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The evolutionary trajectory of the mating-type (mat) genes in Neurospora relates to reproductive behavior of taxa.

Wik L, Karlsson M, Johannesson H - BMC Evol. Biol. (2008)

Bottom Line: However, for fungal reproductive genes the question has remained whether the rapid evolution is a result of stochastic or deterministic processes.Lower selective constraints of mat-genes was found among homothallic than heterothallic taxa, and comparisons with non-reproductive genes argue that this disparity is not a nonspecific, genome-wide phenomenon.Our data show that the mat-genes evolve rapidly in Neurospora.

View Article: PubMed Central - HTML - PubMed

Affiliation: Uppsala University, Department of Evolutionary Biology, Norbyvägen 18D, SE-752 36 Uppsala, Sweden. lotta.wik@bvf.slu.se

ABSTRACT

Background: Comparative sequencing studies among a wide range of taxonomic groups, including fungi, have led to the discovery that reproductive genes evolve more rapidly than other genes. However, for fungal reproductive genes the question has remained whether the rapid evolution is a result of stochastic or deterministic processes. The mating-type (mat) genes constitute the master regulators of sexual reproduction in filamentous ascomycetes and here we present a study of the molecular evolution of the four mat-genes (mat a-1, mat A-1, mat A-2 and mat A-3) of 20 Neurospora taxa.

Results: We estimated nonsynonymous and synonymous substitution rates of genes to infer their evolutionary rate, and confirmed that the mat-genes evolve rapidly. Furthermore, the evolutionary trajectories are related to the reproductive modes of the taxa; likelihood methods revealed that positive selection acting on specific codons drives the diversity in heterothallic taxa, while among homothallic taxa the rapid evolution is due to a lack of selective constraint. The latter finding is supported by presence of stop codons and frame shift mutations disrupting the open reading frames of mat a-1, mat A-2 and mat A-3 in homothallic taxa. Lower selective constraints of mat-genes was found among homothallic than heterothallic taxa, and comparisons with non-reproductive genes argue that this disparity is not a nonspecific, genome-wide phenomenon.

Conclusion: Our data show that the mat-genes evolve rapidly in Neurospora. The rapid divergence is due to either adaptive evolution or lack of selective constraints, depending on the reproductive mode of the taxa. This is the first instance of positive selection acting on reproductive genes in the fungal kingdom, and illustrates how the evolutionary trajectory of reproductive genes can change after a switch in reproductive behaviour of an organism.

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Evolutionary relationship of the included taxa. Topology is constructed from previously reported topologies based on rDNA loci (28S, ITS), nuclear gene loci (Bml, ccg-7, mat a-1, mat A-1), and four anonymous nuclear loci [36-38, 46]. A cross indicates lineages where any of the ORFs is disrupted. A, B and C indicates intraspecific subgroups and PS1 through 3 phylogenetic species [46].
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Figure 1: Evolutionary relationship of the included taxa. Topology is constructed from previously reported topologies based on rDNA loci (28S, ITS), nuclear gene loci (Bml, ccg-7, mat a-1, mat A-1), and four anonymous nuclear loci [36-38, 46]. A cross indicates lineages where any of the ORFs is disrupted. A, B and C indicates intraspecific subgroups and PS1 through 3 phylogenetic species [46].

Mentions: In contrast to many yeast species [13], filamentous ascomycetes of either mating type are unable to switch to the opposite mating type. Nevertheless, it has been suggested that conversion from heterothallic to homothallic mode in filamentous ascomycetes resides within the mat locus, and that homothallic species carry both idiomorphs in a single thallus [14]. In so called pseudohomothallic species, represented in this study by Neurospora tetrasperma, two haploid nuclei of opposite mating-type (mat a and mat A) are maintained in each heterokaryotic ascospore progeny and vegetative cell, while in true homothallic species mat-genes from both idiomorphs are found within a single haploid genome. The structure of the mating type genes in homothallic Neurospora has not been determined in detail; however, hybridizations using cloned portions of the idiomorphs of N. crassa to the genome of related homothallic taxa have revealed three classes of homothallic taxa (Figure 1). The haploid genomes of one group contain both mat a and mat A sequences [15]. Another distinct group consists of taxa containing the entire mat A sequence, while the mat a-1 gene is absent [16,17]. Finally, the hybridization patterns of the homothallic N. terricola provide evidence for the presence of mat a-1, mat A-1 and mat A-2 sequences, but it appears to lack parts of the A-idiomorphic region corresponding to the mat A-3 region [15].


