Onset of virus systemic infection in plants is determined by speed of cell-to-cell movement and number of primary infection foci

Journal of the Royal Society Interface

Volumn 11, Issue 98, 2014, Pages

  Rodrigo, Guillermo ^a,b   Zwart, Mark P ^b   Elena, Santiago F ^b,c  

^a UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

^b UNIVERSITAT POLITÈCNICA DE VALÈNCIA   (Spain)

^c SANTA FE INSTITUTE   (United States)

Author keywords

Local versus global infection; Systems biology of virus infection; Virus evolution; Within host virus dynamics

Indexed keywords

CARDIOVASCULAR SYSTEM; CELLS; PLANTS (BOTANY); VIRUSES;

CELL-TO-CELL MOVEMENTS; HOST-PATHOGEN INTERACTIONS; INFECTION DYNAMICS; INHERENT CHARACTERISTICS; LOCAL VERSUS GLOBAL INFECTION; MECHANISTIC MODELING; VIRUS DYNAMICS; VIRUS INFECTION;

CYTOLOGY;

PLANT RNA;

ARTICLE; CELL MOTION; HEREDITY; HOST; MATHEMATICAL ANALYSIS; NICOTIANA BENTHAMIANA; PLANT DISEASE; PLANT LEAF; PLANT VIRUS; POTYVIRUS; QUANTITATIVE ANALYSIS; RNA VIRUS; TOBACCO; TOBACCO MOSAIC VIRUS; TURNIP; VIRAL GENETICS; VIRUS CELL INTERACTION; VIRUS INFECTION; VIRUS SYSTEMIC INFECTION; HOST PATHOGEN INTERACTION; PHYSIOLOGY; PLANT; THEORETICAL MODEL; TIME; VIROLOGY;

HOST-PATHOGEN INTERACTIONS; MODELS, THEORETICAL; PLANT DISEASES; PLANT LEAVES; PLANT VIRUSES; PLANTS; TIME FACTORS; TOBACCO; TOBACCO MOSAIC VIRUS;

EID: 84904989254     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2014.0555     Document Type: Article

References (33)

