Plant-virus interactions and the agro-ecological interface

Abstract

As a result of human activities, an ever-increasing portion of Earth’s natural landscapes now lie adjacent to agricultural lands. This border between wild and agricultural communities represents an agro-ecological interface, which may be populated with crop plants, weeds of crop systems, and non-crop plants that vary from exotic to native in origin. Plant viruses are important components of the agro-ecological interface because of their ubiquity, dispersal by arthropod vectors, and ability to colonize both crop and wild species. Here we provide an overview of research on plant-virus dynamics across this interface and suggest three research priorities: (1) an increased effort to identify and describe plant virus diversity and distribution in its entirety across agricultural and ecological boundaries; (2) multi-scale studies of virus transmission to develop predictive power in estimating virus propagation across landscapes; and (3) quantitative evaluation of the influence of viruses on plant fitness and populations in environmental contexts beyond crop fields. We close by emphasizing that agro-ecological interfaces are dynamic, influenced by the human-mediated redistribution of plants, vectors, and viruses around the world, climate change, and the development of new crops. Consideration of virus interactions within these environmentally complex systems promises new insight into virus, plant, and vector dynamics from molecular mechanisms to ecological consequences.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2

References

  1. Abe, H., Tomitaka, Y., Shimoda, T., Seo, S., Sakurai, T., Kugimiya, S., et al. (2012). Antagonistic plant defense system regulated by phytohormones assists interactions among vector insect, thrips and a tospovirus. Plant and Cell Physiology, 53(1), 204–212.

    CAS  PubMed  Google Scholar 

  2. Agindotan, B. O., Ahonsi, M. O., Domier, L. L., Gray, M. E., & Bradley, C. A. (2010). Application of sequence-independent amplification (SIA) for the RNA viruses in bioenergy crops. Journal of Virological Methods, 169(1), 119–128.

    CAS  PubMed  Google Scholar 

  3. Alexander, H. M. (2010). Disease in natural plant populations, communities, and ecosystems: insights into ecological and evolutionary processes. Plant Disease, 94(5), 492–503.

    Google Scholar 

  4. Alexander, H. M., & Holt, R. D. (1998). The interaction between plant competition and disease. Perspectives in Plant Ecology, Evolution, and Systematics, 1(2), 206–220.

    Google Scholar 

  5. Anderson, P. K., Cunningham, A. A., Patel, N. G., Morales, F. J., Epstein, P. R., & Daszak, P. (2004). Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends in Ecology & Evolution, 19(10), 535–544.

    Google Scholar 

  6. Antonovics, J., & Alexander, H. M. (1989). The concept of fitness in plant-fungal pathogen systems. In K. J. Leonard & W. E. Fry (Eds.), Plant disease epidemiology. Genetics, resistance, and management (Vol. 2, pp. 185–214). New York: McGraw-Hill.

    Google Scholar 

  7. Badillo-Vargas, I. E., Rotenberg, D., Schneweis, D. J., Hiromasa, Y., Tomich, J. M., & Whitfield, A. E. (2012). Proteomic analysis of Frankliniella occidentalis and differentially expressed proteins in response to Tomato Spotted Wilt Virus infection. Journal of Virology, 86(16), 8793–8809.

    CAS  PubMed Central  PubMed  Google Scholar 

  8. Bedhomme, S., Lafforgue, G., & Elena, S. F. (2012). Multihost experimental evolution of a plant RNA virus reveals local adaptation and host-specific mutations. Molecular Biology and Evolution, 29(5), 1481–1492.

    CAS  PubMed  Google Scholar 

  9. Belliure, B., Janssen, A., Maris, P. C., Peters, D., & Sabelis, M. W. (2005). Herbivore arthropods benefit from vectoring plant viruses. Ecology Letters, 8(1), 70–79.

    Google Scholar 

  10. Bever, J. D. (2003). Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytologist, 157(3), 465–473.

    Google Scholar 

  11. Bi, Y. Q., Tugume, A. K., & Valkonen, J. P. T. (2012). Small-RNA deep sequencing reveals Arctium tomentosum as a natural host of Alstroemeria virus X and a new putative Emaravirus. Plos One, 7(8).

  12. Biddle, J. M., Linde, C., & Godfree, R. C. (2012). Co-infection patterns and geographic distribution of a complex pathosystem targeted by pathogen-resistant plants. Ecological Applications, 22(1), 35–52.

    CAS  PubMed  Google Scholar 

  13. Biek, R., & Real, L. A. (2010). The landscape genetics of infectious disease emergence and spread. Molecular Ecology, 19(17), 3515–3531.

    PubMed Central  PubMed  Google Scholar 

  14. Blanc, S., & Drucker, M. (2011). Functions of virus and host factors during vector-mediated transmission. In C. Caranta, M. A. Arnada, M. Tepfer, & U. Lopez-Moya (Eds.), Recent advances in plant virology (pp. 103–120). Norfolk: Caister Academic Press.

    Google Scholar 

  15. Blitzer, E. J., Dormann, C. F., Holzschuh, A., Klein, A. M., Rand, T. A., & Tscharntke, T. (2012). Spillover of functionally important organisms between managed and natural habitats. Agriculture, Ecosystems & Environment, 146(1), 34–43.

    Google Scholar 

  16. Boncquet, P. A., & Stahl, C. F. (1917). Wild vegetation as a source of curly-top infection of sugar beets. Journal of Economic Entomology, 10, 392–397.

    Google Scholar 

  17. Borer, E. T., Hosseini, P. R., Seabloom, E. W., & Dobson, A. P. (2007). Pathogen-induced reversal of native dominance in a grassland community. Proceedings of the National Academy of Sciences of the United States of America, 104(13), 5473–5478.

