Evolutionary history of the ancient cutinase family in five filamentous Ascomycetes reveals differential gene duplications and losses and in Magnaporthe grisea shows evidence of sub- and neo-functionalization.

* The cuticle is the first barrier for fungi that parasitize plants systematically or opportunistically. Here, the evolutionary history is reported of the multimembered cutinase families of the plant pathogenic Ascomycetes Magnaporthe grisea, Fusarium graminearum and Botrytis cinerea and the saprotrophic Ascomycetes Aspergillus nidulans and Neurospora crassa. * Molecular taxonomy of all fungal cutinases demonstrates a clear division into two ancient subfamilies. No evidence was found for lateral gene transfer from prokaryotes. The cutinases in the five Ascomycetes show significant copy number variation, they form six clades and their extreme sequence diversity is highlighted by the lack of consensus intron. The average ratio of gene duplication to loss is 2 : 3, with the exception of M. grisea and N. crassa, which exhibit extreme family expansion and contraction, respectively. * Detailed transcript profiling in vivo, categorizes the M. grisea cutinases into four regulatory patterns. Symmetric or asymmetric expression profiles of phylogenetically related cutinase genes suggest subfunctionalization and neofunctionalization, respectively. * The cutinase family-size per fungal species is discussed in relation to genome characteristics and lifestyle. The ancestry of the cutinase gene family, together with the expression divergence of its individual members provides a first insight into the drivers for niche differentiation in fungi.

The amphioxus genome and the evolution of the chordate karyotype.

Lancelets ('amphioxus') are the modern survivors of an ancient chordate lineage, with a fossil record dating back to the Cambrian period. Here we describe the structure and gene content of the highly polymorphic approximately 520-megabase genome of the Florida lancelet Branchiostoma floridae, and analyse it in the context of chordate evolution. Whole-genome comparisons illuminate the murky relationships among the three chordate groups (tunicates, lancelets and vertebrates), and allow not only reconstruction of the gene complement of the last common chordate ancestor but also partial reconstruction of its genomic organization, as well as a description of two genome-wide duplications and subsequent reorganizations in the vertebrate lineage. These genome-scale events shaped the vertebrate genome and provided additional genetic variation for exploitation during vertebrate evolution.

Diversifying and purifying selection in the peptide binding region of DRB in mammals.

The class II genes of the major histocompatibility complex encode proteins which play a crucial role in antigen presentation. They are among the most polymorphic proteins known, and this polymorphism is thought to be the result of natural selection. To understand the selective pressure acting on the protein and to examine possible differences in the evolutionary dynamics among species, we apply maximum likelihood models of codon substitution to analyze the DRB genes of six mammalian species: human, chimpanzee, macaque, tamarin, dog, and cow. The models account for variable selective pressures across codons in the gene and have the power to detect amino acid residues under either positive or negative selection. Our analysis detected positive selection in the DRB genes in each of the six mammals examined. Comparison with structural data reveals that almost all amino acid residues inferred to be under positive selection in humans are in the peptide binding region (PBR) and are in contact with the antigen side chains, although residues outside of but close to the PBR are also detected. Strong purifying selection is also detected in the PBR, at sites which contact the antigen and at sites which may be involved in dimerization or T cell binding. The analysis demonstrates the utility of the random-sites analysis even when structural information is available. The different mammalian species are found to share many positively or negatively selected sites, suggesting that their functional roles have remained very similar in the different species, despite the different habitats and pathogens of the species.

The fate of gene duplicates in the genomes of fungal pathogens.

Understanding how molecular changes underlie phenotypic variation within and between species is one of the main goals of evolutionary biology and comparative genetics. The recent proliferation of sequenced fungal genomes offers a unique opportunity to start elucidating the extreme phenotypic diversity in the Kingdom Fungi.1-4 We attempted to investigate the contribution of gene families to the evolutionary forces shaping the diversity of pathogenic lifestyles among the fungi.5 We studied a family of secreted enzymes which is present and expanded in all genomes of fungal pathogens sequenced to date and absent from the genomes of true yeasts.3,4 This family of cutinases6 predates the division between the two major fungal phyla, Ascomycota and Basidiomycota.5 We discuss our molecular phylogenetic analyses, the number and sequence diversity, and gene gains and losses of cutinase family members between five Ascomycetes: the phytopathogens Magnaporthe oryzae, Fusarium graminearum and Botrytis cinerea; and the model organisms Neurospora crassa and Aspergillus nidulans.5 The functional characterization of three members of the M. oryzae cutinase family,6-10 coupled with the regulatory subfunctionalization and neofunctionalization of most gene pairs5 provide the first justification for the retention of paralogs after duplication and for gene redundancy in the genomes of fungal pathogens.

ParaHox cluster evolution--hagfish and beyond.

Abstract The ParaHox genes comprise three Hox-related homeobox gene families, found throughout the animals. They were first discovered in the invertebrate chordate amphioxus, where they are tightly clustered. In this paper we carry out a comparative review of ParaHox gene cluster organization among the deuterostomes, and discuss how the recently published hagfish ParaHox clusters fit into current theories about the evolution of this group of genes.

