title: Interfamilial recombination between viruses led to acquisition of a novel translation-enhancing RNA element that allows resistance breaking.
abstract: 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.
authors.affiliation: Centro de Edafología y Biología Aplicada del Segura (CEBAS), Consejo Superior de Investigaciones Científicas (CSIC), Apdo. Correos 164, 30100, Espinardo, Murcia, Spain.
authors.forename: Manuel
authors.initials: M
authors.lastname: Miras
authors.affiliation: Centro de Edafología y Biología Aplicada del Segura (CEBAS), Consejo Superior de Investigaciones Científicas (CSIC), Apdo. Correos 164, 30100, Espinardo, Murcia, Spain.
authors.forename: Raquel N
authors.initials: RN
authors.lastname: Sempere
authors.affiliation: Department of Plant Pathology and Microbiology, Iowa State University, 351 Bessey Hall, Ames, IA, 50011, USA.
authors.forename: Jelena J
authors.initials: JJ
authors.lastname: Kraft
authors.affiliation: Department of Plant Pathology and Microbiology, Iowa State University, 351 Bessey Hall, Ames, IA, 50011, USA.
authors.forename: W Allen
authors.initials: WA
authors.lastname: Miller
authors.affiliation: Centro de Edafología y Biología Aplicada del Segura (CEBAS), Consejo Superior de Investigaciones Científicas (CSIC), Apdo. Correos 164, 30100, Espinardo, Murcia, Spain.
authors.forename: Miguel A
authors.initials: MA
authors.lastname: Aranda
authors.affiliation: Centro de Edafología y Biología Aplicada del Segura (CEBAS), Consejo Superior de Investigaciones Científicas (CSIC), Apdo. Correos 164, 30100, Espinardo, Murcia, Spain.
authors.forename: Veronica
authors.initials: V
authors.lastname: Truniger
mesh_terms: D001483:Base Sequence; D060467:Disease Resistance / Q000276:immunology*; D004742:Enhancer Elements, Genetic / Q000235:genetics; D039561:Eukaryotic Initiation Factor-4E / Q000378:metabolism; D058507:Host Specificity; D052679:Luteoviridae / Q000235:genetics* / Q000502:physiology; D008969:Molecular Sequence Data; D016254:Mutagenesis, Insertional / Q000235:genetics; D009690:Nucleic Acid Conformation; D010935:Plant Diseases / Q000276:immunology / Q000821:virology*; D014176:Protein Biosynthesis / Q000235:genetics*; D012315:RNA Caps / Q000378:metabolism; D012367:RNA, Viral / Q000737:chemistry / Q000235:genetics*; D011995:Recombination, Genetic; D019183:Tombusviridae / Q000235:genetics* / Q000302:isolation & purification / Q000472:pathogenicity / Q000502:physiology; D014774:Virulence
chemical_list: D039561:Eukaryotic Initiation Factor-4E; D012315:RNA Caps; D012367:RNA, Viral
keywords: 3′-UTR cap-independent translation enhancer (3′-CITE); Cucurbit aphid borne yellows virus (CABYV); Melon necrotic spot virus (MNSV); cap-independent translation; eukaryotic translation initiation factor 4E (eIF4E); recessive resistance; recombination; resistance breaking