    CAS  PubMed Central  PubMed  Google Scholar 

  18. Bos, L. (1981). Wild plants in the ecology of virus diseases. In K. Maramorosch & K. F. Harris (Eds.), Plant diseases and vectors: ecology and epidemiology (pp. 1–33). New York: Academic.

    Google Scholar 

  19. Bosque-Pérez, N. A., & Eigenbrode, S. D. (2011). The influence of virus-induced changes in plants on aphid vectors: insights from luteovirus pathosystems. Virus Research, 159(2), 201–205.

    PubMed  Google Scholar 

  20. Burdon, J. J. (1987). Diseases and plant population ecology. Cambridge: Cambridge University Press.

    Google Scholar 

  21. Burdon, J. J., & Thrall, P. H. (2008). Pathogen evolution across the agro-ecological interface: implications for disease management. Evolutionary Applications, 1(1), 57–65.

    PubMed Central  Google Scholar 

  22. Carter, W. (1961). Ecological aspects of plant virus transmissions. Annual Review of Entomology, 6, 347.

    CAS  PubMed  Google Scholar 

  23. Christiansen-Weniger, P., Powell, C., & Hardie, J. (1998). Plant virus and parasitoid interactions in a shared insect vector/host. Entomologia Experimentalis et Applicata, 86(2), 205–213.

    Google Scholar 

  24. Cobb, R. C., Meentemeyer, R. K., & Rizzo, D. M. (2010). Apparent competition in canopy trees determined by pathogen transmission rather than susceptibility. Ecology, 91(2), 327–333.

    PubMed  Google Scholar 

  25. Coley, P. D., Bryant, J. P., & Chapin, F. S. (1985). Resource availability and plant antiherbivore defense. Science, 230(4728), 895–899.

    CAS  PubMed  Google Scholar 

  26. Cooper, I., & Jones, R. A. C. (2006). Wild plants and viruses: under-investigated ecosystems. In J. M. Thresh (Ed.), Plant virus epidemiology (Vol. 67, pp. 1–47). Advances in Virus Research.

    Google Scholar 

  27. Cooper, I., Kuhne, T., & Polishchuk, V. P. (2006). Virus diseases and crop biosecurity. Amsterdam: Ios Press.

    Google Scholar 

  28. Cox, C. M., Bockus, W. W., Holt, R. D., Fang, L., & Garrett, K. A. (2013). Spatial connectedness of plant species: potential links for apparent competition via plant diseases. Plant Pathology, 62(6), 1195–1204.

    Google Scholar 

  29. Crone, E. E. (2001). Is survivorship a better fitness surrogate than fecundity? Evolution, 55(12), 2611–2614.

    CAS  PubMed  Google Scholar 

  30. Cronin, J. P., Welsh, M. E., Dekkers, M. G., Abercrombie, S. T., & Mitchell, C. E. (2010). Host physiological phenotype explains pathogen reservoir potential. Ecology Letters, 13(10), 1221–1232.

    PubMed  Google Scholar 

  31. Culver, J. N., & Padmanabhan, M. S. (2007). Virus-induced disease: altering host physiology one interaction at a time. Annual Review of Phytopathology, 45, 221–243.

    CAS  PubMed  Google Scholar 

  32. Dáder, B., Moreno, A., Viñuela, E., & Fereres, A. (2012). Spatio-temporal dynamics of viruses are differentially affected by parasitoids depending on the mode of transmission. Viruses-Basel, 4(11), 3069–3089.

    Google Scholar 

  33. Davis, R., Wang, H., Falk, B. W., & Nunez, J. (1998). Curly top virus found in perennial shrubs in foothills. California Agriculture, 52, 38–40.

    Google Scholar 

  34. De Bruyn, A., Villemot, J., Lefeuvre, P., Villar, E., Hoareau, M., Harimalala, M., et al. (2012). East African cassava mosaic-like viruses from Africa to Indian ocean islands: molecular diversity, evolutionary history and geographical dissemination of a bipartite begomovirus. BMC Evolutionary Biology, 12.

  35. Doolittle, S. P., & Walker, M. N. (1925). Further studies on the overwintering and dissemination of cucurbit mosaic. Journal of Agricultural Research, 31, 0001–0058.

    Google Scholar 

  36. Duffus, J. E. (1971). Role of weeds in incidence of virus diseases. Annual Review of Phytopathology, 9, 319.

    Google Scholar 

  37. Dunn, A. M., Torchin, M. E., Hatcher, M. J., Kotanen, P. M., Blumenthal, D. M., Byers, J. E., et al. (2012). Indirect effects of parasites in invasions. Functional Ecology, 26(6), 1262–1274.

    Google Scholar 

  38. Ellis, E. C., Goldewijk, K. K., Siebert, S., Lightman, D., & Ramankutty, N. (2010). Anthropogenic transformation of the biomes, 1700 to 2000. Global Ecology and Biogeography, 19(5), 589–606.

    Google Scholar 

  39. Ellis, E. C., & Ramankutty, N. (2008). Putting people in the map: anthropogenic biomes of the world. Frontiers in Ecology and the Environment, 6(8), 439–447.

    Google Scholar 

  40. Ellstrand, N. C. (2003). Dangerous liaisons? When cultivated plants mate with their wild relatives. Baltimore: The John Hopkins University Press.

    Google Scholar 

  41. Fabre, F., Rousseau, E., Mailleret, L., & Moury, B. (2012). Durable strategies to deploy plant resistance in agricultural landscapes. New Phytologist, 193, 1064–1075.

