renaut J, Hausman JF, Bassett C, Artlip T, Cauchie HM, Witters E, Wisniewski M. 2008. Quantitative proteomic analysis of short photoperiod and low-temperature responses in bark tissues of peach (Prunus persica L. Batsch). Tree Genetics and Genomes 4, 589-600..
46. Robert-Seilaniantz A, Grant M, Jones JD. 2011. Hormone crosstalk in plant disease and defense: more than just jasmonatesalicylate antagonism. Annual Review of Phytopathology 49, 317-343..
47. Rodrigo G, Carrera J, Ruiz-Ferrer V, del Toro FJ, Llave C, Voinnet O, Elena SF. 2012. A meta-analysis reveals the commonalities and differences in Arabidopsis thaliana response to different viral pathogens. PloS One 7, e40526..
48. Rotter A, Usadel B, Baebler S, Stitt M, Gruden K. 2007. Adaptation of the MapMan ontology to biotic stress responses: application in solanaceous species. Plant Methods 3, 10..
49. Sanchéz G, Gerhardt N, Siciliano F, Vojnov A, Malcuit I, Marano MR. 2010. Salicylic acid is involved in the Nb-mediated defense responses to Potato virus X in Solanum tuberosum. Molecular Plant- Microbe Interactions 23, 394-405..
50. Scholthof KB, Adkins S, Czosnek H, et al. 2011. Top 10 plant viruses in molecular plant pathology. Molecular Plant Pathology 12, 938-954..
51. Shirasu K, Lambas C. 1997. Salicylic acid potentiates an agonistdependent gain control that amplifies pathogen signals in the activation of defense mechanisms. The Plant Cell 9, 261-270..
52. Singh RP, Valkonen JPT, Gray SM, Boonham N, Jones RAC, Kerlan C, Schubert J. 2008. Discussion paper: The naming of Potato virus Y strains infecting potato. Archives of Virology 153, 1-13..
53. Smyth GK. 2005. Limma: linear models for microarray data. In: Gentelman R, Carey S, Dudoit S, Irizarry R, Huber W, editors, Bioinformatics and computational biology solutions using R and Bioconductor , New York: Springer, pp. 397-420..
54. Subramanian A, Tamayo P, Mootha VK, et al. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proceedings of the National Academy of Sciences, USA 102, 15545-15550..
55. Szajko K, Chrzanowska M, Witek K, Strzelczyk-?yta D, Zagórska H, Gebhardt C, Hennig J, Marczewski W. 2008. The novel gene Ny- 1 on potato chromosome IX confers hypersensitive resistance to Potato virus Y and is an alternative to Ry genes in potato breeding for PVY resistance. Theoretical and Applied Genetics 116, 297-303..
56. Takahashi H, Kanayama Y, Zheng MS, Kusano T, Hase S, Ikegami M, Shah J. 2004. Antagonistic interactions between the SA and JA signaling pathways in Arabidopsis modulate expression of defense genes and gene-for-gene resistance to cucumber mosaic virus. Plant Cell Physiology 45, 803-809..
57. Talarczyk A, Krzymowska M, Borucki W, Hennig J. 2002. Effect of yeast CTA1 gene expression on response of tobacco plants to tobacco mosaic virus infection. Plant Physiology 129, 1032-1044..
58. Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB. 1997. Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. The Plant Journal 11, 1187-1194..
59. Usadel B, Poree F, Nagel A, Lohse M, Czedik-Eysenberg A, Stitt M. 2009. A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, Maize. Plant, Cell and Environment 32, 1211-1229..
60. van Loon LC, Rep M, Pieterse CMJ. 2006. Significance of inducible defense-related proteins in infected plants. Annual Review of Phytopathology 44, 135-162..
61. van Wees SC, Glazebrook J. 2003. Loss of non-host resistance of Arabidopsis NahG to Pseudomonas syringae pv. phaseolicola is due to degradation products of salicylic acid. The Plant Journal 33, 733-742..
62. Varet A, Parker J, Tornero P, Nass N, Nurnberger T, Dangl JL, Scheel D, Lee J. 2002. NHL25 and NHL3, two NDR1/HIN1-1ike genes in Arabidopsis thaliana with potential role(s) in plant defense. Molecular Plant-Microbe Interactions 15, 608-616..
63. Vogel C, Marcotte EM. 2012. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nature Reviews in Genetics 13, 227-232..
64. Vogel J, Somerville S. 2000. Isolation and characterization of powdery mildew-resistant Arabidopsis mutants. Proceedings of the National Academy of Sciences, USA 97, 1897-1902..
65. Vuorinen AL, Gammerlgard E, Auvien P, Somervuo P, Dere S, Valkonen JPT. 2010. Factors underpinning the responsiveness and higher levels of virus resistance realised in potato genotypes carrying virus-specific R genes. Annals of Applied Biology 157, 229-241..
66. Wang SD, Zhu F, Yuan S, et al. 2011. The roles of ascorbic acid and glutathione in symptom alleviation to SA-deficient plants infected with RNA viruses. Planta 234, 171-181..
67. Wang X, Sager R, Cui W, Zhang C, Lu H, Lee JY. 2013. Salicylic acid regulates plasmodesmata closure during innate immune responses in Arabidopsis. The Plant Cell 25, 2315-2329..
68. Whitham SA, Yang C, Goodin MM. 2006. Global impact: elucidating plant responses to viral infection. Molecular Plant-Microbe Interactions 19, 1207-1215..
69. Yang C, Guo R, Jie F, Nettleton D, Peng J, Carr T, Yeakley JM, Fan JB, Whitham SA. 2007. Spatial analysis of Arabidopsis thaliana gene expression in response to turnip mosaic virus infection. Molecular Plant-Microbe Interactions 20, 358-370..
70. Yang H, Huang Y, Zhi H, Yu D. 2011. Proteomics-based analysis of novel genes involved in response toward soybean mosaic virus infection. Molecular Biology Reports 38, 511-521..
71. Yoshimoto K, Jikumaru Y, Kamiya Y, Kusano M, Consonni C, Panstruga R, Ohsumi Y, Shirasu K. 2009. Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. The Plant Cell 21, 2914-2927..
72. Yu DQ, Liu YD, Fan BF, Klessig DF, Chen ZX. 1997. Is the high basal level of salicylic acid important for disease resistance in potato? Plant Physiology 115, 343-349..
73. Zavaliev R, Levy A, Gera A, Epel BL. 2013. Subcellular dynamics and role of Arabidopsis beta-1,3-glucanases in cell-to-cell movement of tobamoviruses. Molecular Plant-Microbe Interactions 26, 1016-30..
74. Zhu Y, Qian W, Hua J. 2010. Temperature modulates plant defense responses through NB-LRR proteins. PLoS pathogens 6, e1000844..