Interfamilial recombination between viruses led to acquisition of a novel translation-enhancing RNA element that allows resistance breaking


Publication Type:

Journal Article


New Phytol, Volume 202, Number 1, p.233-46 (2014)


1469-8137 (Electronic)<br/>0028-646X (Linking)

Accession Number:



Base Sequence, Disease Resistance/ immunology, Enhancer Elements, Genetic/genetics, Eukaryotic Initiation Factor-4E/metabolism, Host Specificity, Luteoviridae/ genetics/physiology, Molecular Sequence Data, Mutagenesis, Insertional/genetics, Nucleic Acid Conformation, Plant Diseases/immunology/ virology, Protein Biosynthesis/ genetics, Recombination, Genetic, RNA Caps/metabolism, RNA, Viral/chemistry/ genetics, Tombusviridae/ genetics/isolation & purification/pathogenicity/physiology, Virulence


Many plant viruses depend on functional RNA elements, called 3'-UTR cap-independent translation enhancers (3'-CITEs), for translation of their RNAs. In this manuscript we provide direct proof for the existing hypothesis that 3'-CITEs are modular and transferable by recombination in nature, and that this is associated with an advantage for the created virus. By characterizing a newly identified Melon necrotic spot virus (MNSV; Tombusviridae) isolate, which is able to overcome eukaryotic translation initiation factor 4E (eIF4E)-mediated resistance, we found that it contains a 55 nucleotide insertion in its 3'-UTR. We provide strong evidence that this insertion was acquired by interfamilial recombination with the 3'-UTR of an Asiatic Cucurbit aphid-borne yellows virus (CABYV; Luteoviridae). By constructing chimeric viruses, we showed that this recombined sequence is responsible for resistance breaking. Analysis of the translational efficiency of reporter constructs showed that this sequence functions as a novel 3'-CITE in both resistant and susceptible plants, being essential for translation control in resistant plants. In conclusion, we showed that a recombination event between two clearly identified viruses from different families led to the transfer of exactly the sequence corresponding to a functional RNA element, giving rise to a new isolate with the capacity to infect an otherwise nonsusceptible host.


Miras, Manuel<br/>Sempere, Raquel N<br/>Kraft, Jelena J<br/>Miller, W Allen<br/>Aranda, Miguel A<br/>Truniger, Veronica<br/>R01 GM067104/GM/NIGMS NIH HHS/United States<br/>Research Support, Non-U.S. Gov't<br/>Research Support, U.S. Gov't, Non-P.H.S.<br/>England<br/>New Phytol. 2014 Apr;202(1):233-46. doi: 10.1111/nph.12650. Epub 2013 Dec 24.