    PubMed  Google Scholar 

  42. Fargette, D., Konate, G., Fauquet, C., Muller, E., Peterschmitt, M., & Thresh, J. M. (2006). Molecular ecology and emergence of tropical plant viruses. Annual Review of Phytopathology, 44, 235–260.

    CAS  PubMed  Google Scholar 

  43. Fereres, A., & Moreno, A. (2009). Behavioural aspects influencing plant virus transmission by homopteran insects. Virus Research, 141(2), 158–168.

    CAS  PubMed  Google Scholar 

  44. Fraile, A., & Garcia-Arenal, F. (2010). The coevolution of plants and viruses: resistance and pathogenicity. In J. P. Carr & G. Loebenstein (Eds.), Natural and engineered resistance to plant viruses, Pt Ii (Vol. 76, pp. 1–32). Advances in Virus Research.

    Google Scholar 

  45. Friess, N., & Maillet, J. (1997). Influence of cucumber mosaic virus infection on the competitive ability and reproduction of chickweed (Stellaria media). New Phytologist, 135(4), 667–674.

    Google Scholar 

  46. Froissart, R., Doumayrou, J., Vuillaume, F., Alizon, S., & Michalakis, Y. (2010). The virulence-transmission trade-off in vector-borne plant viruses: a review of (non-)existing studies. Philosophical Transactions of the Royal Society B-Biological Sciences, 365(1548), 1907–1918.

    CAS  PubMed Central  Google Scholar 

  47. Gallitelli, D. (2000). The ecology of Cucumber mosaic virus and sustainable agriculture. Virus Research, 71(1–2), 9–21.

    CAS  PubMed  Google Scholar 

  48. García, M. B., & Ehrlén, J. (2002). Reproductive effort and herbivory timing in a perennial herb: fitness components at the individual and population levels. American Journal of Botany, 89(8), 1295–1302.

    PubMed  Google Scholar 

  49. Garrett, K. A. (2012). Information networks for disease: commonalities in human management networks and within-host signalling networks. European Journal of Plant Pathology, 133(1), 75–88.

    Google Scholar 

  50. Ghawana, S., Kumar, H., Kumar, A., Singh, H., Bhardwaj, P., Rani, A., et al. (2011). An RNA isolation system for plant tissues rich in secondary metabolites. BMC Research Notes, 4, 85.

    CAS  PubMed Central  PubMed  Google Scholar 

  51. Gibbs, A. (1980). Plant virus that partially protects its wild legume host against herbivores. Intervirology, 13(1), 42–47.

    CAS  PubMed  Google Scholar 

  52. Gibbs, A. J., Fargette, D., Garcia-Arenal, F., & Gibbs, M. J. (2010). Time - the emerging dimension of plant virus studies. Journal of General Virology, 91, 13–22.

    CAS  PubMed  Google Scholar 

  53. Gilbert, G. S. (2002). Evolutionary ecology of plant diseases in natural ecosystems. Annual Review of Phytopathology, 40, 13–43.

    CAS  PubMed  Google Scholar 

  54. Gilligan, C. A., & van den Bosch, F. (2008). Epidemiological models for invasion and persistence of pathogens. Annual Review of Phytopathology, 46, 385–418.

    CAS  PubMed  Google Scholar 

  55. Hagen, C., Frizzi, A., Gabriels, S., Huang, M. Y., Salati, R., Gabor, B., et al. (2012). Accurate and sensitive diagnosis of geminiviruses through enrichment, high-throughput sequencing and automated sequence identification. Archives of Virology, 157(5), 907–915.

    CAS  PubMed  Google Scholar 

  56. Hagler, J. R., & Jackson, C. G. (2001). Methods for marking insects: current techniques and future prospects. Annual Review of Entomology, 46, 511–543.

    CAS  PubMed  Google Scholar 

  57. Hagler, J. R., & Jones, V. P. (2010). A protein-based approach to mark arthropods for mark-capture type research. Entomologia Experimentalis et Applicata, 135(2), 177–192.

    CAS  Google Scholar 

  58. Herms, D. A., & Mattson, W. J. (1992). The dilemma of plants - to grow or defend. Quarterly Review of Biology, 67(3), 283–335.

    Google Scholar 

  59. Hodge, S., Hardie, J., & Powell, G. (2011). Parasitoids aid dispersal of a nonpersistently transmitted plant virus by disturbing the aphid vector. Agricultural and Forest Entomology, 13(1), 83–88.

    Google Scholar 

  60. Hogenhout, S. A., Ammar, E. D., Whitfield, A. E., & Redinbaugh, M. G. (2008). Insect vector interactions with persistently transmitted viruses. Annual Review of Phytopathology, 46, 327–359.

    CAS  PubMed  Google Scholar 

  61. Ingwell, L. L., Eigenbrode, S. D., & Bosque-Pérez, N. A. (2012). Plant viruses alter insect behavior to enhance their spread. Scientific Reports, 2.

  62. Jeger, M. J., Pautasso, M., Holdenrieder, O., & Shaw, M. W. (2007). Modelling disease spread and control in networks: implications for plant sciences. New Phytologist, 174(2), 279–297.

    PubMed  Google Scholar 

  63. Jeger, M. J., van den Bosch, & Madden, L. V. (2011). Modelling virus-and host-limitation in vectored plant disease epidemics. Virus Research, 159, 215–222.

    CAS  PubMed  Google Scholar 

  64. Jenner, C. E., Wang, X. W., Ponz, F., & Walsh, J. A. (2002). A fitness cost for turnip mosaic virus to overcome host resistance. Virus Research, 86(1–2), 1–6.

