Analyses of genotypic diversity among North, South, and Central American isolates of sugarcane yellow leaf virus: evidence for Colombian origins and for intraspecific spatial phylogenetic variation

Abstract

We have analyzed the genotypic diversity of sugarcane yellow leaf virus (SCYLV) collected from North, South, and Central America by fingerprinting assays and selective cDNA cloning and sequencing. One group of isolates from Colombia, designated the C-population, has been identified as residing at the root node between a separable superpopulation structure of SCYLV and other members of the family Luteoviridae, indicating that the progenitor viruses of the North, South, and Central American isolates of the SCYLV superpopulation most likely arose from a C-population structure. From a model of intrafamilial evolution (F. Moonan et al., Virology 269:156-171, 2000), a prediction could be made that within the SCYLV species, the capacity of genomic sequence divergence would range from lowest in the capsid protein open reading frame 3 (ORF 3) to highest in a region spanning across the carboxy-terminal end of the RNA-dependent RNA polymerase ORF. We have demonstrated the validity and applicability of this intrafamilial model for the prediction of intraspecies SCYLV diversity. Analysis of spatial phylogenetic variation (SPV) within the SCYLV isolates could not be assessed by application of a "partial likelihoods assessed through optimization" (PLATO)-derived intraspecies model alone. However, application of a PLATO-derived intrafamilial model with the intraspecies-derived model allowed distinction of three forms of SPV. Two of the SPV forms identified correspond to the extremes in a continuum of sequence evolution displayed in a SCYLV superpopulation structure, and the third form was diagnostic of a C-population structure. The application of these types of models has value in terms of predicting the types of SCYLV intraspecies diversity that may exist worldwide, and in general, may be useful in application for more informed design of transgenes for use in the elicitation of homology-dependent virus resistance mechanisms in transgenic plants.

FIG. 1.

Phylogenetic relationships assessed with both a UPGMA dendrogram derived from fingerprinting data (A) and phylograms derived from nucleotide (B and C) and deduced peptide (D and E) data. The designations of the isolates and the origins of the sequence or fingerprint data used in the diagrams are given in Table 1. Nucleotide sequence alignments were analyzed with the F84 phylogenetic model of DNAml of the PHYLIP package, and deduced peptide sequence alignments were analyzed with the maximum-likelihood based quartet puzzling method of PUZZLE. The nucleotide sequence ranges analyzed for the isolate phylograms (B and C), respectively, correspond to nt 1518 to 4352 and nt 3144 to 4238 of the SCYLV-A genome described by Moonan et al. (36). Relationships between the deduced peptide sequences of RdRp ORF 2 of SCYLV are shown for both the complete RdRp peptide sequences (D) and a partial RdRp sequence corresponding to amino acid residue positions 471 to 572 of the RdRp of SCYLV-A (E).

FIG. 2.

Splitstree network diagram derived from nt 1518 to 4352 of the SCYLV-A genome, illustrating the most likely possible phylogenetic relationships between isolates of SCYLV. The network was produced in Splitstree from an HKY phylogenetic model produced with PAUP and corresponds to the data used to produce the DNAml phylogram illustrated in Fig. 1B. The designations of the isolates and the origins of the sequences used to produce the network are given in Table 1.

FIG. 3.

Splitstree network diagram derived from nt 1518 to 4352 of the SCYLV genome, illustrating the most likely phylogenetic relationships between the SCYLV isolates and other members of the family Luteoviridae. The network was produced in Splitstree from an HKY phylogenetic model produced with PAUP. The designations of the isolates and the origins of the SCYLV sequences used to produce the network are given in Table 1, and the origins of the Luteoviridae sequences are described in Moonan et al. (36). Isolate clusters formally designated as belonging to the Enamovirus, Polerovirus, and Luteovirus genera are encircled, as are the postulated superpopulation and C-population clusters of SCYLV. Within the network diagram, assignment of the B0 isolate of Maia et al. (29) (in diamond) is based on analyses of partial sequence information data shown in Fig. 1C and E, and assignment of other isolates of SCYLV to the superpopulation (in box) is based upon UPGMA analysis of fingerprint data, as shown in Fig. 1A.

FIG. 4.

Analysis of SPV in isolates of SCYLV from North, South, and Central America, corresponding to nt 1518 to 4352 of the SCYLV-A genome (A), and the tree topology types exhibited in this SPV (B). (A, top to bottom) Relative position of the clonal inserts used to derive the SCYLV sequences for this region; genomic organization of the SCYLV ORFs corresponding to this region, corresponding isolate data-derived PLATO output ranges shown as boxed ranges corresponding to the SCYLV genome; corresponding PLATO output ranges derived from an intrafamilial model; distribution of tree topologies corresponding to regions of SPV; and grouping of isolates into three groups (groups A, B, and C), corresponding to the exhibited patterns of SPV. The SCYLV-A genome used as a reference, the direct extrapolation of the PLATO intrafamilial analysis-based output, and a description of this method of SPV analysis are derived from Moonan et al. (36).