Environmental nutrient supply alters prevalence and weakens competitive interactions among coinfecting viruses

Journal of Physiology

Volumn 204, Issue 2, 2014, Pages 424-433

  Lacroix, Christelle ^a   Seabloom, Eric W ^a   Borer, Elizabeth T ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Coinfection; Host susceptibility; Nutrient; Pathogen interactions; RNA virus; Stoichiometry; Vectored plant pathogen

Indexed keywords

NITROGEN; PHOSPHORUS;

ENVIRONMENT; HOST PATHOGEN INTERACTION; HUMAN; LUTEOVIRIDAE; LUTEOVIRUS; METABOLISM; MIXED INFECTION; OAT; PHYSIOLOGY; PLANT DISEASE; VIROLOGY;

AVENA SATIVA; COINFECTION; ENVIRONMENT; HOST-PATHOGEN INTERACTIONS; HUMANS; LUTEOVIRIDAE; LUTEOVIRUS; NITROGEN; PHOSPHORUS; PLANT DISEASES;

EID: 84923068338     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1111/nph.12909     Document Type: Article

References (104)

1. Adam A, Gaborjanyi R, Tobias I, Kiraly Z. 1987. Effect of nitrogen nutrition on the concentration of viruses, phospholipids and galactolipids of barley leaves infected with Barley Stripe Mosaic-virus ((BSMV). Annals of Applied Biology 110: 313-319.
2. Aerts R, Chapin FS. 2000. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. In: Fitter AH, Raffaelli DG, eds. Advances in Ecological Research 30: 1-67.
3. Ahlquist P, Noueiry AO, Lee W-M, Kushner DB, Dye BT. 2003. Host factors in positive-strand RNA virus genome replication. Journal of Virology 77: 8181-8186.
4. Alizon S. 2013. Parasite co-transmission and the evolutionary epidemiology of virulence. Evolution 67: 921-933.
5. Bawden FC, Kassanis B. 1950a. Some effects of host-plant nutrition on the multiplication of viruses. Annals of Applied Biology 37: 215-228.
6. Bawden FC, Kassanis B. 1950b. Some effects of host nutrition on the susceptibility of plants to infection by certain viruses. Annals of Applied Biology 37: 46-57.
7. Betancourt M, Escriu F, Fraile A, García-Arenal F. 2013. Virulence evolution of a generalist plant virus in a heterogeneous host system. Evolutionary Applications 6: 875-890.
8. Borer ET, Adams VT, Engler GA, Adams AL, Schumann CB, Seabloom EW. 2009. Aphid fecundity and grassland invasion: invader life history is the key. Ecological Applications 19: 1187-1196.
9. Borer ET, Hosseini PR, Seabloom EW, Dobson AP. 2007. Pathogen-induced reversal of native dominance in a grassland community. Proceedings of the National Academy of Sciences, USA 104: 5473-5478.
10. Borer ET, Seabloom EW, Gruner DS, Harpole WS, Hillebrand H, Lind EM, Adler PB, Alberti J, Anderson TM, Bakker JD et al. 2014a. Herbivores and nutrients control grassland plant diversity via light limitation. Nature 508: 517-520.
11. Borer ET, Seabloom EW, Mitchell CE, Cronin JP. 2014b. Multiple nutrients and herbivores interact to govern diversity, productivity, composition, and infection in a successional grassland. Oikos 123: 214-224.
12. Borer ET, Seabloom EW, Mitchell CE, Power AG. 2010. Local context drives infection of grasses by vector-borne generalist viruses. Ecology Letters 13: 810-818.
13. Brennan RF. 1992. Effect of superphosphate and nitrogen on yield and take-all of wheat. Fertilizer Research 31: 43-49.
14. Cardinale BJ, Hillebrand H, Harpole WS, Gross K, Ptacnik R. 2009. Separating the influence of resource 'availability' from resource 'imbalance' on productivity-diversity relationships. Ecology Letters 12: 475-487.
15. Chain F, Riault G, Trottet M, Jacquot E. 2005. Analysis of accumulation patterns of Barley yellow dwarf virus-PAV (BYDV-PAV) in two resistant wheat lines. European Journal of Plant Pathology 113: 343-355.
16. Chapin FS. 1980. The mineral nutrition of wild plants. Annual Review of Ecology and Systematics 11: 233-260.
17. Chesson P. 2000. Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31: 343-367.