    CAS  PubMed  Google Scholar 

  65. Jiménez-Martinez, E. S., Bosque-Pérez, N. A., Berger, P. H., Zemetra, R., Ding, H. J., & Eigenbrode, S. D. (2004a). Volatile cues influence the response of Rhopalosiphum padi (Homoptera : Aphididae) to barley yellow dwarf virus-infected transgenic and untransformed wheat. Environmental Entomology, 33(5), 1207–1216.

    Google Scholar 

  66. Jiménez-Martinez, E. S., Bosque-Pérez, N. A., Berger, P. H., & Zemetra, R. S. (2004b). Life history of the bird cherry-oat aphid, Rhopalosiphum padi (Homoptera : Aphididae), on Transgenic and untransformed wheat challenged with Barley yellow dwarf virus. Journal of Economic Entomology, 97(2), 203–212.

    PubMed  Google Scholar 

  67. Jones, R. A. C. (2004). Using epidemiological information to develop effective integrated virus disease management strategies. Virus Research, 100, 5–30.

    CAS  PubMed  Google Scholar 

  68. Jones, R. A. C. (2005). Patterns of spread of two non-persistently aphid-borne viruses in lupin stands under four different infection scenarios. Annals of Applied Biology, 146(3), 337–350.

    Google Scholar 

  69. Jones, R. A. C. (2009). Plant virus emergence and evolution: origins, new encounter scenarios, factors driving emergence, effects of changing world conditions, and prospects for control. Virus Research, 141(2), 113–130.

    CAS  PubMed  Google Scholar 

  70. Jones, R. A. C., Salam, M. U., Maling, T. J., Diggle, A. J., & Thackray, D. J. (2010). Principles of predicting plant virus disease epidemics. Annual Review of Phytopathology, 48(48), 179–203.

    CAS  PubMed  Google Scholar 

  71. Kareiva, P., Watts, S., McDonald, R., & Boucher, T. (2007). Domesticated nature: shaping landscapes and ecosystems for human welfare. Science, 316(5833), 1866–1869.

    CAS  PubMed  Google Scholar 

  72. Keesing, F., Belden, L. K., Daszak, P., Dobson, A., Harvell, C. D., Holt, R. D., et al. (2010). Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature, 468(7324), 647–652.

    CAS  PubMed  Google Scholar 

  73. Kelley, S. E. (1994). Viral pathogens and the advantage of sex in the perennial grass Anthoxanthum odoratum. Philosophical Transactions of the Royal Society of London B Biological Sciences, 346(1317), 295–302.

    Google Scholar 

  74. Klueken, A. M., Hau, B., Koepke, I., & Poehling, H. M. (2008). Comparison of techniques to survey populations of cereal aphids (Homoptera: Aphididae) in winter cereals during autumn and spring with special consideration of sample size. Journal of Plant Diseases and Protection, 115(6), 279–287.

    Google Scholar 

  75. Kreuze, J. F., Perez, A., Untiveros, M., Quispe, D., Fuentes, S., Barker, I., et al. (2009). Complete viral genome sequence and discovery of novel viruses by deep sequencing of small RNAs: a generic method for diagnosis, discovery and sequencing of viruses. Virology, 388(1), 1–7.

    CAS  PubMed  Google Scholar 

  76. Kumar, P. L., Hanna, R., Alabi, O. J., Soko, M. M., Oben, T. T., Vangu, G. H. P., et al. (2011). Banana bunchy top virus in sub-Saharan Africa: investigations on virus distribution and diversity. Virus Research, 159(2), 171–182.

    CAS  PubMed  Google Scholar 

  77. Lebouvier, M., Laparie, M., Hullé, M., Marais, A., Cozic, Y., Lalouette, L., et al. (2011). The significance of the sub-Antarctic Kerguelen Islands for the assessment of the vulnerability of native communities to climate change, alien insect invasions and plant viruses. Biological Invasions, 13(5), 1195–1208.

    Google Scholar 

  78. Legg, J. P., Jeremiah, S. C., Obiero, H. M., Maruthi, M. N., Ndyetabula, I., Okao-Okuja, G., et al. (2011). Comparing the regional epidemiology of the cassava mosaic and cassava brown streak virus pandemics in Africa. Virus Research, 159(2), 161–170.

    CAS  PubMed  Google Scholar 

  79. Li, R. G., Gao, S., Hernandez, A. G., Wechter, W. P., Fei, Z. J., & Ling, K. S. (2012). Deep sequencing of small RNAs in tomato for virus and viroid identification and strain differentiation. Plos One, 7(5).

  80. Lima, A. T. M., Sobrinho, R. R., Gonzalez-Aguilera, J., Rocha, C. S., Silva, S. J. C., Xavier, C. A. D., et al. (2013). Synonymous site variation due to recombination explains higher genetic variability in begomovirus populations infecting non-cultivated hosts. Journal of General Virology, 94, 418–431.

    CAS  PubMed  Google Scholar 

  81. MacClement, W. D., & Richards, M. G. (1956). Viruses in wild plants. American Journal of Botany, 34, 793–799.

    Google Scholar 

  82. Madden, L. V., Jeger, M. J., & van den Bosch, F. (2000). A theoretical assessment of the effects of vector-virus transmission mechanism on plant virus disease epidemics. Phytopathology, 90(6), 576–594.

    CAS  PubMed  Google Scholar 

  83. Malmstrom, C. M., & Field, C. B. (1997). Virus-induced differences in the response of oat plants to elevated carbon dioxide. Plant Cell and Environment, 20(2), 178–188.

    Google Scholar 

  84. Malmstrom, C. M., Hughes, C. C., Newton, L. A., & Stoner, C. J. (2005a). Virus infection in remnant native bunchgrasses from invaded California grasslands. New Phytologist, 168(1), 217–230.