The evolutionary trajectory of the mating-type (mat) genes in Neurospora relates to reproductive behavior of taxa.

Wik L, Karlsson M, Johannesson H - BMC Evol. Biol. (2008)

Evolutionary relationship of the included taxa. Topology is constructed from previously reported topologies based on rDNA loci (28S, ITS), nuclear gene loci (Bml, ccg-7, mat a-1, mat A-1), and four anonymous nuclear loci [36-38, 46]. A cross indicates lineages where any of the ORFs is disrupted. A, B and C indicates intraspecific subgroups and PS1 through 3 phylogenetic species [46].
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2335104&req=5

Figure 1: Evolutionary relationship of the included taxa. Topology is constructed from previously reported topologies based on rDNA loci (28S, ITS), nuclear gene loci (Bml, ccg-7, mat a-1, mat A-1), and four anonymous nuclear loci [36-38, 46]. A cross indicates lineages where any of the ORFs is disrupted. A, B and C indicates intraspecific subgroups and PS1 through 3 phylogenetic species [46].
Mentions: In contrast to many yeast species [13], filamentous ascomycetes of either mating type are unable to switch to the opposite mating type. Nevertheless, it has been suggested that conversion from heterothallic to homothallic mode in filamentous ascomycetes resides within the mat locus, and that homothallic species carry both idiomorphs in a single thallus [14]. In so called pseudohomothallic species, represented in this study by Neurospora tetrasperma, two haploid nuclei of opposite mating-type (mat a and mat A) are maintained in each heterokaryotic ascospore progeny and vegetative cell, while in true homothallic species mat-genes from both idiomorphs are found within a single haploid genome. The structure of the mating type genes in homothallic Neurospora has not been determined in detail; however, hybridizations using cloned portions of the idiomorphs of N. crassa to the genome of related homothallic taxa have revealed three classes of homothallic taxa (Figure 1). The haploid genomes of one group contain both mat a and mat A sequences [15]. Another distinct group consists of taxa containing the entire mat A sequence, while the mat a-1 gene is absent [16,17]. Finally, the hybridization patterns of the homothallic N. terricola provide evidence for the presence of mat a-1, mat A-1 and mat A-2 sequences, but it appears to lack parts of the A-idiomorphic region corresponding to the mat A-3 region [15].

Bottom Line: However, for fungal reproductive genes the question has remained whether the rapid evolution is a result of stochastic or deterministic processes.Lower selective constraints of mat-genes was found among homothallic than heterothallic taxa, and comparisons with non-reproductive genes argue that this disparity is not a nonspecific, genome-wide phenomenon.Our data show that the mat-genes evolve rapidly in Neurospora.

View Article: PubMed Central - HTML - PubMed

Affiliation: Uppsala University, Department of Evolutionary Biology, Norbyvägen 18D, SE-752 36 Uppsala, Sweden. lotta.wik@bvf.slu.se

ABSTRACT

Background: Comparative sequencing studies among a wide range of taxonomic groups, including fungi, have led to the discovery that reproductive genes evolve more rapidly than other genes. However, for fungal reproductive genes the question has remained whether the rapid evolution is a result of stochastic or deterministic processes. The mating-type (mat) genes constitute the master regulators of sexual reproduction in filamentous ascomycetes and here we present a study of the molecular evolution of the four mat-genes (mat a-1, mat A-1, mat A-2 and mat A-3) of 20 Neurospora taxa.

Results: We estimated nonsynonymous and synonymous substitution rates of genes to infer their evolutionary rate, and confirmed that the mat-genes evolve rapidly. Furthermore, the evolutionary trajectories are related to the reproductive modes of the taxa; likelihood methods revealed that positive selection acting on specific codons drives the diversity in heterothallic taxa, while among homothallic taxa the rapid evolution is due to a lack of selective constraint. The latter finding is supported by presence of stop codons and frame shift mutations disrupting the open reading frames of mat a-1, mat A-2 and mat A-3 in homothallic taxa. Lower selective constraints of mat-genes was found among homothallic than heterothallic taxa, and comparisons with non-reproductive genes argue that this disparity is not a nonspecific, genome-wide phenomenon.

Conclusion: Our data show that the mat-genes evolve rapidly in Neurospora. The rapid divergence is due to either adaptive evolution or lack of selective constraints, depending on the reproductive mode of the taxa. This is the first instance of positive selection acting on reproductive genes in the fungal kingdom, and illustrates how the evolutionary trajectory of reproductive genes can change after a switch in reproductive behaviour of an organism.

Show MeSH
Related in: MedlinePlus