A degenerate ParaHox gene cluster in a degenerate vertebrate.

The ParaHox genes consist of 3 homeobox gene families, Gsx, Xlox, and Cdx, all of which have fundamental roles in development. Xlox (known as IPF1 or PDX1 in vertebrates), for example, is crucial for development of the vertebrate pancreas and is also involved in regulation of insulin expression. The invertebrate amphioxus has a gene cluster containing one gene from each of the gene families, whereas in all vertebrates examined to date there are additional copies resultant from ParaHox gene cluster duplications at the base of the vertebrate lineage. Extant vertebrates basal to bony and cartilaginous fish are central to the question of when and how these multiple genes arose in the vertebrate genome. Here, we report the mapping of a ParaHox gene cluster in 2 species of hagfishes. Unexpectedly, these basal vertebrates have lost a functional Xlox gene from this cluster, unlike every other vertebrate examined to date. Furthermore, our phylogenetic analyses suggest that hagfishes may have diverged from the vertebrate lineage before the duplications, which created the multiple ParaHox clusters in jawed vertebrates.

Vertebrate neurogenin evolution: long-term maintenance of redundant duplicates.

The majority of the cranial sensory neurons of vertebrates, including all of those concerned with the special senses of hearing, balance and taste, are derived from the neurogenic placodes. A number of studies have shown that the production of neuronal cells by the placodes is dependent upon the function of the neurogenin (ngn) gene family of basic helix-loop-helix transcription factors. One member of the gene family is expressed in each placode, suggesting that this specificity of expression could help to determine different neuronal classes. An interesting feature of this expression, however, is that the expression patterns vary amongst the vertebrates; for example, mammals and fish express ngn-1 in the ophthalmic trigeminal placode where birds use ngn-2. This prompted us to use phylogenetic and genomic analysis to unravel the evolutionary history of this gene family. We determined that the duplication that created the neurogenin-1 and -2 subfamilies occurred deep in the vertebrate lineage before the divergence of bony fish 450 million years ago and suggest that concurrent expression of both genes was probably maintained in all neurogenic placodes until after the divergence of birds and mammals 270 million years ago.

Insights into vertebrate evolution from the chicken genome sequence.

The chicken has recently joined the ever-growing list of fully sequenced animal genomes. Its unique features include expanded gene families involved in egg and feather production as well as more surprising large families, such as those for olfactory receptors. Comparisons with other vertebrate genomes move us closer to defining a set of essential vertebrate genes.

An antecedent of the MHC-linked genomic region in amphioxus.

The MHC genes on human chromosome 6 are located within one of the best-characterised paralogy regions of the human genome. Numerous genes mapping around this location, 6p21, have paralogues at one, two or three other chromosomal locations on HSA 1, 9 and 19. The similarity between these four chromosomal regions suggests the linkages may have adaptive significance, and/or they may be echoes of segmental or genome duplication in human ancestry. Here, we show that six amphioxus cosmids, containing genes orthologous to those from the human MHC-linked paralogy regions, map to a single amphioxus chromosome. The composition of the MHC-linked genomic region, therefore, pre-dates vertebrate origins.

Bayesian phylogenetic analysis supports monophyly of ambulacraria and of cyclostomes.

Vertebrates are part of the phylum Chordata, itself part of a three-phylum group known as the deuterostomes. Despite extensive phylogenetic analysis of the deuterostome animals, several unresolved relationships remain. These include the relationship between the three deuterostome phyla (chordates, echinoderms and hemichordates), and the monophyletic or paraphyletic origin of the cyclostomes (hagfish and lampreys). Using robust Bayesian statistical analysis of 18S ribosomal DNA, mitochondrial genes and nuclear protein-coding DNA, we find strong support for a hemichordate-echinoderm clade, and for monophyly of the cyclostomes.

Were vertebrates octoploid?

It has long been suggested that gene and genome duplication play important roles in the evolution of organismal complexity. For example, work by Ohno proposed that two rounds of whole genome doubling (tetraploidy) occurred during the evolution of vertebrates: the extra genes permitting an increase in physiological and anatomical complexity. Several modifications of this 'two tetraploidies' hypothesis have been proposed, taking into account accumulating data, and there is wide acceptance of the basic scheme. In the past few years, however, several authors have raised doubts, citing lack of direct support or even evidence to the contrary. Here, we review the evidence for and against the occurrence of tetraploidies in early vertebrate evolution, and present a new compilation of molecular phylogenetic data for amphioxus. We argue that evidence in favour of tetraploidy, based primarily on genome and gene family analyses, is strong. Furthermore, we show that two observations used as evidence against genome duplication are in fact compatible with the hypothesis: but only if the genome doubling occurred by two closely spaced sequential rounds of autotetraploidy. We propose that early vertebrates passed through an autoautooctoploid phase in the evolution of their genomes.