Environment and evolution modulate plant virus pathogenesis.

The study of plant viruses has focussed on those causing diseases in crops and, only recently, in wild plants. However, increasing evidence shows that plant viruses often are neutral, or even beneficial, for their hosts. Thus, plant viruses can be conditional mutualists, although the underlying mechanisms have been seldom analyzed. Little is known about what environmental factors modulate virus pathogenesis, and how. A major factor can be higher horizontal transmission rates in agricultural than in wild ecosystems. However, ecosystem simplification in human-managed habitats may result in changed epidemiological factors that influence pathogenesis. The interplay between ecology, evolution and pathogenesis awaits further research.

[1]  S. Sacristán,et al.  Association and Host Selectivity in Multi-Host Pathogens , 2006, PloS one.

[2]  J. García,et al.  How do plant viruses induce disease? Interactions and interference with host components. , 2011, The Journal of general virology.

[3]  M. Milgroom,et al.  Vertical Transmission Selects for Reduced Virulence in a Plant Virus and for Increased Resistance in the Host , 2014, PLoS pathogens.

[4]  Santiago F. Elena,et al.  Distribution of Fitness and Virulence Effects Caused by Single-Nucleotide Substitutions in Tobacco Etch Virus , 2007, Journal of Virology.

[5]  C A Gilligan,et al.  Disease control and its selection for damaging plant virus strains in vegetatively propagated staple food crops; a theoretical assessment , 2007, Proceedings of the Royal Society B: Biological Sciences.

[6]  M. Manns,et al.  Hepatitis A virus infection suppresses hepatitis C virus replication and may lead to clearance of HCV. , 2006, Journal of hepatology.

[7]  L. Kramer,et al.  The evolution of virulence of West Nile virus in a mosquito vector: implications for arbovirus adaptation and evolution , 2013, BMC Evolutionary Biology.

[8]  Samuel Alizon PARASITE CO‐TRANSMISSION AND THE EVOLUTIONARY EPIDEMIOLOGY OF VIRULENCE , 2013, Evolution; international journal of organic evolution.

[9]  S. Elena,et al.  Differences in Accumulation and Virulence Determine the Outcome of Competition during Tobacco etch virus Coinfection , 2011, PloS one.

[10]  Peter Daszak,et al.  Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. , 2004, Trends in ecology & evolution.

[11]  Martin Samuelsson,et al.  A Genetic Basis of Susceptibility to Acute Pyelonephritis , 2007, PloS one.

[12]  J. Bull,et al.  Theory and Empiricism in Virulence Evolution , 2014, PLoS pathogens.

[13]  E. Borer,et al.  Non-random biodiversity loss underlies predictable increases in viral disease prevalence , 2014, Journal of The Royal Society Interface.

[14]  S. Howell,et al.  Cauliflower mosaic virus gene VI produces a symptomatic phenotype in transgenic tobacco plants. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[15]  F. Breinig,et al.  The viral killer system in yeast: from molecular biology to application. , 2002, FEMS microbiology reviews.

[16]  N. Bosque-pérez,et al.  Variation in barley yellow dwarf virus transmission efficiency by Rhopalosiphum padi (Homoptera: Aphididae) after acquisition from transgenic and nontransformed wheat genotypes. , 2004, Journal of economic entomology.

[17]  A. Fraile,et al.  Virulence evolution of a generalist plant virus in a heterogeneous host system , 2013, Evolutionary applications.

[18]  N. Mideo,et al.  Virulence evolution and the trade‐off hypothesis: history, current state of affairs and the future , 2009, Journal of evolutionary biology.

[19]  D. Martin,et al.  Sequence diversity and virulence in Zea mays of Maize streak virus isolates. , 2001, Virology.

[20]  N. Colegrave,et al.  The Coevolution of Virulence: Tolerance in Perspective , 2010, PLoS pathogens.

[21]  D. Piñero,et al.  Landscape heterogeneity shapes host‐parasite interactions and results in apparent plant–virus codivergence , 2013, Molecular ecology.

[22]  F. García-Arenal,et al.  Transmissibility of Cucumber mosaic virus by Aphis gossypii Correlates with Viral Accumulation and Is Affected by the Presence of Its Satellite RNA. , 2000, Phytopathology.

[23]  J. Bull,et al.  SELECTION OF BENEVOLENCE IN A HOST–PARASITE SYSTEM , 1991, Evolution; international journal of organic evolution.

[24]  C. Mitchell,et al.  The role of viruses in biological invasions: friend or foe? , 2011, Current opinion in virology.

[25]  Sylvain Gandon,et al.  Evolution of Virulence in Emerging Epidemics , 2013, PLoS pathogens.

[26]  Y. Michalakis,et al.  Adaptive virulence evolution: the good old fitness-based approach. , 2015, Trends in ecology & evolution.

[27]  M. Roossinck,et al.  Plant virus metagenomics: what we know and why we need to know more , 2014, Front. Plant Sci..

[28]  I. Cooper,et al.  Wild plants and viruses: under-investigated ecosystems. , 2006, Advances in virus research.

[29]  J. Bull,et al.  Virulence evolution in a virus obeys a trade off , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[30]  C. Malmstrom,et al.  Virus infection in remnant native bunchgrasses from invaded California grasslands. , 2005, The New phytologist.

[31]  W. Dawson,et al.  A point mutation in the tobacco mosaic virus capsid protein gene induces hypersensitivity in Nicotiana sylvestris. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[32]  A. Fraile,et al.  Arabidopsis thaliana as a model for the study of plant–virus co-evolution , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[33]  M. Roossinck,et al.  Plant virus metagenomics: biodiversity and ecology. , 2012, Annual review of genetics.

