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The evolutionary history of cytochrome P450 genes in four filamentous Ascomycetes.

Deng J, Carbone I, Dean RA - BMC Evol. Biol. (2007)

Bottom Line: To resolve conflicting results between different clustering analyses and standard family designation, a higher order relationship was formulated. 376 genes were clustered into 115 clans.MG experienced more genes and clans gains compared to the other fungi.The exception was the NC lineage, which exhibited pure P450 gene loss.

View Article: PubMed Central - HTML - PubMed

Affiliation: Center for Integrated Fungal Research, North Carolina State University, Raleigh, NC 27695, USA. dengj@email.unc.edu <dengj@email.unc.edu>

ABSTRACT

Background: The Cytochrome P450 system is important in fungal evolution for adapting to novel ecological niches. To elucidate the evolutionary process of cytochrome P450 genes in fungi with different life styles, we studied the patterns of gene gains and losses in the genomes of four filamentous Ascomycetes, including two saprotrophs (Aspergillus nidulans (AN) and Neurospora crassa (NC)) and two plant pathogens (Fusarium graminearum (FG) and Magnaporthe grisea (MG)).

Results: A total of 376 P450 genes were assigned to 168 families according to standard nomenclature. On average, only 1 to 2 genes per family were in each genome. To resolve conflicting results between different clustering analyses and standard family designation, a higher order relationship was formulated. 376 genes were clustered into 115 clans. Subsequently a novel approach based on parsimony was developed to build the evolutionary models. Based on these analyses, a core of 30 distinct clans of P450s was defined. The core clans experienced contraction in all four fungal lineages while new clans expanded in all with exception of NC. MG experienced more genes and clans gains compared to the other fungi. Parsimonious analyses unanimously supported one species topology for the four fungi.

Conclusion: The four studied fungi exhibit unprecedented diversity in their P450omes in terms of coding sequence, intron-exon structures and genome locations, suggesting a complicated evolutionary history of P450s in filamentous Ascomycetes. Clan classification and a novel strategy were developed to study evolutionary history. Contraction of core clans and expansion of novel clans were identified. The exception was the NC lineage, which exhibited pure P450 gene loss.

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Three possible unrooted species tree of the four filamentous Ascomycetes and their support by different analyses. Steps refer to the fewest total number of state changes of all characters required for a particular tree topology. Compatible characters refer to the number of characters compatible with a particular tree topology (the number of steps for a compatible character equals to the minimum value for a particular tree topology compared to other topologies). Reconcile cost refers to the sum of reconcile cost for a particular tree topology as described in the text. The percentage under the classical genes refers to the bootstrap support.
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Figure 3: Three possible unrooted species tree of the four filamentous Ascomycetes and their support by different analyses. Steps refer to the fewest total number of state changes of all characters required for a particular tree topology. Compatible characters refer to the number of characters compatible with a particular tree topology (the number of steps for a compatible character equals to the minimum value for a particular tree topology compared to other topologies). Reconcile cost refers to the sum of reconcile cost for a particular tree topology as described in the text. The percentage under the classical genes refers to the bootstrap support.

Mentions: For four taxa there are three possible unrooted trees (Figure 3). The species tree topology constructed by the MP algorithm based on character data matrix derived from standard family clustering, clan clustering and COGs clustering unanimously support tree 1 (Figure 3). In a recent comprehensive analysis, this tree is supported by the evaluation of 25 genes in 33 fungal species [14]. The monophyletic relationship of the Pyrenomycetes was supported by phylogenies constructed using 75 randomly selected sets of 20 concatenated genes[15]. Based on this topology, AN, a Plectomycetes, is first split from the other Pyrenomycetes. Within the three Pyrenomycetes, FG split from the common ancestor of MG and NC. This topology was also supported by results from our reconcile analyses (Figure 3). In total, 17 clans contained members from all four species. Reconciling each of the 17 genes trees to each of the three species tree topology resulted in three cost values for each clan corresponding to each species tree topology. Summing the cost value for each species tree topology across all 17 clans provided the total cost for each species tree. Tree 1 resulted in the least cost among the three topologies (Figure 3). However, species trees constructed using sequences of three classical genes, 18S rRNA, α tubulin and elongation factor 2 did not uniformly support a particular topology (Figure 3). Among the trees constructed from DNA or protein sequences of each of the 3 genes and 3 different tree construction methods, all three possible unrooted trees obtained support from at least one gene combined with one method. However, in many cases the bootstrap support was very weak. In the only three cases were bootstrap values more than 95%, two supported tree 2 and 1 supported tree 1, our preferred topology. Interestingly, in many cases using DNA sequence and protein sequence for the same gene resulted in different supported trees. Regardless of the inconsistent results using individual genes, additional analyses were conducted using tree 1, the phylogeny supported by all parsimonious analyses results using P450s.