    CAS  PubMed  Google Scholar 

  85. Malmstrom, C. M., McCullough, A. J., Johnson, H. A., Newton, L. A., & Borer, E. T. (2005b). Invasive annual grasses indirectly increase virus incidence in California native perennial bunchgrasses. Oecologia, 145(1), 153–164.

    PubMed  Google Scholar 

  86. Malmstrom, C. M., Melcher, U., & Bosque-Pérez, N. A. (2011). The expanding field of plant virus ecology: historical foundations, knowledge gaps, and research directions. Virus Research, 159(2), 84–94.

    CAS  PubMed  Google Scholar 

  87. Malmstrom, C. M., Shu, R., Linton, E. W., Newton, L. A., & Cook, M. A. (2007). Barley yellow dwarf viruses (BYDVs) preserved in herbarium specimens illuminate historical disease ecology of invasive and native grasses. Journal of Ecology, 95, 1153–1166.

    CAS  Google Scholar 

  88. Malmstrom, C. M., Stoner, C. J., Brandenburg, S., & Newton, L. A. (2006). Virus infection and grazing exert counteracting influences on survivorship of native bunchgrass seedlings competing with invasive exotics. Journal of Ecology, 94(2), 264–275.

    PubMed Central  PubMed  Google Scholar 

  89. Márquez, L. M., Redman, R. S., Rodriguez, R. J., & Roossinck, M. J. (2007). A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science, 315, 513–515.

    PubMed  Google Scholar 

  90. Maskell, L. C., Raybould, A. F., Cooper, J. I., Edwards, M. L., & Gray, A. J. (1999). Effects of turnip mosaic virus and turnip yellow mosaic virus on the survival, growth and reproduction of wild cabbage (Brassica oleracea). Annals of Applied Biology, 135(1), 401–407.

    Google Scholar 

  91. Mauck, K., Bosque-Perez, N. A., Eigenbrode, S. D., De Moraes, C. M., & Mescher, M. C. (2012). Transmission mechanisms shape pathogen effects on host-vector interactions: evidence from plant viruses. Functional Ecology, 26(5), 1162–1175.

    Google Scholar 

  92. Mauck, K. E., De Moraes, C. M., & Mescher, M. C. (2010). Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. Proceedings of the National Academy of Sciences of the United States of America, 107(8), 3600–3605.

    CAS  PubMed Central  PubMed  Google Scholar 

  93. McElhany, P., Real, L. A., & Power, A. G. (1995). Vector preference and disease dynamics—a study of barley yellow dwarf virus. Ecology, 76(2), 444–457.

    Google Scholar 

  94. McGraw, J. B., & Caswell, H. (1996). Estimation of individual fitness from life-history data. American Naturalist, 147(1), 47–64.

    Google Scholar 

  95. Meentemeyer, R. K., Haas, S. E., & Václavík, T. (2012). Landscape epidemiology of emerging infectious diseases in natural and human-altered ecosystems. Annual Review of Phytopathology, 50, 379–402.

    CAS  PubMed  Google Scholar 

  96. Melcher, U., & Grover, V. (2011). Genomic approaches to discovery of viral species diversity of non-cultivated plants. In C. Caranta & M. A. Aranda (Eds.), Recent advances in plant virology. Norfolk: Caister Academic Press.

    Google Scholar 

  97. Melcher, U., Muthukumar, V., Wiley, G. B., Min, B. E., Palmer, M. W., Verchot-Lubicz, J., et al. (2008). Evidence for novel viruses by analysis of nucleic acids in virus-like particle fractions from Ambrosia psilostachya. Journal of Virological Methods, 152(1–2), 49–55.

    CAS  PubMed  Google Scholar 

  98. Mitchell, C. E., & Power, A. G. (2006). Disease dynamics in plant communities. In S. K. Collinge & C. Ray (Eds.), Disease ecology: community structure and pathogen dynamics (pp. 58–72). Oxford: Oxford University Press.

    Google Scholar 

  99. Moreno-Delafuente, A., Garzo, E., Moreno, A., & Fereres, A. (2013). A plant virus manipulates the behavior of its whitefly vector to enhance its transmission efficiency and spread. Plos One, 8(4).

  100. Moritz, G., Kumm, S., & Mound, L. (2004). Tospovirus transmission depends on thrips ontogeny. Virus Research, 100(1), 143–149.

    CAS  PubMed  Google Scholar 

  101. Moslonka-Lefebvre, M., Finley, A., Dorigatti, I., Dehnen-Schmutz, K., Harwood, T., Jeger, M. J., et al. (2011). Networks in plant epidemiology: from genes to landscapes, countries, and continents. Phytopathology, 101(4), 392–403.

    PubMed  Google Scholar 

  102. Moury, B., Fabre, F., & Senoussi, R. (2007). Estimation of the number of virus particles transmitted by an insect vector. Proceedings of the National Academy of Sciences of the United States of America, 104(45), 17891–17896.

    CAS  PubMed Central  PubMed  Google Scholar 

  103. Nathan, R., Perry, G., Cronin, J. T., Strand, A. E., & Cain, M. L. (2003). Methods for estimating long-distance dispersal. Oikos, 103(2), 261–273.

    Google Scholar 

  104. Navas-Castillo, J., Fiallo-Olivé, E., & Sánchez-Campos, S. (2011). Emerging virus diseases transmitted by whiteflies. Annual Review of Phytopathology, 49(49), 219–248.

    CAS  PubMed  Google Scholar 

  105. Ng, J. C. K., & Falk, B. W. (2006). Virus-vector interactions mediating nonpersistent and semipersistent transmission of plant viruses. Annual Review of Phytopathology, 44, 183–212.

