Random Plant Viral Variants Attain Temporal Advantages During Systemic Infections and in Turn Resist other Variants of the Same Virus.
Infection of plants with viruses containing multiple variants frequently leads to dominance by a few random variants in the systemically infected leaves (SLs), for which a plausible explanation is lacking. We show here that SL dominance by a given viral variant is adequately explained by its fortuitous lead in systemic spread, coupled with its resistance to superinfection by other variants. We analyzed the fate of a multi-variant turnip crinkle virus (TCV) population in Arabidopsis and N. benthamiana plants. Both wild-type and RNA silencing-defective plants displayed a similar pattern of random dominance by a few variant genotypes, thus discounting a prominent role for RNA silencing. When introduced to plants sequentially as two subpopulations, a twelve-hour head-start was sufficient for the first set to dominate. Finally, SLs of TCV-infected plants became highly resistant to secondary invasions of another TCV variant. We propose that random distribution of variant foci on inoculated leaves allows different variants to lead systemic movement in different plants. The leading variants then colonize large areas of SLs, and resist the superinfection of lagging variants in the same areas. In conclusion, superinfection resistance is the primary driver of random enrichment of viral variants in systemically infected plants.
Department of Plant Pathology , Ohio Agricultural Research and Development Center, The Ohio State University, 024 Selby Hall, 1680 Madison Ave, Wooster, 44691, US.|State Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing, 100193, China.
Xiao-Feng
XF
Zhang
Department of Plant Pathology , Ohio Agricultural Research and Development Center, The Ohio State University, 024 Selby Hall, 1680 Madison Ave, Wooster, 44691, US.|School of Mathematics, Physics and Biological Engineering, Inner Mongolia University of Science and Technology, 27 Shaoxian Rd, Qingshan, Baotou, China.
Jiangbo
J
Guo
Department of Plant Pathology , Ohio Agricultural Research and Development Center, The Ohio State University, 024 Selby Hall, 1680 Madison Ave, Wooster, 44691, US.|Key Laboratory of Biology and Genetic Resources of Tropical Crops, ITBB, CATAS, Haikou, 571101, PR, China.
Xiuchun
X
Zhang
Department of Plant Pathology , Ohio Agricultural Research and Development Center, The Ohio State University, 024 Selby Hall, 1680 Madison Ave, Wooster, 44691, US.|Molecular and Cellular Imaging Center, Ohio Agricultural Research and Development Center, The Ohio State University, 025 Selby Hall, 1680 Madison Ave, Wooster, 44691, US.
Tea
T
Meulia
Department of Plant Pathology , Ohio Agricultural Research and Development Center, The Ohio State University, 024 Selby Hall, 1680 Madison Ave, Wooster, 44691, US.
Pierce
P
Paul
Department of Plant Pathology , Ohio Agricultural Research and Development Center, The Ohio State University, 024 Selby Hall, 1680 Madison Ave, Wooster, 44691, US.
Laurence V
LV
Madden
State Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing, 100193, China.
Dawei
D
Li
Department of Plant Pathology , Ohio Agricultural Research and Development Center, The Ohio State University, 024 Selby Hall, 1680 Madison Ave, Wooster, 44691, US.
Feng
F
Qu
D017360:Arabidopsis / Q000821:virology; D019184:Carmovirus / Q000502:physiology; D023061:Gene Order; D014644:Genetic Variation; D016679:Genome, Viral; D008954:Models, Biological; D010935:Plant Diseases / Q000821:virology*; D018515:Plant Leaves / Q000821:virology; D010942:Plant Viruses / Q000502:physiology*; D014762:Viral Interference