[34]  D. Ebert The Epidemiology and Evolution of Symbionts with Mixed-Mode Transmission , 2013 .

[35]  S. Eigenbrode,et al.  Transmission mechanisms shape pathogen effects on host–vector interactions: evidence from plant viruses , 2012 .

[36]  E. Stukenbrock,et al.  The origins of plant pathogens in agro-ecosystems. , 2008, Annual review of phytopathology.

[37]  J. Sinclair,et al.  Human cytomegalovirus modulation of CCR5 expression on myeloid cells affects susceptibility to human immunodeficiency virus type 1 infection. , 2006, The Journal of general virology.

[38]  H. R. Prendeville,et al.  Effects of virus on plant fecundity and population dynamics. , 2014, The New phytologist.

[39]  T. Scott,et al.  Mode of transmission and the evolution of arbovirus virulence in mosquito vectors , 2009, Proceedings of the Royal Society B: Biological Sciences.

[40]  T. Saito,et al.  Coat protein gene sequence of tobacco mosaic virus encodes a host response determinant. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[41]  F. García-Arenal,et al.  Ecosystem simplification, biodiversity loss and plant virus emergence , 2015, Current Opinion in Virology.

[42]  J. hily,et al.  Environment and host genotype determine the outcome of a plant-virus interaction: from antagonism to mutualism. , 2016, The New phytologist.

[43]  F. García-Arenal,et al.  Differential Tolerance to Direct and Indirect Density-Dependent Costs of Viral Infection in Arabidopsis thaliana , 2009, PLoS pathogens.

[44]  A. Wargo,et al.  Virulence correlates with fitness in vivo for two M group genotypes of Infectious hematopoietic necrosis virus (IHNV). , 2010, Virology.

[45]  D. Piñero,et al.  Effect of Biodiversity Changes in Disease Risk: Exploring Disease Emergence in a Plant-Virus System , 2012, PLoS pathogens.

[46]  Andrew D Stewart,et al.  AN EMPIRICAL STUDY OF THE EVOLUTION OF VIRULENCE UNDER BOTH HORIZONTAL AND VERTICAL TRANSMISSION , 2005, Evolution; international journal of organic evolution.

[47]  F. García-Arenal,et al.  The Relationship of Within-Host Multiplication and Virulence in a Plant-Virus System , 2007, PloS one.

[48]  L. Sumner,et al.  Virus infection improves drought tolerance. , 2008, The New phytologist.

[49]  E. Borer,et al.  Invasive annual grasses indirectly increase virus incidence in California native perennial bunchgrasses , 2005, Oecologia.

[50]  M. Roossinck Move Over, Bacteria! Viruses Make Their Mark as Mutualistic Microbial Symbionts , 2015, Journal of Virology.

[51]  S. Fellous,et al.  How can your parasites become your allies? , 2009, Trends in parasitology.

[52]  S. Sacristán,et al.  The evolution of virulence and pathogenicity in plant pathogen populations , 2010 .

[53]  Samuel Alizon,et al.  Multiple infections and the evolution of virulence. , 2013, Ecology letters.

[54]  M. Roossinck The good viruses: viral mutualistic symbioses , 2011, Nature Reviews Microbiology.

[55]  Sam P. Brown,et al.  Ecology of Microbial Invasions: Amplification Allows Virus Carriers to Invade More Rapidly When Rare , 2006, Current Biology.

[56]  Alberto Fereres,et al.  Insect vectors as drivers of plant virus emergence. , 2015, Current opinion in virology.

[57]  H. R. Prendeville,et al.  Virus infections in wild plant populations are both frequent and often unapparent. , 2012, American journal of botany.

[58]  A. Wargo,et al.  In Vivo Fitness Associated with High Virulence in a Vertebrate Virus Is a Complex Trait Regulated by Host Entry, Replication, and Shedding , 2011, Journal of Virology.

[59]  Samuel Alizon,et al.  Multiple Infections, Immune Dynamics, and the Evolution of Virulence , 2008, The American Naturalist.

[60]  R. Froissart,et al.  Reduction of leaf area and symptom severity as proxies of disease-induced plant mortality: the example of the Cauliflower mosaic virus infecting two Brassicaceae hosts. , 2013, Virus research.

[61]  E. Borer,et al.  The community ecology of barley/cereal yellow dwarf viruses in Western US grasslands. , 2011, Virus research.

[62]  A. Fraile,et al.  THE EVOLUTION OF VIRULENCE IN A PLANT VIRUS , 2003, Evolution; international journal of organic evolution.

[63]  Y. Michalakis,et al.  Pleiotropic action of parasites: How to be good for the host. , 1992, Trends in ecology & evolution.

[64]  A. Jarosz,et al.  Effects of disease in wild plant populations and the evolution of pathogen aggressiveness , 1995 .

[65]  A. Gibbs A plant virus that partially protects its wild legume host against herbivores. , 1980, Intervirology.

[66]  R. Senoussi,et al.  Narrow Bottlenecks Affect Pea Seedborne Mosaic Virus Populations during Vertical Seed Transmission but not during Leaf Colonization , 2014, PLoS pathogens.

[67]  R. Froissart,et al.  AN EXPERIMENTAL TEST OF THE TRANSMISSION‐VIRULENCE TRADE‐OFF HYPOTHESIS IN A PLANT VIRUS , 2013, Evolution; international journal of organic evolution.

[68]  K. A. Garrett,et al.  Plant-virus interactions and the agro-ecological interface , 2013, European Journal of Plant Pathology.