1. Waigmann E, Ueki S, Trutnyeva K, Citovsky V. 2004 The ins and outs of nondestructive cell-to-cell and systemic movement of plant viruses. Crit. Rev. Plant Sci. 23, 195-250. (doi:10.1080/07352680490452807)
2. Waterhouse PM, Wang MB, Lough T. 2001 Gene silencing as an adaptive defence against viruses. Nature 411, 834-842. (doi:10.1038/35081168)
3. Dunoyer P, Lecellier CH, Parizotto EA, Himber C, Voinnet O. 2004 Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. Plant Cell 16, 1235-1250. (doi:10.1105/tpc.020719)
4. Prins M, Laimer M, Noris E, Schubert J, Wassenegger M, Tepfer M. 2008 Strategies for antiviral resistance in transgenic plants. Mol. Plant Pathol. 9, 73-83. (Pubitemid 350295873)
5. Kermack WO, McKendrick AG. 1927 A contribution to the mathematical theory of epidemics. Proc. R. Soc. Lond. A 115, 700-721. (doi:10.1098/rspa.1927.0118)
6. Segarra J, Jeger MJ, van den Bosch F. 2001 Epidemic dynamics and patterns of plant diseases. Phytopathology 91, 1001-1010. (doi:10.1094/PHYTO.2001.91.10. 1001)
7. Keeling MJ. 2005 The implications of network structure for epidemic dynamics. Theor. Popul. Biol. 67, 1-8. (doi:10.1016/j.tpb.2004.08.002)
8. Dolja VV, McBride HJ, Carrington JC. 1992 Tagging of plant potyvirus replication and movement by insertion of b-glucuronidase into the viral polyprotein. Proc. Natl Acad. Sci. USA 89, 10 208-10 212. (doi:10.1073/pnas.89. 21.10208)
9. Zwart MP, Daròs JA, Elena SF. 2011 One is enough: in vivo effective population size is dose-dependent for a plant RNA virus. PLoS Pathog. 7, e1002122. (doi:10.1371/journal.ppat.1002122)
10. Bedoya LC, Martinez F, Orzáez D, Daròs JA. 2012 Visual tracking of plant virus infection and movement using a reporter MYB transcription factor that activates anthocyanin biosynthesis. Plant Physiol. 158, 1130-1138. (doi:10.1104/pp.111.192922)
11. Lafforgue G, Tromas N, Elena SF, Zwart MP. 2012 Dynamics of the establishment of systemic potyvirus infection: independent yet cumulative action of primary infection sites. J. Virol. 86, 12 912-12 922. (doi:10.1128/JVI. 02207-12)
12. Holmes FO. 1929 Local lesions in tobacco mosaic. Bot. Gazette 87, 39-55. (doi:10.1086/333923)
13. Bald JG. 1937 The use of numbers of infections for comparing the concentration of plant virus suspensions: dilution experiments with purified suspensions. Ann. Appl. Biol. 24, 33-55. (doi:10.1111/j.1744-7348.1937.tb05019. x)
14. Baulcombe D. 2004 RNA silencing in plants. Nature 431, 356-363. (doi:10.1038/nature02874)
15. Kunkel BN, Brooks DM. 2002 Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 5, 325-331. (doi:10.1016/S1369- 5266(02)00275-3)
16. Kørner CJ, Klauser D, Niehl A, Domínguez-Ferreras A, Chinchilla D, Boller T, Heinlein M, Hann DR. 2013 The immunity regulator BAK1 contributes to resistance against diverse RNA viruses. Mol. Plant Microbe Interact. 26, 1271-1280. (doi:10.1094/MPMI-06-13-0179-R)
17. Rodrigo G, Carrera J, Jaramillo A, Elena SF. 2011 Optimal viral strategies for bypassing RNA silencing. J. R. Soc. Interface 8, 257-268. (doi:10.1098/rsif.2010.0264)
18. Kleczkowski A. 1950 Interpreting relationships between the concentrations of plant viruses and numbers of local lesions. J. Gen. Microbiol. 4, 53-69. (doi:10.1099/00221287-4-1-53)
19. Van der Plank JE. 1965 Dynamics of epidemics of plant disease. Science 147, 120-124. (doi:10.1126/science.147.3654.120)
20. Zwart MP, Daròs JA, Elena SF. 2012 Effects of potyvirus effective population size in inoculated leaves on viral accumulation and the onset of symptoms. J. Virol. 86, 9737-9747. (doi:10.1128/JVI.00909-12)
21. Carrington JC, Kasschau KD, Mahajan SK, Schaad MC. 1996 Cell-to-cell and long-distance transport of viruses in plants. Plant Cell 8, 1669-1681. (doi:10.1105/tpc.8.10.1669)
22. Gibbs A. 1976 Viruses and plasmodesmata. In Intercellular communication in plants: studies on plasmodesmata (eds BES Gunning, AW Robards), pp. 149-164. New York, NY: Springer.
23. Hillung J, Elena SF, Cuevas JM. 2013 Intra-specific variability and biological relevance of P3N-PIPO protein length in potyviruses. BMC Evol. Biol. 13, 249. (doi:10.1186/1471-2148-13-249)
24. Dengler N, Kang J. 2001 Vascular patterning and leaf shape. Curr. Opin. Plant Biol. 4, 50-56. (doi:10.1016/S1369-5266(00)00135-7)
25. Samuel G. 1934 The movement of Tobacco mosaic virus within the plant. Ann. Appl. Biol. 21, 90-111. (doi:10.1111/j.1744-7348.1934.tb06891.x)
26. Kawakami S, Watanabe Y, Beachy RN. 2004 Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc. Natl Acad. Sci. USA 101, 6291-6296. (doi:10.1073/pnas.0401221101)
27. Bedoya L, Martínez F, Rubio L, Daròs JA. 2010 Simultaneous equimolar expression of multiple proteins in plants from a disarmed potyvirus vector. J. Biotechnol. 150, 268-275. (doi:10.1016/j.jbiotec.2010.08.006)
28. Wei T, Zhang C, Hong J, Xiong R, Kasschau KD, Zhou X, Carrington JC, Wang A. 2010 Formation of complexes at plasmodesmata for potyvirus intercellular movement is mediated by the viral protein P3N-PIPO. PLoS Pathog. 6, e1000962. (doi:10.1371/journal.ppat.1000962)
29. Bragard C, Caciagli P, Lemaire O, López-Moya JJ, MarFarlane S, Peters D, Susi P, Torrance L. 2013 Status and prospects of plant virus control through interference with vector transmission. Annu. Rev. Phytopathol. 51, 177-201. (doi:10.1146/annurev-phyto-082712-102346)
30. Sacristán S, Díaz M, Fraile A, García-Arenal F. 2011 Contact transmission of Tobacco mosaic virus: a quantitative analysis of parameters relevant for virus evolution. J. Virol. 85, 4974-4981. (doi:10.1128/JVI.00057-11)
31. Thung TH. 1928 Physiologisch onderzoek met betrekking tot het virus der bladrolziekte van de aardappel-plant, Solanum tuberosum L. Tijdschrift over Plantenziekten 34, 1-74.
32. Kunkel LO. 1934 Studies on acquired immunity with tobacco and aucuba mosaic. Phytopathology 24, 437-66.
33. Sánchez-Navarro JA, Zwart MP, Elena SF. 2013 Effects of the number of genome segments on primary and systemic infection for a multipartite plant RNA virus. J. Virol. 87, 10 805-10 815. (doi:10.1128/JVI.01402-13)