Interfamilial recombination between viruses led to acquisition of a novel translation-enhancing RNA element that allows resistance breaking
Article first published online: 24 DEC 2013
© 2013 The Authors. New Phytologist © 2013 New Phytologist Trust
Volume 202, Issue 1, pages 233–246, April 2014
How to Cite
Miras, M., Sempere, R. N., Kraft, J. J., Miller, W. A., Aranda, M. A. and Truniger, V. (2014), Interfamilial recombination between viruses led to acquisition of a novel translation-enhancing RNA element that allows resistance breaking. New Phytologist, 202: 233–246. doi: 10.1111/nph.12650
- Issue published online: 25 FEB 2014
- Article first published online: 24 DEC 2013
- Manuscript Accepted: 19 NOV 2013
- Manuscript Received: 30 AUG 2013
- Ministerio de Ciencia e Innovación. Grant Numbers: AGL2009-07552/AGR, EUI2009-04009
- USDA National Research Initiative. Grant Number: 2011-67012-30715
- 3′-UTR cap-independent translation enhancer (3′-CITE);
- cap-independent translation;
- Cucurbit aphid borne yellows virus (CABYV);
- eukaryotic translation initiation factor 4E (eIF4E);
- Melon necrotic spot virus (MNSV);
- recessive resistance;
- resistance breaking
- 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.