18. Clasen JL, Elser JJ. 2007. The effect of host Chlorella NC64A carbon: phosphorus ratio on the production of Paramecium bursaria Chlorella Virus-1. Freshwater Biology 52: 112-122.
19. Cleland EE, Harpole WS. 2010. Nitrogen enrichment and plant communities: Nitrogen enrichment and plant communities. Annals of the New York Academy of Sciences 1195: 46-61.
20. Craine JM, Morrow C, Stock WD. 2008. Nutrient concentration ratios and co-limitation in South African grasslands. New Phytologist 179: 829-836.
21. Creamer R, Falk BW. 1990. Direct detection of transcapsidated Barley Yellow Dwarf Luteoviruses in doubly infected plants. Journal of General Virology 71: 211-217.
22. D'arcy CJ. 1995. Symptomatology and host range of Barley yellow dwarf. In: D'arcy CJ, Burnett PA, eds. Barley yellow dwarf, 40 years of progress. St. Paul, MN, USA: The American Phytopathological Society, 9-28.
23. Deb M, Anderson JM. 2008. Development of a multiplexed PCR detection method for Barley and Cereal yellow dwarf viruses, Wheat spindle streak virus, Wheat streak mosaic virus and Soil-borne wheat mosaic virus. Journal of Virology Methods 148: 17-24.
24. Dordas C. 2009. Role of nutrients in controlling plant diseases in sustainable agriculture: a review. In: Lichtfouse E, Navarrete M, Debaeke P, Véronique S, Alberola C, eds. Sustainable agriculture. Dordrecht, the Netherlands: Springer, 443-460.
25. Downs RJ, Hellmers H. 1975. Environment and the experimental control of plant growth. New York, NY, USA: Academic Press.
26. Elser JJ, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie S, Fagan W, Schade J et al. 2003. Growth rate-stoichiometry couplings in diverse biota. Ecology Letters 6: 936-943.
27. Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE. 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters 10: 1135-1142.
28. Elser JJ, Fagan WF, Kerkhoff AJ, Swenson NG, Enquist BJ. 2010. Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytologist 186: 593-608.
29. Eraslan F, Akbas B, Inal A, Tarakcioglu C. 2007. Effects of foliar sprayed calcium sources onTomato mosaic virus (ToMV) infection in tomato plants grown in greenhouses. Phytoparasitica 35: 150-158.
30. 2? Plant Physiology 118: 573-580.
31. Field CJ, Johnson IR, Schley PD. 2002. Nutrients and their role in host resistance to infection. Journal of Leukocyte Biology 71: 16-32.
32. Frost PC, Ebert D, Smith VH. 2008. Responses of a bacterial pathogen to phosphorus limitation of its aquatic invertebrate host. Ecology 89: 313-318.
33. Ge S, Zheng D, Zhao Y, Liu H, Liu W, Sun Q, Li J, Yu S, Zuo Y, Han X et al. 2012. Evaluating viral interference between Influenza virus and Newcastle disease virus using real-time reverse transcription-polymerase chain reaction in chicken eggs. Virology Journal 9: 128.
34. Gent MPN, Parrish ZD, White JC. 2005. Nutrient uptake among subspecies of Cucurbita pepo L. is related to exudation of citric acid. Journal of the American Society For Horticultural Science 130: 782-788.
35. Gray S, Gildow FE. 2003. Luteovirus-aphid interactions. Annual Review of Phytopathology 41: 539-566.
36. Gray SM. 2008. Aphid transmission of plant viruses. Current Protocols in Microbiology Chapter 16: 10:16B.1.1-16B.1.10.
37. Gruner DS, Smith JE, Seabloom EW, Sandin SA, Ngai JT, Hillebrand H, Harpole WS, Elser JJ, Cleland EE, Bracken MES et al. 2008. A cross-system synthesis of consumer and nutrient resource control on producer biomass. Ecology Letters 11: 740-755.
38. Haddad NM, Haarstad J, Tilman D. 2000. The effects of long-term nitrogen loading on grassland insect communities. Oecologia 124: 73-84.
39. Haile D, Nigussie D, Ayana A. 2012. Nitrogen use efficiency of bread wheat: effects of nitrogen rate and time of application. Journal of Soil Science and Plant Nutrition 12: 389-409.