    CAS  PubMed  Google Scholar 

  106. Ng, T. F. F., Duffy, S., Polston, J. E., Bixby, E., Vallad, G. E., & Breitbart, M. (2011). Exploring the diversity of plant DNA viruses and their satellites using vector-enabled metagenomics on whiteflies. Plos One, 6(4).

  107. Nguyen, H. D., Tomitaka, Y., Ho, S. Y. W., Duchêne, S., Vetten, H. J., Lesemann, D., et al. (2013). Turnip mosaic potyvirus probably first spread to Eurasian Brassica crops from wild orchids about 1000 years ago. Plos One, 8(2).

  108. Orr, H. A. (2009). Fitness and its role in evolutionary genetics. Nature Reviews Genetics, 10(8), 531–539.

    CAS  PubMed Central  PubMed  Google Scholar 

  109. Osmond, C. B., Berry, J. A., Balachandran, S., Buchenosmond, C., Daley, P. F., & Hodgson, R. A. J. (1990). Potential consequences of virus infection for shade-sun acclimmation in leaves. Botanica Acta, 103(3), 226–229.

    Google Scholar 

  110. OtimNape, G. W., Thresh, J. M., & Shaw, M. W. (1997). The effects of cassava mosaic virus disease on yield and compensation in mixed stands of healthy and infected cassava. Annals of Applied Biology, 130(3), 503–521.

    Google Scholar 

  111. Pagán, I., Fraile, A., Fernandez-Fueyo, E., Montes, N., Alonso-Blanco, C., & García-Arenal, F. (2010). Arabidopsis thaliana as a model for the study of plant-virus co-evolution. Philosophical Transactions of the Royal Society B-Biological Sciences, 365(1548), 1983–1995.

    PubMed Central  Google Scholar 

  112. Pagán, I., Gonzalez-Jara, P., Moreno-Letelier, A., Rodelo-Urrego, M., Fraile, A., Pinero, D., et al. (2012). Effect of biodiversity changes in disease risk: exploring disease emergence in a plant-virus system. PLoS Pathogens, 8(7).

  113. Pagán, I., & Holmes, E. C. (2010). Long-term evolution of the Luteoviridae: time scale and mode of virus speciation. Journal of Virology, 84(12), 6177–6187.

    PubMed Central  PubMed  Google Scholar 

  114. Pallett, D. W., Ho, T., Cooper, I., & Wang, H. (2010). Detection of cereal yellow dwarf virus using small interfering RNAs and enhanced infection rate with cocksfoot streak virus in wild cocksfoot grass (Dactylis glomerata). Journal of Virological Methods, 168(1–2), 223–227.

    CAS  PubMed  Google Scholar 

  115. Plantegenest, M., Le May, C., & Fabre, F. (2007). Landscape epidemiology of plant diseases. Journal of the Royal Society Interface, 4(16), 963–972.

    PubMed Central  Google Scholar 

  116. Power, A. G. (1996). Competition between viruses in a complex plant-pathogen. Ecology, 77(4), 1004–1010.

    Google Scholar 

  117. Power, A. G. (2008). Community ecology of plant viruses. In M. J. Roossinck (Ed.), Plant virus evolution. Berlin Heidelberg: Springer.

    Google Scholar 

  118. Power, A. G. (2010). Ecosystem services and agriculture: tradeoffs and synergies. Philosophical Transactions of the Royal Society B-Biological Sciences, 365(1554), 2959–2971.

    PubMed Central  Google Scholar 

  119. Power, A. G., Borer, E. T., Hosseini, P., Mitchell, C. E., & Seabloom, E. W. (2011). The community ecology of barley/cereal yellow dwarf viruses in Western US grasslands. Virus Research, 159(2), 95–100.

    CAS  PubMed  Google Scholar 

  120. Power, A. G., & Mitchell, C. E. (2004). Pathogen spillover in disease epidemics. American Naturalist, 164(5), S79–S89.

    PubMed  Google Scholar 

  121. Predajňa, L., Šubr, Z., Candresse, T., & Glasa, M. (2012). Evaluation of the genetic diversity of Plum pox virus in a single plum tree. Virus Research, 167(1), 112–117.

    PubMed  Google Scholar 

  122. Prendeville, H. R., Ye, X. H., Morris, T. J., & Pilson, D. (2012). Virus infections in wild plant populations are both frequent and often unapparent. American Journal of Botany, 99(6), 1033–1042.

    PubMed  Google Scholar 

  123. Rakotomalala, M., Pinel-Galzi, A., Mpunami, A., Randrianasolo, A., Ramavovololona, P., Rabenantoandro, Y., et al. (2013). Rice yellow mottle virus in Madagascar and in the Zanzibar Archipelago; island systems and evolutionary time scale to study virus emergence. Virus Research, 171(1), 71–79.

    CAS  PubMed  Google Scholar 

  124. Remold, S. K. (2002). Unapparent virus infection and host fitness in three weedy grass species. Journal of Ecology, 90(6), 967–977.

    Google Scholar 

  125. Robertson, N. L. (2007). Identification and characterization of a new virus in the genus Potyvirus from wild populations of Angelica lucida L. and A-genuflexa Nutt., family Apiaceae. Archives of Virology, 152(9), 1603–1611

  126. Robertson, N. L., Côté, F., Pare, C., Leblanc, E., Bergeron, M. G., & Leclerc, D. (2007). Complete nucleotide sequence of Nootka lupine vein-clearing virus. Virus Genes, 35(3), 807–814.

