The present review focuses on the history of genes involved in the major histocompatibility complex (MHC), with a special emphasis on class I function in peptide presentation. The MHC class II story is covered in less detail, as it does not have a major impact on the general understanding of the MHC evolution. We first redefine the MHC as the definition evolved over time. We then use phylogenetic analysis to investigate the history of genes involved in the MHC class I process. As not all the genes involved in this process have been phylogenetically analyzed and because new sequences have been recently released in biological databases, we have re-investigated this matter. In the light of the phylogenetic analysis, the functions of the orthologs of the genes involved in MHC processes are examined in species not having an MHC system. We then demonstrate that the emergence of this new function is due to various levels of co-option.
The genomes of many higher organisms, including plants and bony fish, frequently undergo polyploidization, and it has long been hypothesized that these, and other, large-scale genomic duplications have played an important role in the major evolutionary transitions of our past. Here we build upon an early work to show that the human genomic region 8p11.21-8p21.3 has three paralogous regions on chromosomes 4, 5, and 10 that were produced by two rounds of duplications after the protostomian-deuterostomian split and before the actinopterygian-sarcopterygian split. We base our analysis on the phylogenetic reconstruction of the evolutionary history of 38 gene families located in these regions. Using an alignment centered on protein domains, three different phylogenetic methods, and divergence time estimation, this analysis gives more support in favor of two ancient polyploidization events in the vertebrate ancestral genome.
Achieving a better comprehension of the evolution of species has always been an important matter for evolutionary biologists. The deuterostome phylogeny has been described for many years, and three phyla are distinguishable: Echinodermata (including sea stars, sea urchins, etc…), Hemichordata (including acorn worms and pterobranchs), and Chordata (including urochordates, cephalochordates and extant vertebrates). Inside the Chordata phylum, the position of vertebrate species is quite unanimously accepted. Nonetheless, the position of urochordates in regard with vertebrates is still the subject of debate, and has even been suggested by some authors to be a separate phylum from cephalochordates and vertebrates. It was also the case for agnathans species -myxines and hagfish-for which phylogenetic evidence was recently given for a controversial monophyly. This raises the following question: which one of the cephalochordata or urochordata is the sister group of vertebrates and what are their relationships? In the present work, we analyzed 82 protein families presenting homologs between urochordata and other deuterostomes and focused on two points: 1) testing accurately the position of urochordata and cephalochordata phyla in regard with vertebrates as well as chordates monophyly, 2) performing an estimation of the rate of gene loss in the Ciona intestinalis genome. We showed that the urochordate phyla is the vertebrate sister group and that gene loss played a major role in structuring the urochordate genome.
The present day structure of the vertebrate major histocompatibility complex (MHC) and its three paralogous regions has always been a focus of interest. In a recent study, nine human anchor genes located in the MHC region were cloned from a Branchiostoma floridae (amphioxus) cosmid library. The identification and analysis of 31 surrounding genes led to the most probable model of two rounds of en bloc duplication giving rise to these regions. These events were estimated to have occurred after the cephalochordata-craniata divergence [approximately 766 million years ago (Mya)] and before the Gnathostomata radiation (approximately 528 Mya). Furthermore, it was also shown that after this large-scale duplication one of these regions, corresponding to the human 9q33-q34, had retained an ancestral organisation. In the present study, four new cosmids in the amphioxus proto-MHC region were identified by the chromosomal walking technique. These cosmids were sequenced, and their structural annotation was performed, leading to the prediction of eleven genes. Their phylogenetic relationships among species corroborate the results obtained previously and provide more evidence for the plesiomorphic state of the human chromosome 9q33-34 MHC paralogous region.
In Fig. 1B, the orientation of the cosmid MP-MGc117I0962Q6 (NCBI accession number AY246562) must be inverted, as must that of all of the genes. Consequently, the Neuraminidase-like 2 gene should overlap Neu on the RXR A,B,G cosmid, and MORN-like should overlap EC whose ortholog in humans is the gene C9ORF18 in 9q34.11. EC and MORN-like are exactly the same gene (100% identity) and should thus both be renamed C9ORF18-like. An updated version of the figure is available upon request and on our laboratory web site: http://www.up.univ-mrs.fr/evol/Supplement/Supplement-MHC/erratum.html.
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