40. Halbert S, Voegtlin D. 1995. Biology and taxonomy of vectors of Barley yellow dwarf viruses. In: D'arcy CJ, Burnett PA, eds. Barley yellow dwarf, 40 years of progress. St. Paul, MN, USA: The American Phytopathological Society, 217-258.
41. Hall GS, Little DP. 2013. Within-host competition between barley yellow dwarf-PAV and -PAS. Virus Research 174: 148-151.
42. Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken MES, Elser JJ, Gruner DS, Hillebrand H, Shurin JB et al. 2011. Nutrient co-limitation of primary producer communities: community co-limitation. Ecology Letters 14: 852-862.
43. Hessen DO, Elser JJ, Sterner RW, Urabe J. 2013. Ecological stoichiometry: an elementary approach using basic principles. Limnology and Oceanography 58: 2219-2236.
44. Hewings AD. 1995. Purification and virion characterization of Barley yellow dwarf viruses. In: D'arcy CJ, Burnett PA, eds. Barley yellow dwarf, 40 years of progress. St. Paul, MN, USA: The American Phytopathological Society, 165-179.
45. Hillebrand H, Matthiessen B. 2009. Biodiversity in a complex world: consolidation and progress in functional biodiversity research. Ecology Letters 12: 1405-1419.
46. Hoagland DR, Arnon DI. 1938. The water culture method for growing plants without soil. California Agricultural Experiment Station Circular 347: 1-32.
47. Hoffland E, Jeger MJ, Van Beusichem ML. 2000. Effect of nitrogen supply rate on disease resistance in tomato depends on the pathogen. Plant and Soil 218: 239-247.
48. Honek A. 1991. Nitrogen-fertilization and abundance of the cereal aphids Metopolophium dirhodum and Sitobion avenae (Homoptera, Aphididae). Zeitschrift fur Pflanzenkrankheiten und Pflanzenschutz-Journal of Plant Diseases and Protection 98: 655-660.
49. Irwin ME, Thresh JM. 1990. Epidemiology of Barley Yellow Dwarf - a study in ecological complexity. Annual Review of Phytopathology 28: 393-424.
50. Kamal SM, Bianchi L, Al Tawil A, Koziel M, El Sayed Khalifa K, Peter T, Rasenack JW. 2001. Specific cellular immune response and cytokine patterns in patients coinfected with Hepatitis C Virus and Schistosoma mansoni. The Journal of Infectious Diseases 184: 972-982.
51. Kaplan RC, Bergman EL. 1985. Virus infection and nutrient elemental content of the host plant: a review. Communications in Soil Science and Plant Analysis 16: 439-465.
52. Karley AJ, Hawes C, Iannetta PPM, Squire GR. 2008. Intraspecific variation in Capsella bursa-pastoris in plant quality traits for insect herbivores. Weed Research 48: 147-156.
53. Karpinets TV, Greenwood DJ, Sams CE, Ammons JT. 2006. RNA: protein ratio of the unicellular organism as a characteristic of phosphorous and nitrogen stoichiometry and of the cellular requirement of ribosomes for protein synthesis. Bmc Biology 4: 1-10.
54. Kirkegaard JA, Howe GN, Mele PM. 1999. Enhanced accumulation of mineral-N following canola. Australian Journal of Experimental Agriculture 39: 587-593.
55. Koskella B, Giraud T, Hood ME. 2006. Pathogen relatedness affects the prevalence of within-host competition. The American Naturalist 168: 121-126.
56. Kostandi SF, Soliman MF. 1991. The significance of NPK fertilizers on yield and smut incidence of corn. Journal of Agronomy and Crop Science-Zeitschrift fur Acker und Pflanzenbau 167: 269-276.
57. Lal RB, Rudolph D, Alpers MP, Sulzer AJ, Yaping S, Lal AA. 1994. Immunological cross-reactivity between structural proteins of Human T-cell Lymphotropic Virus Type-I and the blood-stage of Plasmodium falciparum. Clinical and Diagnostic Laboratory Immunology 1: 5-10.
58. Leclercq-Le Quillec F, Plantegenest M, Riault G, Dedryver CA. 2000. Analyzing and modeling temporal disease progress of Barley yellow dwarf virus serotypes in barley fields. Phytopathology 90: 860-866.
59. Lello J, Boag B, Fenton A, Stevenson IR, Hudson PJ. 2004. Competition and mutualism among the gut helminths of a mammalian host. Nature 428: 840-844.
