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, 95 (5), 2044-9

Multiple Evolutionary Origins of the Fungus Causing Panama Disease of Banana: Concordant Evidence From Nuclear and Mitochondrial Gene Genealogies

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Multiple Evolutionary Origins of the Fungus Causing Panama Disease of Banana: Concordant Evidence From Nuclear and Mitochondrial Gene Genealogies

K O'Donnell et al. Proc Natl Acad Sci U S A.

Abstract

Panama disease of banana, caused by the fungus Fusarium oxysporum f. sp. cubense, is a serious constraint both to the commercial production of banana and cultivation for subsistence agriculture. Previous work has indicated that F. oxysporum f. sp. cubense consists of several clonal lineages that may be genetically distant. In this study we tested whether lineages of the Panama disease pathogen have a monophyletic origin by comparing DNA sequences of nuclear and mitochondrial genes. DNA sequences were obtained for translation elongation factor 1alpha and the mitochondrial small subunit ribosomal RNA genes for F. oxysporum strains from banana, pathogenic strains from other hosts and putatively nonpathogenic isolates of F. oxysporum. Cladograms for the two genes were highly concordant and a partition-homogeneity test indicated the two datasets could be combined. The tree inferred from the combined dataset resolved five lineages corresponding to "F. oxysporum f. sp. cubense" with a large dichotomy between two taxa represented by strains most commonly isolated from bananas with Panama disease. The results also demonstrate that the latter two taxa have significantly different chromosome numbers. F. oxysporum isolates collected as nonpathogenic or pathogenic to other hosts that have very similar or identical elongation factor 1alpha and mitochondrial small subunit genotypes as banana pathogens were shown to cause little or no disease on banana. Taken together, these results indicate Panama disease of banana is caused by fungi with independent evolutionary origins.

Figures

Figure 1
Figure 1
(A) Distribution of phylogenetically informative nucleotide positions across the EF-1α gene exons and introns. Each bar represents the number of steps (= base substitutions) per 10-bp interval traced by macclade (22) from the MPT (Fig. 2A) for the 36 taxa studied. The two arrows identify the only informative substitutions within exons. (B) Map of the region of the EF-1α gene sequenced showing exons and introns. Numbered half-arrows indicate the position of PCR and sequencing primers. Degenerate oligonucleotide primers used for PCR were based on conserved nucleotide sequences in the EF-1α gene shared by the filamentous fungi Trichoderma reesei and Histoplasma capsulatum (GenBank accession nos. Z23012 and U14100).
Figure 2
Figure 2
Concordance of single most-parsimonious cladograms inferred from individual (A) EF-1α gene and (B) mtSSU rDNA datasets for the F. oxysporum complex rooted by the outgroup method. Bootstrap replication frequencies >50% and decay indices (in parentheses) are indicated above nodes. Edge length is indicated below nodes and branches. The node subtending the two major subclades resolved by each dataset is indicated with bold lines.
Figure 3
Figure 3
Single most-parsimonious phylogram by parsimony branch-and-bound search implemented in paup (18) based on the combined EF-1α gene and mtSSU rDNA dataset for the F. oxysporum complex rooted with sequences from Fusarium sp. NRRL 22903 and 25184. Numbering of the five clonal lineages (C1-C5) of “F. oxysporum f. sp. cubense” is according to the frequency with which each has been recovered from diseased bananas (6). The number of strains sequenced from each of the five clonal lineages is indicated in parentheses. Bootstrap values (1,000 replications) are indicated above nodes. Decay indices calculated with treerot (21) are indicated below nodes.
Figure 4
Figure 4
Frequency distribution histogram for chromosome number from strains assigned to clonal lineage C1 or C2 of F. oxysporum f. sp. cubense. Chromosome number estimates were made as previously described (11). Strains were assigned to lineages on the basis of corresponding VCGs as described in the text.

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