    CAS  PubMed  Google Scholar 

  127. Rodelo-Urrego, M., Pagán, I., González-Jara, P., Betancourt, M., Moreno-Letelier, A., Ayllón, M. A., et al. (2013). Landscape heterogeneity shapes host-parasite interactions and results in apparent plantvirus codivergence. Molecular Ecology, 22(8), 2325–2340.

    CAS  PubMed  Google Scholar 

  128. Roossinck, M. J. (2010). Lifestyles of plant viruses. Philosophical Transactions of the Royal Society B-Biological Sciences, 365(1548), 1899–1905.

    PubMed Central  Google Scholar 

  129. Roossinck, M. J. (2011). The good viruses: viral mutualistic symbioses. Nature Reviews Microbiology, 9(2), 99–108.

    CAS  PubMed  Google Scholar 

  130. Roossinck, M. J. (2012). Plant virus metagenomics: biodiversity and ecology. Annual Review of Genetics, 46, 359–369.

    CAS  PubMed  Google Scholar 

  131. Roossinck, M. J., Saha, P., Wiley, G. B., Quan, J., White, J. D., Lai, H., et al. (2010). Ecogenomics: using massively parallel pyrosequencing to understand virus ecology. Molecular Ecology, 19, 81–88.

    PubMed  Google Scholar 

  132. Rotenberg, D., Krishna Kumar, N. K., Ullman, D. E., Montero-Astúa, M., Willis, D. K., German, T. L., et al. (2009). Variation in tomato spotted wilt virus titer in Frankliniella occidentalis and its association with frequency of transmission. Phytopathology, 99(4), 404–410.

    CAS  PubMed  Google Scholar 

  133. Rua, M. A., Pollina, E. C., Power, A. G., & Mitchell, C. E. (2011). The role of viruses in biological invasions: friend or foe? Current Opinion in Virology, 1(1), 68–72.

    PubMed  Google Scholar 

  134. Ruščić, J., Gutiérrez-Aguirre, I., Urbas, L., Kramberger, P., Mehle, N., Škorić, D., et al. (2013). A novel application of methacrylate based short monolithic columns: concentrating Potato spindle tuber viroid from water samples. Journal of Chromatography A, 1274, 129–136.

    PubMed  Google Scholar 

  135. Sasu, M. A., Ferrari, M. J., Du, D. L., Winsor, J. A., & Stephenson, A. G. (2009). Indirect costs of a nontarget pathogen mitigate the direct benefits of a virus-resistant transgene in wild Cucurbita. Proceedings of the National Academy of Sciences of the United States of America, 106(45), 19067–19071.

    CAS  PubMed Central  PubMed  Google Scholar 

  136. Scholthof, K. B. G., Adkins, S., Czosnek, H., Palukaitis, P., Jacquot, E., Hohn, T., et al. (2011). Top 10 plant viruses in molecular plant pathology. Molecular Plant Pathology, 12(9), 938–954.

    CAS  PubMed  Google Scholar 

  137. Schrotenboer, A. C., Allen, M. S., & Malmstrom, C. M. (2011). Modification of native grasses for biofuel production may increase virus susceptibility. Global Change Biology Bioenergy, 3(5), 360–374.

    Google Scholar 

  138. Seabloom, E. W., Borer, E. T., Lacroix, C., Mitchell, C. E., & Power, A. G. (2013). Richness and composition of niche-assembled viral pathogen communities. Plos One, 8(2).

  139. Seabloom, E. W., Hosseini, P. R., Power, A. G., & Borer, E. T. (2009). Diversity and composition of viral communities: coinfection of barley and Cereal yellow dwarf viruses in California grasslands. American Naturalist, 173(3), E79–E98.

    PubMed  Google Scholar 

  140. Shapiro, L., De Moraes, C. M., Stephenson, A. G., & Mescher, M. C. (2012). Pathogen effects on vegetative and floral odours mediate vector attraction and host exposure in a complex pathosystem. Ecology Letters, 15(12), 1430–1438.

    PubMed  Google Scholar 

  141. Shaw, R. G., & Geyer, C. J. (2010). Inferring fitness landscapes. Evolution, 64(9), 2510–2520.

    PubMed  Google Scholar 

  142. Sisterson, M. S. (2008). Effects of insect-vector preference for healthy or infected plants on pathogen spread: Insights from a model. Journal of Economic Entomology, 101(1), 1–8.

    PubMed  Google Scholar 

  143. Srininvasan, R., Alvarez, J. M., Eigenbrode, S. D., & Bosque-Perez, N. A. (2006). Influence of hairy nightshade Solanum sarrachoides (Sendtner) and Potato leafroll virus (Luteoviridae : Polerovirus) on the host preference of Myzus persicae (Sulzer) (Homoptera : Aphididae). Environmental Entomology, 35(2), 546–553.

    Google Scholar 

  144. Stafford, C. A., Walker, G. P., & Ullman, D. E. (2011). Infection with a plant virus modifies vector feeding behavior. Proceedings of the National Academy of Sciences of the United States of America, 108(23), 9350–9355.

    CAS  PubMed Central  PubMed  Google Scholar 

  145. Stumpf, C. F., & Kennedy, G. G. (2007). Effects of tomato spotted wilt virus isolates, host plants, and temperature on survival, size, and development time of Frankliniella occidentalis. Entomologia Experimentalis et Applicata, 123(2), 139–147.

    Google Scholar 

  146. Sutrave, S., Scoglio, C., Isard, S. A., Hutchinson, J. M. S., & Garrett, K. A. (2012). Identifying highly connected counties compensates for resource limitations when evaluating national spread of an invasive pathogen. Plos One, 7(6).

  147. Syller, J. (2012). Facilitative and antagonistic interactions between plant viruses in mixed infections. Molecular Plant Pathology, 13(2), 204–216.

