Genetic diversity of avian paramyxovirus type 1: Proposal for a unified nomenclature and classification system of Newcastle disease virus genotypes Diego G. Diel a , Luciana H.A. da Silva a,b , Hualei Liu c , Zhiliang Wang c , Patti J. Miller a , Claudio L. Afonso a,⇑ a Southeast Poultry Research Laboratory, United States Department of Agriculture, Agricultural Research Services, 934 College Station Rd., Athens, GA 30605, United States b Laboratory of Animal Virology, Institute of Biology, State University of Campinas, Campinas, SP, Brazil c National Reference Laboratory for Newcastle Disease, China Animal Health and Epidemiology Center (CAHEC), 369 Nanjing Road, Qingdao 266032, China article info Article history: Received 20 April 2012 Received in revised form 11 July 2012 Accepted 12 July 2012 Available online 7 August 2012 Keywords: APMV-1 NDV Newcastle disease Evolution Epidemiology Genotyping abstract The avian paramyxovirus type 1 (APMV-1), or Newcastle disease virus (NDV), comprise a diverse group of viruses with a single-stranded, negative-sense RNA genome. Historically, two systems have been simul- taneously used to classify NDV isolates into lineages or genotypes, generating confusion in the nomencla- ture and discrepancies in the assignment of genetic groups. In the present study we assessed the genetic diversity of the avian paramyxovirus type-1 (APMV-1) and propose a unified nomenclature and a classi- fication system based on objective criteria to separate NDV into genotypes. Complete F gene sequences of class I (n = 110) and class II (n = 602) viruses were used for the phylogenetic reconstruction and to iden- tify distinct taxonomic groups. The mean interpopulational evolutionary distance was estimated (10%) and set as the cutoff value to assign new genotypes. Results of our study revealed that class I viruses com- prise a single genotype, while class II contains 15 genetic groups including 10 previously established (I– IX, and XI) and five new genotypes (X, XII, XIII, XIV and XV). Sub-genotypes were identified among class I and class II genotypes. Adoption of a unified nomenclature and of objective criteria to classify NDV iso- lates will facilitate studies on NDV epidemiology, evolution, disease control and diagnostics. Published by Elsevier B.V. 1. Introduction Newcastle disease virus (NDV), or avian paramyxovirus type 1 (APMV-1), is a member of the genus Avulavirus of the family Paramyxoviridae (Alexander and Senne, 2008). The APMV type 1 comprise a diverse group of viruses with a single-stranded, nega- tive-sense RNA genome (Alexander and Senne, 2008). As for other RNA viruses, the evolutionary dynamics of NDV is determined mainly by positive and negative selection and by the inherent error rate of the viral RNA dependent RNA polymerase (Holland et al., 1982; Chare et al., 2003; Miller et al., 2009b). While selection and polymerase errors are the main forces driving the evolution of NDV, it has been suggested that recombination may also play a role in shaping the genetic structure of the APMV type 1 (Han et al., 2008; Qin et al., 2008a,b; Miller et al., 2009b; Zhang et al., 2010). Since the emergence of NDV in 1926, several genetic groups (lineages or genotypes) have been identified among the APMV-1 (Aldous et al., 2003; Cattoli et al., 2010; Miller et al., 2010), and phylogenetic studies have shown that viruses of distinct genetic groups undergo simultaneous evolutionary changes in different geographic locations of the world (Miller et al., 2010, 2009b). This evolutionary dynamics impose significant difficulties for disease control and diagnosis (Cattoli et al., 2010; Kim et al., 2007b; Miller et al., 2010; Rue et al., 2010). It has been shown, for example, that genotype-heterologous vaccines are less effective in preventing virus replication and shedding after challenge (Miller et al., 2007, 2009a). Therefore, genotype-homologous vaccines have been developed and are available in countries that experience signifi- cant economical burdens due to ND outbreaks (Hu et al., 2009, 2011; IASA – Investigación Aplicada S.A. de C.V., 2012). Evolution- ary changes on the NDV genome have also been implicated in the failure of standard diagnostic tests to detect new genetic variants of the virus (Cattoli et al., 2010; Diel et al., 2011; Khan et al., 2010; Rue et al., 2010), requiring the development of new diagnos- tic tests to effectively detect variant viruses. These observations highlight the importance of constant epidemiologic and molecular surveillance for NDV. Historically, NDV isolates have been classified into lineages or genotypes based on the phylogenetic analysis of the partial or complete nucleotide sequences of the fusion (F) gene (Aldous et al., 2003; Cattoli et al., 2010; Czeglédi et al., 2006; Kim et al., 2007a,b, 2008; Liu et al., 2003; Perozo et al., 2008; Snoeck et al., 2009). The lineage classification, was defined by Aldous and collab- orators, and initially grouped NDV isolates into six lineages (1–6) and 13 sub-lineages (Aldous et al., 2003), with one additional line- age (lineage 7) and seven sub-lineages being proposed later 1567-1348/$ - see front matter Published by Elsevier B.V. http://dx.doi.org/10.1016/j.meegid.2012.07.012 ⇑ Corresponding author. Tel.: +1 706 546 3462; fax: +1 706 546 3161. E-mail address: claudio.afonso@ars.usda.gov (C.L. Afonso). Infection, Genetics and Evolution 12 (2012) 1770–1779 Contents lists available at SciVerse ScienceDirect Infection, Genetics and Evolution journal homepage: www.elsevier.com/locate/meegid