60. MacArthur RH. 1972. Geographical ecology: patterns in the distribution of species. Princeton, NJ, USA: Princeton University Press.
61. Malmstrom CM, Hughes CC, Newton LA, Stoner CJ. 2005a. Virus infection in remnant native bunchgrasses from invaded California grasslands. New Phytologist 168: 217-230.
62. Malmstrom CM, McCullough AJ, Johnson HA, Newton LA, Borer ET. 2005b. Invasive annual grasses indirectly increase virus incidence in California native perennial bunchgrasses. Oecologia 145: 153-164.
63. Marks F. 1996. Protein phosphorylation. New York, NY, USA, Weinheim, Germany: VCH Publishers Inc.
64. Maule A, Leh V, Lederer C. 2002. The dialogue between viruses and hosts in compatible interactions. Current Opinion in Plant Biology 5: 279-284.
65. McCullagh P, Nelder J. 1989. Generalized linear models. New York, USA: Chapman and Hall.
66. Merrett MJ, Sunderland DW. 1965. Some effects of phosphorus on phosphorus compounds of Tobacco mosaic virus infected and non infected tissue cultures. Physiologia Plantarium 18(410): 417.
67. Miller TE, Burns JH, Munguia P, Walters EL, Kneitel JM, Richards PM, Mouquet N, Buckley HL. 2005. A critical review of twenty years' use of the resource-ratio theory. The American Naturalist 165: 439-448.
68. Miller WA, Rasochova L. 1997. Barley yellow dwarf viruses. Annual Review of Phytopathology 35: 167-190.
69. 2, nitrogen deposition, and decreased species diversity on foliar fungal plant disease. Global Change Biology 9: 438-451.
70. Montefiori DC, Pantaleo G, Fink LM, Zhou JT, Zhou JY, Bilska M, Miralles GD, Fauci AS. 1996. Neutralizing and infection-enhancing antibody responses to human immunodeficiency virus type 1 in long-term nonprogressors. Journal of Infectious Diseases 173: 60-67.
71. Pedersen AB, Fenton A. 2007. Emphasizing the ecology in parasite community ecology. Trends in Ecology&Evolution 22: 133-139.
72. Perry KL, Kolb FL, Sammons B, Lawson C, Cisar G, Ohm H. 2000. Yield effects of Barley yellow dwarf virus in soft red winter wheat. Phytopathology 90: 1043-1048.
73. Pinheiro JC, Bates DM. 2000. Mixed effects models in S and S-Plus. New York, USA: Springer-Verlag.
74. Power AG, Gray SM. 1995. Aphid Transmission of Barley yellow dwarf viruses: interactions between viruses, vectors and host plants. In: D'arcy CJ, Burnett PA, eds. Barley Yellow Dwarf: 40 years of progress. St Paul, MN, USA: The American Phytopathological Society, 259-289.
75. Reuveni M, Agapov V, Reuveni R. 1997. A foliar spray of micronutrient solutions induces local and systemic protection against powdery mildew (Sphaerotheca fuliginia) in cucumber plants. European Journal of Plant Pathology 103: 581-588.
76. Richardson SJ, Press MC, Parsons AN, Hartley SE. 2002. How do nutrients and warming impact on plant communities and their insect herbivores? A 9-year study from a sub-Arctic heath. Journal of Ecology 90: 544-556.
77. Rigaud T, Perrot-Minnot M-J, Brown MJF. 2010. Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proceedings of the Royal Society B: Biological Sciences 277: 3693-3702.
78. Robertson NL, French R. 2007. Genetic structure in natural populations of barley/cereal yellow dwarf virus isolates from Alaska. Archives of Virology 152: 891-902.
79. Rockstrom J, Steffen W, Noone K, Persson A, Chapin FS, Lambin EF, Lenton TM, Scheffer M, Folke C, Schellnhuber HJ et al. 2009. A safe operating space for humanity. Nature 461: 472-475.
80. Rousk J, Brookes PC, Bååth E. 2011. Fungal and bacterial growth responses to N fertilization and pH in the 150-year 'Park Grass' UK grassland experiment: N and pH influence on microbial growth in grassland soils. FEMS Microbiology Ecology 76: 89-99.
81. 2 spurs reciprocal positive effects between a plant virus and an arbuscular mycorrhizal fungus. New Phytologist 199: 541-549.