    PubMed  Google Scholar 

  148. Thresh, J. M. (Ed.). (1981). Pests, pathogens, and vegetation. London: Pitman Books Limited.

    Google Scholar 

  149. Thresh, J. M. (2006). Plant virus epidemiology: the concept of host genetic vulnerability. In J. M. Thresh (Ed.), Plant virus epidemiology (Vol. 67, pp. 89–125). Advances in Virus Research.

    Google Scholar 

  150. Todesco, M., Balasubramanian, S., Hu, T. T., Traw, M. B., Horton, M., Epple, P., et al. (2010). Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature, 465(7298), 632–U129.

    CAS  PubMed Central  PubMed  Google Scholar 

  151. Tomlinson, J. A., & Carter, A. L. (1970). Studies on seed transmission of cucumber mosaic virus in chickwee (Stellaria media) in relation to the ecology of the virus. Annals of Applied Biology, 66(3), 381.

    Google Scholar 

  152. Turechek, W. W., Kousik, C. S., & Adkins, S. (2010). Distribution of four viruses in single and mixed infections within infected watermelon plants in Florida. Phytopathology, 100(11), 1194–1203.

    PubMed  Google Scholar 

  153. Varsani, A., Shepherd, D. N., Monjane, A. L., Owor, B. E., Erdmann, J. B., Rybicki, E. P., et al. (2008). Recombination, decreased host specificity and increased mobility may have driven the emergence of maize streak virus as an agricultural pathogen. Journal of General Virology, 89, 2063–2074.

    CAS  PubMed  Google Scholar 

  154. Wang, M. B., Masuta, C., Smith, N. A., & Shimura, H. (2012). RNA silencing and plant viral diseases. Molecular Plant-Microbe Interactions, 25(10), 1275–1285.

    CAS  PubMed  Google Scholar 

  155. Webster, C. G., Coutts, B. A., Jones, R. A. C., Jones, M. G. K., & Wylie, S. J. (2007). Virus impact at the interface of an ancient ecosystem and a recent agroecosystem: studies on three legume-infecting potyviruses in the southwest Australian floristic region. Plant Pathology, 56(5), 729–742.

    CAS  Google Scholar 

  156. Whitfield, A. E., Campbell, L. R., Sherwood, J. L., & Ullman, D. E. (2003). Tissue blot immunoassay for detection of Tomato spotted wilt virus in Ranunculus asiaticus and other ornamentals. Plant Disease, 87(6), 618–622.

    Google Scholar 

  157. Willner, D., & Hugenholtz, P. (2013). From deep sequencing to viral tagging: recent advances in viral metagenomics. Bioessays, 35(5), 436–442.

    CAS  PubMed  Google Scholar 

  158. Wintermantel, W. M., Cortez, A. A., Anchieta, A. G., Gulati-Sakhuja, A., & Hladky, L. L. (2008). Co-infection by two Criniviruses alters accumulation of each virus in a host-specific manner and influences efficiency of virus Transmission. Phytopathology, 98(12), 1340–1345.

    PubMed  Google Scholar 

  159. Wisler, G. C., & Norris, R. E. (2005). Interactions between weeds and cultivated plants as related to management of plant pathogens. Weed Science, 53(6), 914–917.

    CAS  Google Scholar 

  160. Wren, J. D., Roossinck, M. J., Nelson, R. S., Scheets, K., Palmer, M. W., & Melcher, U. (2006). Plant virus biodiversity and ecology. PLoS Biology, 4(3), 314–315.

    CAS  Google Scholar 

  161. Wu, B. L., Blanchard-Letort, A., Liu, Y., Zhou, G. H., Wang, X. F., & Elena, S. F. (2011). Dynamics of molecular evolution and phylogeography of Barley yellow dwarf virus-PAV. Plos One, 6(2).

  162. Wylie, S. J., Li, H., Dixon, K. W., Richards, H., & Jones, M. G. K. (2013). Exotic and indigenous viruses infect wild populations and captive collections of temperate terrestrial orchids (Diuris species) in Australia. Virus Research, 171(1), 22–32.

    CAS  PubMed  Google Scholar 

  163. Xu, P., Chen, F., Mannas, J. P., Feldman, T., Sumner, L. W., & Roossinck, M. J. (2008). Virus infection improves drought tolerance. New Phytologist, 180(4), 911–921.

    PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by 1) University of Kansas General Research Fund 2301545 (HMA), 2) National Science Foundation DDIG (DEB-1011122) and a grant from the Pennsylvania Soybean Board (KEM), 3) National Science Foundation CAREER grant IOS-0953786 (AEW), 4) CGIAR Research Program on Roots, Tubers and Bananas, Seed Degeneration Project (KAG), and 5) National Science Foundation grants IOS-0639139 & DEB-0843140, the Department of Energy Great Lakes Bioenergy Research Center (DOE Office of Science BER DE-FC02-07ER64494), USDA NIFA Sustainable Biofuels Program Award 2011-67009-30137 and AgBioResearch Hatch project MICL02055 (CMM). AEW and KAG also note that this is Contribution No. 13-325-J from the Kansas Agricultural Experiment Station. We thank PVEN colleagues and anonymous reviewers for helpful feedback.

Author information

Affiliations

Authors

Corresponding author

Correspondence to H. M. Alexander.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Alexander, H.M., Mauck, K.E., Whitfield, A.E. et al. Plant-virus interactions and the agro-ecological interface. Eur J Plant Pathol 138, 529–547 (2014). https://doi.org/10.1007/s10658-013-0317-1

Download citation

Keywords

  • Agro-ecological interface
  • Crop
  • Plant fitness
  • Plant virus
  • Vector
  • Wild plant