The evolutionary history of cytochrome P450 genes in four filamentous Ascomycetes.

Deng J, Carbone I, Dean RA - BMC Evol. Biol. (2007)

Three possible unrooted species tree of the four filamentous Ascomycetes and their support by different analyses. Steps refer to the fewest total number of state changes of all characters required for a particular tree topology. Compatible characters refer to the number of characters compatible with a particular tree topology (the number of steps for a compatible character equals to the minimum value for a particular tree topology compared to other topologies). Reconcile cost refers to the sum of reconcile cost for a particular tree topology as described in the text. The percentage under the classical genes refers to the bootstrap support.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1828051&req=5

Figure 3: Three possible unrooted species tree of the four filamentous Ascomycetes and their support by different analyses. Steps refer to the fewest total number of state changes of all characters required for a particular tree topology. Compatible characters refer to the number of characters compatible with a particular tree topology (the number of steps for a compatible character equals to the minimum value for a particular tree topology compared to other topologies). Reconcile cost refers to the sum of reconcile cost for a particular tree topology as described in the text. The percentage under the classical genes refers to the bootstrap support.
Mentions: For four taxa there are three possible unrooted trees (Figure 3). The species tree topology constructed by the MP algorithm based on character data matrix derived from standard family clustering, clan clustering and COGs clustering unanimously support tree 1 (Figure 3). In a recent comprehensive analysis, this tree is supported by the evaluation of 25 genes in 33 fungal species [14]. The monophyletic relationship of the Pyrenomycetes was supported by phylogenies constructed using 75 randomly selected sets of 20 concatenated genes[15]. Based on this topology, AN, a Plectomycetes, is first split from the other Pyrenomycetes. Within the three Pyrenomycetes, FG split from the common ancestor of MG and NC. This topology was also supported by results from our reconcile analyses (Figure 3). In total, 17 clans contained members from all four species. Reconciling each of the 17 genes trees to each of the three species tree topology resulted in three cost values for each clan corresponding to each species tree topology. Summing the cost value for each species tree topology across all 17 clans provided the total cost for each species tree. Tree 1 resulted in the least cost among the three topologies (Figure 3). However, species trees constructed using sequences of three classical genes, 18S rRNA, α tubulin and elongation factor 2 did not uniformly support a particular topology (Figure 3). Among the trees constructed from DNA or protein sequences of each of the 3 genes and 3 different tree construction methods, all three possible unrooted trees obtained support from at least one gene combined with one method. However, in many cases the bootstrap support was very weak. In the only three cases were bootstrap values more than 95%, two supported tree 2 and 1 supported tree 1, our preferred topology. Interestingly, in many cases using DNA sequence and protein sequence for the same gene resulted in different supported trees. Regardless of the inconsistent results using individual genes, additional analyses were conducted using tree 1, the phylogeny supported by all parsimonious analyses results using P450s.

Bottom Line: To resolve conflicting results between different clustering analyses and standard family designation, a higher order relationship was formulated. 376 genes were clustered into 115 clans.MG experienced more genes and clans gains compared to the other fungi.The exception was the NC lineage, which exhibited pure P450 gene loss.

View Article: PubMed Central - HTML - PubMed

Affiliation: Center for Integrated Fungal Research, North Carolina State University, Raleigh, NC 27695, USA. dengj@email.unc.edu <dengj@email.unc.edu>

ABSTRACT

Background: The Cytochrome P450 system is important in fungal evolution for adapting to novel ecological niches. To elucidate the evolutionary process of cytochrome P450 genes in fungi with different life styles, we studied the patterns of gene gains and losses in the genomes of four filamentous Ascomycetes, including two saprotrophs (Aspergillus nidulans (AN) and Neurospora crassa (NC)) and two plant pathogens (Fusarium graminearum (FG) and Magnaporthe grisea (MG)).

Results: A total of 376 P450 genes were assigned to 168 families according to standard nomenclature. On average, only 1 to 2 genes per family were in each genome. To resolve conflicting results between different clustering analyses and standard family designation, a higher order relationship was formulated. 376 genes were clustered into 115 clans. Subsequently a novel approach based on parsimony was developed to build the evolutionary models. Based on these analyses, a core of 30 distinct clans of P450s was defined. The core clans experienced contraction in all four fungal lineages while new clans expanded in all with exception of NC. MG experienced more genes and clans gains compared to the other fungi. Parsimonious analyses unanimously supported one species topology for the four fungi.

Conclusion: The four studied fungi exhibit unprecedented diversity in their P450omes in terms of coding sequence, intron-exon structures and genome locations, suggesting a complicated evolutionary history of P450s in filamentous Ascomycetes. Clan classification and a novel strategy were developed to study evolutionary history. Contraction of core clans and expansion of novel clans were identified. The exception was the NC lineage, which exhibited pure P450 gene loss.

Show MeSH
Related in: MedlinePlus