82. Salvaudon L, De Moraes CM, Mescher MC. 2013. Outcomes of co-infection by two potyviruses: implications for the evolution of manipulative strategies. Proceedings of the Royal Society B: Biological Sciences 280: 20122959.
83. Seabloom EW, Benfield CD, Borer ET, Stanley AG, Kaye TN, Dunwiddie PW. 2011. Provenance, life span, and phylogeny do not affect grass species' responses to nitrogen and phosphorus. Ecological Applications 21: 2129-2142.
84. Seabloom EW, Borer ET, Jolles A, Mitchell CE. 2009. Direct and indirect effects of viral pathogens and the environment on invasive grass fecundity in Pacific Coast grasslands. Journal of Ecology 97: 1264-1273.
85. Seabloom EW, Borer ET, Lacroix C, Mitchell CE, Power AG. 2013. Richness and composition of niche-assembled viral pathogen communities. PLoS ONE 8: e55675.
86. Seabloom EW, Borer ET, Mitchell CE, Power AG. 2010. Viral diversity and prevalence gradients in North American Pacific Coast grasslands. Ecology 91: 721-732.
87. Selman IW, Grant SA. 1957. Some effects of nitrogen supply on the infection of tomato plants with Tomato spotted wilt virus. Annals of Applied Biology 45: 448-455.
88. Shetty NP, Jorgensen HJL, Jensen JD, Collinge DB, Shetty HS. 2008. Roles of reactive oxygen species in interactions between plants and pathogens. European Journal of Plant Pathology 121: 267-280.
89. Smith V. 2007. Host resource supplies influence the dynamics and outcome of infectious disease. Integrative and Comparative Biology 47: 310-316.
90. Smith VH. 1993. Resource competition between host and pathogen. BioScience 43: 21-30.
91. Smith VH, Holt RD. 1996. Resource competition and within-host disease dynamics. Trends in Ecology&Evolution 11: 386-389.
92. Solomon PS, Tan KC, Oliver RP. 2003. The nutrient supply of pathogenic fungi: a fertile field for study. Molecular Plant Pathology 4: 203-210.
93. Spencer EL. 1941. Influence of nitrogen supply on the rate of multiplication of Tobacco mosaic virus. Plant Physiology 16: 663-675.
94. Sterner RW, Elser JJ. 2002. Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton, NJ, USA: Princeton University Press.
95. Tilman D. 1977. Resource competition between plankton algae: an experimental and theoretical approach. Ecology 58: 338-348.
96. Tilman D. 1982. Resource competition and community structure. Princeton, NJ, USA: Princton University Press.
97. Tilman D, Fargione J, Wolff B, D'Antonio C, Dobson A, Howarth R, Schindler D, Schlesinger WH, Simberloff D, Swackhamer D. 2001. Forecasting agriculturally driven global environmental change. Science 292: 281-284.
98. Tirado SMC, Yoon K-J. 2003. Antibody-dependent enhancement of virus infection and disease. Viral Immunology 16: 69-86.
99. Turner PE. 2005. Parasitism between co-infecting bacteriophages. Advances in Ecological Research 37: 309-332.
100. Urbino C, Gutiérrez S, Antolik A, Bouazza N, Doumayrou J, Granier M, Martin DP, Peterschmitt M. 2013. Within-host dynamics of the emergence of Tomato Yellow Leaf Curl Virus recombinants. PLoS ONE 8: e58375.
101. Vitousek PM, Walker LR, Whiteaker LD, Matson PA. 1993. Nutrient limitations to plant growth during primary succession in Hawaii Volcanoes National Park. Biogeochemistry 23: 197-215.
102. Vörösmarty CJ, McIntyre PB, Gessner MO, Dudgeon D, Prusevich A, Green P, Glidden S, Bunn SE, Sullivan CA, Liermann CR et al. 2010. Global threats to human water security and river biodiversity. Nature 467: 555-561.
103. Williams RF. 1948. The effects of phosphorus supply on the rates of intake of phosphorus and nitrogen and upon certain aspects of phosphorus metabolism in gramineous plants. Australian Journal of Biological Sciences 1: 333-361.
104. Zehnder CB, Hunter MD. 2009. More is not necessarily better: the impact of limiting and excessive nutrients on herbivore population growth rates. Ecological Entomology 34: 535-543.